The effects of dietary supplementation with ellagic acid on the growth performance, nutrient apparent metabolic rate, slaughter performance, and fecal microbiota diversity of young pigeons

The purpose of this study was to evaluate the effects of ellagic acid (EA) supplementation on growth performance, apparent metabolic rate of nutrients, slaughter characteristics, and fecal flora diversity in American King Pigeons. As a natural polyphenolic compound, EA has potential application prospects in livestock and poultry breeding due to its multiple biological activities. This study aims to clarify the suitable supplementation level of EA in the diet of meat pigeons, so as to provide a theoretical basis for its rational application. A total of 192 29-day-old American King Pigeons, weighing 470 ± 10 g with equal numbers of males and females, were selected. The pigeons were randomly divided into four groups, with 6 replicates per group and 8 pigeons per replicate. The control group was fed a basal diet, while the test groups I, II, and III were supplemented with EA at 100 mg/kg, 200 mg/kg, and 400 mg/kg respectively. The experiment included a 4-day prefeeding period followed by a 28-day formal experimental period. Relevant indicators were determined after the formal period, and data were statistically analyzed with P < 0.05 considered significant. In terms of growth performance, the chest width and tibia length of test group III were significantlyhigher than those of other groups (P < 0.05), and the chest depth of test group III was significantly higher than that of test groups III and II (P < 0.05). For slaughter performance, the leg muscle weight and gizzard weight of test group III were significantly higher than those of the control group (P < 0.05), and the thymus weight and index of test group I were significantly higher than those of the control group (P < 0.05). Regarding immune cytokines, the GSH-Px activity of test group I was significantly higher than that of the control group (P < 0.05), the MDA content of test group III was significantly lower than that of the control group (P < 0.05), and the immunoglobulin IgA levels of test groups I and II were significantly higher than that of the control group (P < 0.05). For nitrogen metabolism and liver function indexes, the TP content of test group I was significantly higher than that of the control group (P < 0.05), and the AST activity of test group III was significantly lower than that of the control group (P < 0.05). As for fecal flora diversity, 200 mg/kg EA supplementation was beneficial to maintaining the richness and stability of intestinal microflora. In conclusion, adding ellagic acid to the diet can improve the growth performance, immunity, total protein level, and intestinal microflora stability of American King Pigeons. Different doses of EA exert specific effects: high dose (400 mg/kg) is superior in body size development and muscle deposition, low dose (100 mg/kg) focuses on immune enhancement, while medium dose (200 mg/kg) shows the most significant comprehensive effect. Therefore, 200 mg/kg is the suitable EA supplementation level for American King Pigeons.

1 Introduction

Squabs typically refer to pigeons aged between 29 and 60 days that have left their parents and are transitioning to independent breeding (Liang et al., 2025). This period represents a critical stage of growth and development, during which their digestive system is still immature, with insufficient digestive enzyme secretion and underdeveloped intestinal villi, limiting their ability to effectively digest and absorb feed (Shan et al., 2019). Additionally, squabs undergo a significant transition from reliance on parental milk to self-feeding. Pigeons’ milk is rich in immune factors, and during early life, their immunity is primarily supported by maternal antibodies (Li et al., 2012). However, when squabs become young pigeons, they lose this maternal antibody protection, and their immature immune systems make them vulnerable. Moreover, a series of environmental stresses, such as leaving their parents, beginning self-feeding, and changes in housing and feed, negatively affect their health (Yang et al., 2010). Therefore, identifying a green, safe, and effective feed additive has become a viable solution to address these challenges. Ellagic acid (EA), as a novel, safe, and eco-friendly additive, offers potential benefits in enhancing animal growth performance, promoting nutrient absorption, and modulating gut microbiota (Wang, 2023). Xiao showed that EA protects against oxidative damage induced by paraquat in piglets, enhances intestinal barrier integrity, and alleviates systemic oxidative stress through the Nrf2 pathway (Xiao et al., 2022). Wang’s research found that by adding appropriate amount of ellagic acid to the feed, the oxidative stress of broilers can be alleviated, and the contents of serum total protein and albumin can be significantly increased (Wang et al., 2025). Chen found that oral administration of EA increases plasma total protein levels and reduces plasma total bilirubin levels (Chen et al., 2024). Liu found that by adding ellagic acid to the feed, it was found that ellagic acid could adjust the intestinal flora structure of ewes, significantly increase the abundance of beneficial bacteria such as Bifidobacterium and lactic acid bacteria, and reduce the proportion of harmful bacteria such as Escherichia coli and Salmonella. The Shannon and Simpson indices of flora increased significantly, and the intestinal microecological environment became more stable (Liu, 2025).

Although EA has a good protective effect on other livestock and poultry species (such as piglets, broilers and ewes), there is still a key research gap: there is no research focusing on the application of EA in young pigeons during the critical parental separation and nutritional transition period. The existing research on EA has not solved the unique physiological challenges of young pigeons at this stage (such as immature digestion, maternal immunity decline and combined environmental pressure), nor has it explored whether EA can alleviate these challenges to improve the health and production performance of young pigeons. This lack of targeted research hinders the rational application of EA in pigeon breeding industry, especially in the critical period of pigeon’s transition to independence. Based on the above research gaps, this study assumes that: Adding EA to the diet will improve the growth performance and apparent digestibility of nutrients of young pigeons during the transition period of 29–60 days by enhancing digestive function; Supplementing EA will reduce oxidative stress and improve the slaughter performance of young pigeons by regulating serum biochemical indices related to nutritional metabolism and immunity; EA can adjust the composition of fecal microflora of young pigeons, increase the abundance of beneficial bacteria and reduce harmful bacteria, thus stabilizing the intestinal microecological environment. In order to test these hypotheses, this study discussed the effects of different dietary e a levels on the growth performance, apparent nutritional metabolism, slaughter characteristics and fecal microbial diversity of young pigeons, aiming at providing scientific basis for the rational application of EA in pigeon feeding and determining its optimal addition level, so as to enhance the health of young pigeons in the critical transition period.

2 Materials and methods

2.1 Ethical considerations

The animal protocols for this study were approved by the Laboratory Animal Welfare Ethics Committee of Xinjiang Agricultural University (Protocol No. 2023008). The research was conducted at Moyu Blue Sea Pigeon Industry Co., Ltd., Hetian, Xinjiang, China, from September to October 2023.

2.2 Animals and experimental design

The Test group employed a single-factor randomized trial design, selecting 29-day-old American King pigeons. A total of 192 pigeons, with similar weight and good physical condition (471.00 ± 9.95 g), were randomly assigned to four groups, each with six replicates, and eight pigeons per replicate. The basic diet composition in each test group was the same, and the addition levels of ellagic acid in the test group were 100 mg/kg, 200 mg/kg and 400 mg/kg respectively. The pre-feeding period lasted for 4 days, followed by a formal experimental period of 28 days. The birds were housed in individual cages with a standard cage size of 45 cm × 50 cm × 60 cm, placed centrally in a vertical arrangement. The basic diet used was a routine self-use formula prepared by Mo Yuxian Blue Sea Pigeon Industry Development Co., Ltd. Based on its own breeding experience and the physiological characteristics of King Pigeon. The raw material composition (corn 51.91%, DM: 87.00; CP: 8.50; EE: 4.00; CF:2.20; NFE: 72.10; Ca: 0.04; P: 0.28; soybean meal 30.00%,DM: 89.00; CP: 44.50; EE: 2.00; CF: 5.00; NFE: 35.00; Ca: 0.30; P: 0.55; bran 2.86%,DM: 88.00; CP: 15.00; EE: 3.50; CF: 10.00; NFE: 57.50; Ca: 0.15; P: 1.10. etc.) and nutritional level (crude protein 17.5%, metabolic energy 14.15 MJ/kg, etc.) of the basic diet used in the test group are all mature formulas that have been used for a long time in the cage culture mode of meat pigeons and verified to be effective, which could ensure the stable basic nutritional supply of young pigeons during the experiment, reduced the feeding stress caused by the strangeness of the formula, and reflected the real impact of ellagic acid addition on the experimental indicators more accurately. The level of EA supplementation in the experiment (on the basis of Table 1, ellagic acid is added at 100,200 and 400 mg/kg per kg of feed) is closely related to the verification range in poultry and livestock nutrition research, especially for growth performance, antioxidant capacity and intestinal health. Reference king’s experimental design (Wang, 2023). The pigeons were vaccinated according to the field immunization program. The Test group took place in an open pigeon house, with designated personnel responsible for feeding and testing. Prior to the experiment, the pigeon house was thoroughly cleaned and disinfected, and routine disinfection procedures were followed throughout the study. Material boxes and water cups were checked daily to ensure cleanliness, allowing the pigeons to feed and drink freely throughout the experiment. The feeding amount for the next day was adjusted based on the remaining feed from the previous day. Artificial lighting duration was adjusted according to the pigeons’ age, with natural ventilation combined with positive pressure ventilation used for airflow management. Feeding times were standardized to align with those of the pigeon farm.

Table 1

Table 1. Composition and nutrient level of basic diets (air-dry foundation).

2.3 Sample collection

2.3.1 Collection of growth performance data

On the 0th, 7th, 14th, 21st, and 28th days of the experiment, the fasting body weight (g) of the pigeons was measured using an electronic balance (Mettler-Toledo, Gryffindor, Switzerland) AL204 electronic balance with an accuracy of 0.1 mg). Feed intake and feed intake and feed conversion. Chest depth (cm) and chest width were measured using a vernier caliper (INSIZE vernier caliper (Suzhou, China), 0–150 mm, accuracy 0.02 mm.) on the 0th and 30th days. Keel length (cm), body oblique length (cm), and tibia circumference (cm) were measured using a tape measure (Great Wall mild steel tape measure (Ningbo, China), with a range of 0–200 cm and an accuracy of 1 mm).

2.3.2 Blood sample collection

At 09:00 am on the 28th day of the experiment, 16 pigeons in each group were randomly collected from the inferior pterygoid vein on an empty stomach, and 2 mL of blood was collected from the inferior pterygoid vein into the blood collection tube, centrifuged at 3500 r/min for 15 min, and serum was collected. After the blood in the centrifuge tube is allowed to stand for 2 h at room temperature, it will stay overnight in the refrigerator at 4 C. After the serum is separated out, it will be centrifuged at 4000 r/min for 20 min, and the serum will be sucked up and placed in a 1.5 mL centrifuge tube. Then the separated serum will be centrifuged at the same speed for 20 min, and the precipitation will be discarded, and the sub-package label will be-80 C for later use.

2.3.3 Collection of slaughtered organs

When the squabs reached 60 days of age, one pigeon was selected from each replicate, totaling 24 pigeons. These pigeons underwent a fasting stage for 12 hours before slaughter. They were then subjected to lethal bloodletting, feathering, and organ collection, with the attached fat removed from the organs.

2.3.4 Collection of digestive and metabolic samples

Feces were collected from the cage units over a 5-day period before the trial concluded. Pre-weighed and appropriately sized dung plates were placed in plastic bags and positioned under the cages. Feces were collected daily one hour before feeding, with any impurities (such as feathers and feed) removed during collection. The collected fecal samples were mixed, weighed, and treated with 10% tartaric acid to fix the nitrogen content. The samples were then sealed and stored at -20°C. After the experiment, the samples were thawed at room temperature, air-dried in the shade, and subsequently dried in a constant-temperature oven (Shanghai Yiheng DHG-9070A, 70L, temperature range RT + 10~300°C, temperature control accuracy: 1°C, China) until completely dry, after which they were weighed.

Feed residues from the repeated cages were collected for 5 consecutive days before the end of the experiment. For cages without remaining feed, 10 g feed samples were collected using a four-point sampling method. These samples were then mixed, and 10 g was taken for the determination of conventional nutritional components.

2.4 Sample determination

2.4.1 Measurement of growth performance indicators

The growth performance indicators were determined following the method outlined by Kim (Kim et al., 2024).

2.4.2 Blood sample index measurement

(1) Antioxidant and immune indicators were measured according to the method by Adil (Adil et al., 2024).

(2) Additional indicators included total protein (TP) (Mindray BS-420 Automatic Biochemical Analyzer, Shenzhen, China), albumin (ALB) (Mindray BS-420 Automatic Biochemical Analyzer, Shenzhen, China), globulin (GLB) (Mindray BS-420 Automatic Biochemical Analyzer, Shenzhen, China), triiodothyronine (T3) (Mindray BS-420 Automatic Biochemical Analyzer, Shenzhen, China), and tetraiodothyronine (T4). (Mindray BS-420 Automatic Biochemical Analyzer, Shenzhen, China). Instrumentation used included a spectrophotometer (Puxi General TU-1901 UV-Visible Spectrophotometer, Beijing, China, 400–700 nm) and an enzyme-labeled instrument (Mindray MR-96A Vet Automatic Microplate Reader, Shenzhen, China).

2.4.3 Measurement of slaughter indicators

Slaughter performance parameters were assessed according to NY/T 823—2020 “Poultry Production Performance Terminology and Measurement Calculation Method” and national food safety standards. Measurements included live weight, carcass weight, total clean bore weight, semi-clean bore weight, chest muscle weight, leg muscle weight, and organ weights (heart, lung, liver, muscular stomach, glandular stomach, spleen, bursa of Fabricius, gonad). The slaughter rate, semi-clean bore rate, total clean bore rate, chest muscle rate, leg muscle rate, and organ index were also calculated.

2.4.4 Conventional nutrient composition determination

The dry matter content of feed and fecal samples was determined using the adsorption water method (Shanghai Yiheng DHG-9070A Electric Blast Drying Oven, (Shanghai, China), electric air blower drying oven, 200 L ~ 500 L). Organic matter content was measured according to GB5009.4–2016 using a 550°C muffle furnace (Shanghai Yiheng SX2-4-10N Box-Type Muffle Furnace (Shanghai, China) furnace size: 200 × 120 × 80 mm, power: 1.5 kW, voltage: 220 V). The crude protein content in diet and fecal samples was determined by the Kjeldahl nitrogen method [Shanghai Peiou SKD-200 Automatic Kjeldahl Nitrogen Analyzer (Shanghai, China)] in accordance with GB5009.5-2016. Crude fat content was measured via petroleum ether extraction as per GB5009.6-2016 [Shanghai Xinjia JK-200C Crude Fat Analyzer (Shanghai, China)]. Calcium and phosphorus contents were quantified by atomic absorption spectrometry (Beijing Purkinje General TAS-990 Atomic Absorption Spectrophotometer (Beijing, China)).

The apparent metabolic rate of a certain nutrient is calculated as (the content of a certain nutrient in feed - the content of a certain nutrient in feces and urine) divided by the content of a certain nutrient in feed, multiplied by 100%.

2.4.5 Sample determination of fecal microflora

The sequencing and result analysis were entrusted to Beijing Huaying Institute of Biotechnology for assistance.

2.5 Statistical analysis

Data preprocessing was initially performed in Excel, followed by one-way ANOVA using SPSS 27.0 software. Multiple comparisons between groups were conducted using Duncan’s method, and experimental results are presented as mean ± standard deviation (Mean ± SD). Statistical significance was set at P < 0.05, with P < 0.01 indicating extremely significant differences.

3 Results

3.1 Effect of ellagic acid supplementation on nutrient digestion and metabolism in young pigeons

Table 2 indicates no statistically significant difference between the control and test groups (P > 0.05).

Table 2

Table 2. Effect of ellagic acid supplementation on nutrient digestion and metabolism in young pigeons (unit:%).

3.2 Effect of ellagic acid supplementation on the growth performance of young pigeons

The effects of EA on the growth performance of young pigeons are presented in Table 3. As shown, the average daily weight gain in test group I, test group II, and test group III increased by 3.25%, 15.58%, and 12.99%(P>0.05), respectively, compared to the control group. Among these, the average daily gain in test group II was the highest. Additionally, the feed-to-weight ratio in test group I, test group II, and test group III decreased by 6.84%, 14.13%, and 17.88%(P>0.05), respectively. The feed-to-weight ratio in test group III was the lowest. These results suggest that EA supplementation improved the growth performance of young pigeons and reduced the feed-to-weight ratio.

Table 3

Table 3. Effect of ellagic acid supplementation on the growth performance of young pigeons (unit:g).

3.3 Effect of ellagic acid supplementation on the body length and size of young pigeons

Table 4 presents the effects of EA supplementation on the body length and measurements of young pigeons. No significant differences were observed in the body length and body size of the 29-day-old pigeon groups. However, at 60 days of age, significant differences were noted. The chest width in test group III was significantly higher than in the other groups (P < 0.05), showing a 9.87%, 9.87%, and 6.03% increase compared to the control, test group I, and test group II, respectively (P < 0.05). Chest depth in test group III was higher than in the control group (P > 0.05) and significantly higher than in test group I and test group II (P < 0.05), with increases of 5.85% and 5.69%, respectively. The tibia length in test group III was significantly greater than in the other groups (P < 0.05), with increases of 6.54%, 8.01%, and 6.54% compared to the control group, test group I, and test group II, respectively (P < 0.05). These findings demonstrate that EA supplementation significantly improved chest width, chest depth, and tibia length in pigeons.

Table 4

Table 4. Effect of ellagic acid supplementation on the body length and size of young pigeons (unit: cm).

3.4 Effect of ellagic acid supplementation on the slaughter performance of young pigeons

The effect of EA supplementation on the slaughter performance of young pigeons is shown in Table 5. As indicated, the semi-clean bore weight in the test groups was higher than in the control group, with test groups II and III showing significant increases of 8.48% and 7.55%, respectively (P < 0.05), compared to the control group. Chest muscle weight in test groups II and III was 14.27% and 10.37% higher than in the control group, respectively (P < 0.05), with test group II showing a significant 9.12% increase compared to test group I (P < 0.05). The leg muscle weight in test group III was significantly higher than in the control group, with a 23.89% increase (P < 0.05). In the aspect of semi-clean bore rate, the test group II and test group III were significantly higher than the control group, increasing by 8.23% and 8.07% respectively (P < 0.05).

Table 5

Table 5. Effect of ellagic acid supplementation on the slaughter performance of young pigeons.

3.5 Effect of ellagic acid supplementation on organ weight and index of young pigeons

The effect of EA supplementation on organ weight and indices in young pigeons is shown in Table 6. As per the table, gizzard weight in test group III were significantly higher than in the control group, with a 16.67% increase (P < 0.05). These findings indicate that EA supplementation significantly increases muscle and stomach weight.

Table 6

Table 6. Effect of ellagic acid supplementation on the organ weight and index of young pigeons.

3.6 Effect of ellagic acid supplementation on the weight and index of immune organs in young pigeons

Table 7 presents the effect of EA on the weight and index of immune organs in young pigeons. The thymus weight and thymus index in test group I were significantly higher than in the control group, which increased by 7.33% and 8.62% respectively (P < 0.05). The bursa of Fabricius weight and index in test group III were significantly higher than in the control group, with increases of 37.5% and 50%, respectively (P < 0.05). These results suggest that EA supplementation can enhance the immune organ index, thereby impacting the immunity of young pigeons.

Table 7

Table 7. Effect of ellagic acid supplementation on the weight and index of immune organs in young pigeons.

3.7 Effect of ellagic acid supplementation on serum parameters of young pigeons

Figure 1: levels of immune cytokines (Figure 1A). Compared with the control group, the levels of IL-2 and IL-6 in each test group have no significant difference (P > 0.05). Antioxidant index (Figure 1B), GSH-Px in test group I was significantly higher than that in control group (P < 0.05), and MDA content in test group III was significantly lower than that in control group (P < 0.05). The level of immunoglobulin (Figure 1C), the IgA of test group I and test group II was significantly higher than that of control group (P < 0.05). Nitrogen metabolism and liver function index (Figure 1D) TP in test group I was significantly higher than that in control group (P < 0.05), and AST in test group III was significantly lower than that in control group (P < 0.05). Hormones (Figure 1E) There was no significant difference between the test groups and the control group.

Figure 1

Figure 1. Effect of ellagic acid supplementation on serum parameters of young pigeons. (A) Interleukin; (B) Antioxidant index; (C) Immune index; (D) Nitrogenmetallism and Kyoto level. (E) Hormone. * indicates that there are significant differences among other groups (P < 0.05).

3.8 Venn diagram based on OTO

The Venn diagram is a useful tool for displaying the common and unique features between samples, offering a clear visual representation of feature overlap. Each sample is depicted in a different color, and the numbers in the overlapping sections indicate the number of shared features between samples. Figure 1 presents a Venn diagram based on OTUs, showing that the fecal microbiota of squabs grouped as A, B, C, and D share a total of 224 OTUs. This means that 224 species are common across the groups, with 56 OTUs unique to group A, 50 unique to group B, 64 unique to group C, and 27 unique to group D. Notably, group C has the highest number of unique species compared to the other groups. As shown in Figure 2.

Figure 2

Figure 2. Venn diagram based on OTO. The four groups of ABCD compared in the figure correspond to control group, test group I, test group II and test group III respectively. Panel 2A: OTU diagrams of the control group. Panel 2B: OTU diagrams of the test group I. Panel 2C: OTU diagrams of the test group II. Panel 2D: OTU diagrams of the test group III.

3.9 Analysis of differences in alpha diversity index

The analysis of different groups (A, B, C, D) according to various indexes reveals the following results: Simpson index (Figure 3A): No significant statistical difference was found between groups, but the box chart shows different dispersion and concentration trends. Group a is relatively stable, while group b shows high dispersion; ACE index (Figure 3B): A significant difference was observed between group B and group D (P = 0.034), and group D had a significantly lower average index, indicating a lower community richness; PD whole tree index (Figure 3C): There was a significant difference between group C and group D (P = 0.021), and group D showed a significant decrease in phylogenetic diversity. Shannon index (Figure 3D): There was a significant difference between group C and group D (P = 0.042), and the species diversity of group D was low. Chao1 index (Figure 3E): Significant differences were found between group B and group D (P = 0.048) and group C and group D (P = 0.034), and the index of group D was significantly lower than that of other groups, indicating significant differences in species richness.

Figure 3

Figure 3. Analysis of differences in alpha diversity index. The four groups of ABCD compared in the figure correspond to control group, control group, test group I, test group II and test group III respectively. The ABCD compared in the figure corresponds to each other. (A) Differences in Simpson index. (B) ACE index. (C) PD whole-tree index. (D) Shannon index. (E) Chao1 index.

3.10 Effect of ellagic acid supplementation on the fecal microbiota of young pigeons

As shown in Figure 4A, at the phylum level, the top 10 phyla in pigeon feces include Firmicutes, Proteobacteria, Bacteroidota, Actinobacteria, Campylobacter, Desulfobacter, Verrucomicrobiota, Fusobacteria, Patescibacter, and Deferribacter. The relative abundance of Firmicutes in test groups I and III was higher than that in the control group (P > 0.05). Figure 4B presents the top 10 bacterial classes in pigeon feces, which include Bacillus, Gammaproteobacteria, Alphaproteobacteria, Bacteroides, Clostridia, Actinobacteria, Campylobacteria, Negativicutes, Desulfovibrio, and Fusobacteria. Statistically significant differences in the average relative abundance of Bacillus, Proteobacteria, and Alphaproteobacteria were observed between the groups (P < 0.05). Figure 4C illustrates the top 10 bacterial families in pigeon feces, which are Lactobacillaceae, Comamonadaceae, Sphingomonadaceae, Rhodococcaceae, Yersiniaceae, Burkholderiaceae, Lachnospiraceae, Enterobacteriaceae, Muribacaceae, and Bifidobacteriaceae. At the genus level, Figure 4D shows the top 10 bacterial species in the feces of young pigeons, including Lactobacillus, Acidovorax, Limosilactobacillus, Sphingomonas, Methylloversatilis, Serratia, Ralstonia, Aquabacterium, and Escherichia coli. Finally, Figure 4E presents the top 10 bacterial species at the species level in the feces of young pigeons, which include Lactobacillus bulgaricus, Acidovorax autersii, Lactobacillus agile, Lactobacillus crispatus, Lactobacillus johnsonii, Lactobacillus reuteri, Lactobacillus mucilaginosin, Lactobacillus salivarius, Lactococcus vaginalis, and Proteobacterium symbiont of Nilaparvata lugens.

Figure 4

Figure 4. Effect of ellagic acid supplementation on the fecal microbiota of young pigeons. The four groups of ABCD compared in the figure correspond to control group, control group, test group I, test group II and test group III respectively. (A) Effects of ellagic acid supplementation on fecal microbiota in squabs at the phylum level. (B) Class level. (C) Family level. (D) Genus level. (E) Top ten bacterial species at the species level.

3.11 Functional gene prediction analysis

3.11.1 PICRUSt2 function prediction

Figure 5 shows the relative abundance distribution characteristics of differentially expressed genes. The functions of these differential genes can be divided into six categories: primary metabolism-related genes account for the highest proportion, and their functions cover the synthesis and decomposition pathways of basic substances such as carbohydrate metabolism, lipid metabolism, amino acid metabolism and nucleotide metabolism, and also include key physiological processes such as cofactors and vitamin synthesis, energy metabolism and biosynthesis of secondary metabolites; Disease-related metabolic genes take the second place, mainly involved in the regulation of antibacterial, anti-tumor, anti-parasitic infection and immune diseases, suggesting that such genes may play an important role in resisting exogenous stimuli and maintaining immune homeostasis; The function of environmental information processing genes involves membrane transport, signal molecular transmission and interaction between cells and signal transduction, and is the key carrier to mediate cells to perceive changes in the external environment and start adaptive response. The relative abundance ratio of cell process genes is consistent with that of biological system genes. The former covers the basic cytological behaviors of prokaryotes such as cell process, cell mobility, growth and death, and material transport and decomposition, while the latter is directly related to the functional regulation of endocrine system, circulatory system and immune system, reflecting the multi-dimensional extension of gene functions from cell level to system level. Other system-related genes account for the lowest proportion, including regulatory genes of nervous system, excretory system, digestive system and other pathways.

Figure 5

Figure 5. PICRUSt2 function prediction. Tong pigeon KEGG metabolic pathway bar chart.

3.11.2 BugBase phenotype prediction

As shown in Figure 6, the relative abundance percentage of anaerobic bacteria in each group includes Clostridium difficile, Sphingomonas genus, Clostridium family, Desulfovibrio family, Fabaceae family, Spiridae family, Streptococcus family, Prevotellaceae family, Pasteurella, and others. Helicobacter pylori is a common pathogen responsible for human intestinal infections, particularly enteritis. Pasteurella can cause respiratory infections in various animals, including poultry, pigs, cats, and dogs, and may also cause human infections in certain cases, especially when in contact with animals or animal products. Pasteurella is generally linked to respiratory diseases in animals. In the Streptococcus family, certain Lactobacillus strains, such as lactobacilli, are considered probiotics, as they help maintain a healthy gut microbiota balance and inhibit harmful bacteria growth. However, some Streptococcus species are associated with diseases, including streptococcal infections. Bacteria from the Caryophyllaceae family can be harmful under certain conditions, such as during food spoilage, necessitating appropriate control measures during food processing and storage. Certain Clostridium difficile species, including C. difficile, are associated with severe intestinal infections, particularly when antibiotics disrupt the normal gut microbiota.

Figure 6

Figure 6. BugBase phenotype prediction. Bar chart of juvenile pigeon BugBase species. The four groups of ABCD compared in the figure correspond to control group, control group, test group I, test group II and test group III respectively.

3.11.3 FAPROTAX ecological function prediction

As shown in Figure 7, based on FAPROTAX functional gene database, the functional annotation of operational classification unit OTU of pigeon feces samples was completed and the data was homogenized. The differences of functional annotation of OTU of feces samples under four kinds of ellagic acid feeding methods were compared by T-test, and the results are shown in Figure. Compared with the test group I, the number of OTU in the fecal bacterial community in the former was significantly higher than that in the latter (P < 0.01), while that in the test group I was significantly lower than that in the control group (P < 0.01). The number of OTU’s in fecal bacterial community in test group II, which was marked with nitrite ammoniation and respiration, aerobic chemotaxis, nitrate reduction, nitrogen respiration and fumaric acid respiration, was significantly higher than that in control group (P < 0.01), while the number of OTU’s marked with chemotaxis and fermentation function was significantly lower than that in control group (P < 0.01). The number of OTU in the fecal bacterial community of the test group III, which was marked as human intestine, animal parasite/symbiont and mammal intestine, was significantly higher than that of the control group (P < 0.01), while the number of OTU marked as chemoheterotrophic and fermentation function was significantly lower than that of the control group (P < 0.01).

Figure 7

Figure 7. Prediction of ecological function of FAPROTAXs. Results plot of Faprotax differences in squabs. (a) Faprotax difference result diagram of group A and group B; (b) the result diagram of the difference of Faprotax between group A and group C; (c) the result chart of the difference between group A and group D.

3.12 Correlation network analysis

As shown in Figure 8, in this study, the top 41 genera with the highest interspecific correlation under the six phylum classification of Firmicutes, Bacteroides, Desulfurization, Proteus, Actinobacillus and Campylobacter were selected, and the positive and negative correlation analysis was carried out based on Spearman algorithm and the statistical test was completed. Visualize the nodes with correlation coefficient > 0.1 and P < 0.05 and their relationship in the network diagram, and select the top 5 dominant bacteria nodes for in-depth analysis. The results showed that the average richness of Lactobacillus was the highest, and it was positively correlated with Aeriscardovia and negatively correlated with Methyloversatilis. Followed by acidophilus (positively related to rolston, Sphingomonas, Mycoplasma, Hydrobacter, Pseudomonas, etc.), limosilolacobacter (positively related to Aeriscardovia), Sphingomonas (positively related to Acidophilus, rolston, Mycoplasma, Allorhizobium-neorhizobium-pararhizobium-rhizobium, Pelomonas, etc. are positively correlated) and Methyloversatilis (negatively correlated with Lactobacillus).

Figure 8

Figure 8. Horizontal co-occurrence network analysis. Horizontal co-occurrence network analysis.

4 Discussion

Animal growth performance is closely linked to food intake, which directly influences nutritional metabolism, growth, and development. Currently, research on the use of EA as an effective substitute for antibiotics in pigeon diets is limited, both domestically and internationally. Due to the incomplete development of the immune system and digestive organs in pigeons, immune function may decline, reducing the efficiency of nutrient digestion and metabolism, ultimately affecting growth performance. Previous research (Baradan Rahimi et al., 2020) has shown that incorporating EA into animal diets can enhance immune function, regulate intestinal flora richness, improve growth performance, and promote overall health. The results of this Test group demonstrated that supplementing the diet with 200 mg/kg EA increased the average daily weight gain and average daily feed intake of young pigeons, while reducing the feed-to-weight ratio. These findings align with previous studies. For instance, adding a suitable amount of EA to broiler diets has been shown to enhance immune function, increase feed intake and daily weight gain, and thereby accelerate healthy growth (Kishawy et al., 2016). Lu observed that adding 500 mg/kg EA to weaned piglet diets significantly improved daily weight gain and reduced diarrhea rates. Additionally (Lu et al., 2022), Gul reported that EA can regulate intestinal flora, improve intestinal health, and support animal growth and development, ultimately benefiting human health (Gul et al., 2022). Wang found that EA supplementation in broiler diets improved the structure and function of the digestive system, enhancing nutrient digestion and absorption, thereby improving growth performance (Wang et al., 2022). In this study, different doses of EA had no statistically significant effect on the apparent metabolic rate of meat pigeons, which may be due to the differences in feeding cycle, individual animals and detection conditions, and EA did not cause significant changes in nutritional digestion and metabolism indexes. This shows that EA can improve the digestion and absorption efficiency of nutrients and promote animal feed intake and weight gain by enhancing immune function, regulating intestinal flora structure and improving the structure and function of digestive system.

Body size is a key index for evaluating the growth and performance of poultry, encompassing parameters such as body height, body oblique length, chest width, chest depth, tibia length, and tibia circumference. These indices not only reflect the development of bones and muscles but are also closely associated with economic traits, such as slaughter performance and meat yield. From the perspective of intestinal health, EA may enhance the intestinal microecological balance, promote nutrient digestion and absorption, and indirectly influence body size traits in poultry.

However, from the body size and weight, we also found a problem, that is, there are advantages between 400mg/kg EA and 200 mg/kg EA. The reasons are as follows: on the one hand, the biggest response of bone development to EA dose is higher: 400 mg/kg EA may provide sufficient physiological motivation for bone growth by promoting osteoblast activity and enhancing mineral element absorption, so the improvement of body shape index is more obvious; On the other hand, 200 mg/kg EA is more conducive to the accumulation of weight gain: this dose can effectively improve the utilization rate of nutrients without causing metabolic pressure on the body, and nutrients may be more like tissue synthesis, showing the peak of daily average weight gain; However, the nutrient distribution of 400 mg/kg EA group may be more inclined to bone mineralization, so the weight gain is slightly lower than that of 200 mg/kg EA group.

A healthy intestinal microbiota is crucial for improving intestinal barrier function, increasing feed conversion efficiency, and providing sufficient nutritional support for poultry growth and development. Moreover, EA may also affect body size development by modulating hormone secretion in poultry. Growth hormone (GH), insulin-like growth factor-1 (IGF-1), and other hormones play a central role in regulating growth and development by promoting chondrocyte proliferation and hypertrophy in the bone growth plate and stimulating muscle growth. In this study, dietary supplementation with varying concentrations of EA revealed that 400 mg/kg EA significantly improved the body size development of 60-day-old pigeons, specifically enhancing chest width, chest depth, and tibia length compared to the other concentration groups. It shows that ellagic acid may promote food intake by regulating the diversity of intestinal flora, and then affect the chest width, chest depth and other indicators.

Slaughter performance is a key indicator for assessing the production performance of meat pigeons, directly influencing economic returns. Generally, higher slaughter performance correlates with greater economic benefits (Li et al., 2024). The slaughter index of poultry is useful for breeding and identifying poultry varieties and serves as an important reference for evaluating the management and nutritional status of poultry. Organ weight reflects the state of organ growth and development and provides insight into metabolism, digestion, absorption, and immune function (Martínez et al., 2021). The results of this Test group showed that the semi-clean bore weight, chest muscle weight, leg muscle weight, and muscle stomach weight of the Test group were significantly higher than those of the control group, indicating that dietary supplementation with EA positively impacted both slaughter performance and organ index. Wang examined the effects of EA on the growth and development of pig breast and leg muscles and meat quality (Wang et al., 2024). Their findings indicated that EA increased breast and leg muscle weight, improved muscle tenderness, and enhanced water retention. Similarly, the results of this study show that the semi-clean bore weight, chest muscle weight and leg muscle weight of young pigeons are significantly increased after EA is added to the diet-this phenotypic change further proves that EA can alleviate the low nutritional and metabolic efficiency of young pigeons due to incomplete immune development by enhancing immune function (such as the increase of IgA and IgG levels in this experiment), thus providing more adequate nutritional and metabolic support for the growth of muscles and other tissues, and finally indirectly promoting the growth and development of the body.

The spleen and bursa of Fabricius are critical immune organs in poultry, and their development reflects the growth and immune function of the birds (Song et al., 2023). Studies have shown that EA promotes the development of immune organs, such as the thymus, spleen, and bursa of Fabricius, through its antioxidant and anti-inflammatory properties (Yang et al., 2022). In broilers, EA supplementation significantly increased thymus and spleen weight, indicating enhanced immune function. These findings highlight the potential of EA in promoting the development and function of immune organs (Wang et al., 2025), consistent with the results of this experiment. The data suggest that EA enhances animal immune function by promoting the development of immune organs, particularly the thymus and bursa of Fabricius. The possible reason is that EA can promote the development of immune organs such as thymus, spleen and bursa of fabricius by virtue of its antioxidant and anti-inflammatory properties, and then promote the immune function of animals themselves.

Immunoglobulins are key indicators of animal immunity. IgA, IgM, and IgG are closely associated with blood diseases, infections, and autoimmune disorders (Fuentes et al., 2019). Among these, IgG represents the largest proportion and plays a pivotal role in maintaining the body’s immune barrier and early defense mechanisms (Vidarsson et al., 2014). IgA exhibits antiviral and bacteriostatic properties, serving as the main effector molecule in humoral and mucosal immunity, directly participating in immune responses. IgM is a high-performance antibody involved in human defense, with bactericidal and antiviral functions (Zhang et al., 2024). The antioxidant properties of EA may reduce oxidative stress-induced damage to immune cells, thereby indirectly enhancing immunoglobulin synthesis and secretion. Deng demonstrated that EA regulates the levels of inflammatory factors, immunoglobulins, and T cells in burned rats, promoting wound healing and improving symptoms of immunosuppression (Deng et al., 2023). In this study, EA supplementation increased the secretion of IgA, IgG, and IgM. These results indicate that EA supplementation improves the humoral immune response and immune system function in pigeons. Although certain doses of EA increased antioxidant enzyme activity and immune markers (such as IgA), the highest dose (400 mg/kg) also elevated MDA levels, suggesting a higher level of potential oxidative stress. At this dose, EA may induce mild oxidative stress (evidenced by a slight increase in reactive oxygen species, or ROS). In response, the body activates a compensatory mechanism, upregulating antioxidant enzymes such as SOD and GSH-Px to eliminate ROS. However, when ROS production exceeds the scavenging capacity of these enzymes, lipid peroxidation is triggered, leading to the accumulation of MDA. Therefore, the increase in MDA may reflect an intermediate state between the initiation of oxidative stress and the incomplete compensation by antioxidant mechanisms, rather than indicating a final “redox imbalance” outcome. In addition, EA can promote the expression and activity of downstream antioxidant enzymes such as SOD and GSH-Px by activating Nrf2 pathway in young pigeons. Activated Nrf2 can regulate the transcription of phase II detoxification enzyme gene and enhance the ability of liver to remove toxic intermediates produced during metabolism. However, it is worth noting that the appropriate dosage of EA of 200 mg/kg can accurately match the antioxidant needs of young pigeons during the transition period, while the dosage of EA of 400 mg/kg is close to the effect threshold, which may be related to the fact that excessive EA exceeds the metabolic capacity of young pigeons and interferes with the steady-state regulation of Nrf2 pathway. It shows that EA can enhance the antioxidant capacity of the body and reduce oxidative stress through multiple ways: on the one hand, it can directly scavenge free radicals and inhibit lipid peroxidation; on the other hand, it can regulate the activity and gene expression of antioxidant enzymes such as SOD, GSH-Px and CAT in blood, and at the same time reduce the level of MDA, thus maintaining cell stability and reducing DNA damage.

Although direct studies on the effect of EA on serum nitrogen metabolism are limited, insights can be drawn from other animal models. For example, in various mouse models, EA has been shown to reduce serum total cholesterol (TC) and triglycerides (TG), while increasing high-density lipoprotein cholesterol (HDL-C) (Xu et al., 2021). This mechanism may involve EA’s regulation of lipid metabolism genes, such as inhibiting the expression of SREBP-1c mRNA and FAS mRNA, and promoting the expression of LPL mRNA to lower lipid levels. While this study primarily focuses on lipid metabolism, the underlying mechanism may be similar to nitrogen metabolism, as both involve the regulation of metabolic pathways. EA supplementation in animal diets may also indirectly influence nitrogen metabolism through its antioxidant and anti-inflammatory effects. Studies have demonstrated that EA has significant antioxidant capacity, reducing oxidative stress and inflammation (BenSaad et al., 2017). This shows that EA can maintain the homeostasis of intracellular environment through these effects, and then ensure the activity and function of enzymes involved in nitrogen metabolism.

EA supplementation has been found to reduce liver function enzyme levels, such as ALT and AST. For instance, in sheep, EA significantly reduced serum ALT and AST levels, thereby improving liver function (Li et al., 2022). Additionally, EA has been shown to mitigate abnormal liver function induced by silver nanoparticles, including lowering ALT and AST levels (Dabbaghi et al., 2023). EA also exhibits immunomodulatory effects, enhancing immune function by increasing serum IL-2 levels (Umesalma and Sudhandiran, 2010 Furthermore, EA possesses anti-inflammatory properties, reducing levels of inflammatory factors. In an experimental rat model, intraperitoneal injection of EA combined with carrageenan-induced paw inflammation demonstrated its long-lasting anti-inflammatory effects, potentially interacting with known cyclooxygenase inhibitors. Additionally, EA may act as a cyclooxygenase inhibitor, exerting anti-inflammatory effects by suppressing the release and activity of inflammatory mediators (Corbett et al., 2010). This shows that EA has triple effects of liver protection, immune enhancement and anti-inflammation, and may play an anti-inflammatory role by enhancing its own immunity and reducing the release of inflammatory mediators, thus alleviating inflammatory stress injury. Thereby improving liver function.

Cortisol, a stress hormone, is closely linked to oxidative stress (Balasundram et al., 2006). Tannin compounds, including EA, are widely present in plants and have demonstrated beneficial effects on the digestive and immune systems (Park et al., 2021). Feeding high-quality feed in combination with low-quality roughage has been shown to elevate serum cortisol concentrations in dairy cows. However, EA supplementation may reduce stress responses through its antioxidant properties, thereby lowering cortisol levels (Bai et al., 2022). Additionally, EA has been found to regulate the expression of leptin, a key protein secreted by adipose tissue, which plays a pivotal role in energy balance and weight regulation (Cisneros-Zevallos et al., 2020). By influencing leptin secretion or receptor expression, EA may positively affect body weight and metabolism. However, the effect of EA on the hormone level of meat pigeons and its related mechanism with production performance still need further verification and clarification in follow-up studies.

Non-starch polysaccharides in plants are not hydrolyzed by enzymes secreted by the host but are instead decomposed and utilized by microorganisms such as Bacteroides and Cladosporium in the intestine, serving as a primary carbon source for intestinal microbiota (Mo et al., 2023). Bacteroides and Cladosporium comprise more than 90% of the total intestinal microbiota, and their wide-ranging functions are attributed to their secretion of various degrading enzymes. EA exerts an antibacterial effect by interacting with bacterial cell wall components, such as NDK protein and GND protein, disrupting the structure (Fan et al., 2022). This may inhibit the formation of biofilms by beneficial bacteria like lactic acid bacteria (Ratti et al., 2023) and indirectly influence bacterial metabolism by regulating apoptosis-related genes (such as Bax and Bcl-2) and antioxidant capacity (Wu, 2018).

The bacteriostatic effect of EA is dose-dependent. At concentrations of 0 mg/kg, 100 mg/kg, 200 mg/kg, and 400 mg/kg, a low concentration (100 mg/kg) may promote the abundance of Firmicutes and Bacteroides through antioxidant effects (Xia et al., 2023). A medium concentration (200 mg/kg) may inhibit certain microbiota, while a high concentration (400 mg/kg) can cause fluctuating abundance levels due to toxicity. This fluctuation may result from the competitive effects of EA, the formation of metabolites, and the regulation of intestinal barrier function (Liu et al., 2016; Wang et al., 2022). Bacilli, as the dominant flora, is capable of protein decomposition (Partanen et al., 2010), while α-Proteobacteria positively correlates with humoral immune IgG levels (Yu, 2023) and impacts feed conversion efficiency along with Clostridia in the jejunum (He, 2021). Notable members include Burkholderia, which secretes antibacterial and anticancer secondary metabolites for bioremediation (Depoorter et al., 2016; Kunakom and Eustáquio, 2019) and serves as a host for heterologous expression (Liu et al., 2021). Lactobacillus bulgaricus, used as a feed additive, synthesizes antioxidant exopolysaccharides (Xu et al., 2017; Sasikumar et al., 2017), regulates immunity (Moro-Garcia et al., 2013), and promotes digestion to improve animal health. Its preparation enhances growth performance and antioxidant capacity in nursing pigs (Niu, 2022). Additionally, Flavobacteriia IIA improves nutrient utilization through pantothenic acid synthesis (Clemmons et al., 2019), and changes in the abundance of Fusobacteriia and Gammaproteobacteria are associated with diarrhea, stress (Liu, 2021), and potential pathogenicity, respectively. Sphingomonas tolerates environmental stress through its antioxidant properties, and Acidovorax creates an acidic microenvironment through acid production (Huang et al., 2024), influencing microbiota balance.

Although this study initially revealed the improvement of growth performance, immune function and antioxidant capacity of meat pigeons by adding EA to the diet, and explained some regulatory mechanisms, there were still some limitations. In this study, the effect of EA was analyzed only by serum biochemical indicators and routine immune indicators, and the combined analysis of metabonomics, transcriptomics and other multi-omics technologies was not carried out, so it was difficult to intuitively and accurately analyze the molecular network and key targets of EA regulating intestinal metabolism-immunity-growth axis of meat pigeons. Future research can integrate multi-omics technology, combined with intestinal histological observation and functional gene verification, further clarify the core pathway of EA to improve the meat quality of meat pigeons, and provide more comprehensive theoretical support for its application as an antibiotic substitute in poultry breeding.

5 Conclusion

In conclusion, supplementing the diet with EA can enhance growth performance, immunity, total protein content, and help maintain the richness and stability of the intestinal microbiota in young pigeons. The optimal effect is observed with the addition of 200 mg/kg EA to the feed.

Data availability statement

The original contributions presented in the study are included in the article/supplementary material. Further inquiries can be directed to the corresponding author.

Ethics statement

The studies involving humans were approved by The Laboratory Animal Welfare Ethics Committee of Xinjiang Agricultural University. The studies were conducted in accordance with the local legislation and institutional requirements. The participants provided their written informed consent to participate in this study. The animal study was approved by The Laboratory Animal Welfare Ethics Committee of Xinjiang Agricultural University. The study was conducted in accordance with the local legislation and institutional requirements.

Author contributions

JR: Writing – original draft, Writing – review & editing, Data curation. YFL: Validation, Writing – review & editing, Conceptualization, Writing – original draft, Data curation. MD: Writing – review & editing, Funding acquisition, Writing – original draft. YHL: Writing – original draft, Writing – review & editing, Funding acquisition. XZ: Writing – review & editing, Writing – original draft, Funding acquisition. HL: Supervision, Conceptualization, Writing – review & editing, Writing – original draft, Project administration, Funding acquisition. HY: Project administration, Funding acquisition, Writing – original draft, Supervision, Writing – review & editing, Conceptualization. JL: Supervision, Writing – original draft, Conceptualization, Writing – review & editing, Funding acquisition, Project administration.

Funding

The author(s) declared that financial support was received for this work and/or its publication. This research was supported by the Xinjiang Uygur Autonomous Region Key R&D Program-Xinjiang Characteristic Pigeon Breed Development and Key Technology R&D Promotion (2023B02036), “Tianshan Talent” Training Program (2023TSYCCY0003), Regional Modern Agricultural Industrial Technology System (XJARS-12-2), and the Poultry Functional Feed Formula Technology Achievement Transformation Demonstration Project (ZYYD2022CG01).

Conflict of interest

Authors JL was employed by company Moyu Blue Sea Pigeon Industry Co., LTD.

The remaining author(s) declared that this work was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Generative AI statement

The author(s) declared that generative AI was not used in the creation of this manuscript.

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