Effect of dietary substitution of corn with Flammulina velutipes residue on growth performance, serum biochemical indicators, slaughter performance and cecal microbiota in geese

Abstract

The experiment sought to determine the effects of substituting Flammulina velutipes residue (FVR) for corn on growth performance, serum biochemical parameters, slaughter performance and caecum microbiota of geese. One hundred and ninety-two 35old Hordobagy geese were used in this experiment, and they were divided into four groups and fed with various diets for 28 d. The geese in the control group were fed with a basal diet. The other groups substituted 12%, 24% and 32% FVR for corn in their diets, respectively. There was no significant difference in the feed/gain ratio between the addition of 12% and 24% FVR to the diet, however, these additions considerably raised final body weight, average daily feed intake, and average daily growth (p < 0.05). When 24% FVR was substituted for corn in the diet, the levels of albumin (ALB) and high-density lipoprotein cholesterol (HDL-C) dramatically rose (p < 0.05). The examination of caecal microbiota revealed that the substitution of FVR for corn greatly increased both the variety and quantity of the caecal microbiota as well as the amount of bacteria that produce short-chain fatty acids (SCFAs). In conclusion, FVR has the potential to be an effective corn replacement with a 24% acceptable substitution level.

HIGHLIGHTS

• Partial replacement of corn with Flammulina velutipes residue (FVR) can increase the average daily feed intake and final body weight of geese.

• Partial replacement of corn with 24% FVR can increase the levels of albumin (ALB) and high-density lipoprotein cholesterol (HDL-C) in goose serum.

• Partial replacement of corn with 24% FVR increases the abundance of short-chain fatty acid (SCFA) producing bacteria in the goose caecum.

Keywords:

• Flammulina velutipes residue
• growth performance
• serum protein
• lipid
• caecal microbiome

Introduction

Corn is a common energy source in animal diets around the world, particularly for pigs and poultry (Lyu et al. 2020; Muszyński et al. 2022). In order to help these animals fulfil their high energy needs during growth and production, it offers a quickly digested source of carbohydrates (Cemin et al. 2020). Geese are frequently bred for meat and feather (Ochrem et al. 2018), and the quality and quantity are greatly influenced by the diets. The COVID-19 and war have had a substantial impact on corn prices, resulting in its shortage and high cost (Lv and Wu 2022). This has prompted researchers to look for substitute feeds that can take the place of maize and lower the cost of raising geese (Das et al. 2022; Landim et al. 2022; Ogbuewu and Mbajiorgu 2022).

Flammulina velutipes (F-velutipes) is a type of edible mushroom that is commonly cultivated for human consumption (Li and Xu 2022). The leftovers from the cultivation process can be used as a source of feed for animals once the fruiting bodies have been gathered. The F-velutipes residue (FVR) is an excellent feed for livestock and poultry since it is high in protein and fibre. It was found that the addition of FVR to the dietary had no significant impact on the egg production rate, feed intake and feed conversion ratio in laying hens. Similarly, it was reported that substituting a portion of corn did not have adverse effects on the growth performance of laying hens (Na et al. 2005). Miles and Chang (2004) also observed that FVR can improve calcium and phosphorus metabolism, promote calcium absorption, increase calcium deposition and reduce calcium excretion in laying hens. FVR has been found to enhance the lipid and antioxidant characteristics of broilers and mitigate oxidative stress, leading to improved growth performance, and it can lower TC and LDL-C levels while improving immune status in broiler chickens (Mahfuz, He, et al. 2019; Mahfuz, Song, et al. 2019). Adding 2.5% FVR to pig diets improved serum LDL-C levels, fatty acid composition and increases jejunal VH/CD. When FVR is less than 3% in pigs weaned at 56 d, it increases levels of volatile fatty acid content and antioxidant immunity (Liu et al. 2020). In the digestion and metabolism process of poultry, Caecal bacteria are essential (Li et al. 2022; Montso et al. 2022). It has been demonstrated that adding FVR to broiler feed significantly lowers the amount of Salmonella in the caecum (Lee et al. 2012). Geese are better at consuming and digesting fibrous feed than other waterfowl. This is mainly because their caecum contains extremely effective bacteria, such as those from the Desulfovibrionaceae, Ruminococcaceae and Bacteroidetes (Liu et al. 2018; Gao et al. 2016).

The results of this experiment will reveal important details about the possibility of FVR as a component feed component for geese. If the results are positive, this could lead to the wider adoption of FVR in goose, reducing the reliance on corn and contributing to sustainable and economically viable poultry farming practices.

Materials and methods

Animal ethics

The experiment has been ethically approved by the Laboratory Animal Ethics Committee of the Shanghai Academy of Agricultural Sciences with the approval number was SAASPZ0522046. All methods used in the experiment have been conducted in accordance with the relevant regulations and ethical guidelines.

Experimental design, diets and birds

FVR was supplied by the Zhuang Hang Comprehensive Experimental Station of the Shanghai Academy of Agricultural Sciences (Shanghai, China) and processed by Shengwang Feed Co., Ltd. (Shanghai, China) for this experiment. FVR was dried at 65 °C using a three-stage rotary drum dryer (Lunji, Shandong, China), then pulverised with a grinder (Jishun, Shandong, China), and sieved through a 2-mm mesh to obtain a powder form. This powder was mixed with commercial feed for the experiments. All experiments were conducted using the same batch of FVR. The obtained FVR powder was sent to Ingele Testing Technology Service Co., Ltd. (Shanghai) for analysis. The analysis results revealed a crude protein content of 12.11%, crude fibre content of 14.63% and crude fat content of 14.14%, the specific nutrition and amino acid composition are shown in Table 1.

Table 1. Nutritional level of Flammulina velutipes residue (dry matter).

Items	Content
EE, %	3.14
Ash, %	14.14
CF, %	14.63
CP, %	12.11
ME (MJ/kg)	13.00
Ca, %	2.02
P, %	1.22
Amino acids
Asparagine, %	0.82
Threonine, %	0.40
Serine, %	0.42
Glutamic acid, %	1.08
Glycine, %	0.52
Alanine, %	0.51
Cysteine, %	0.30
Valine, %	0.46
Methionine, %	0.17
Isoleucine, %	0.33
Leucine, %	0.58
Tyrosine, %	0.27
Phenylalanine, %	0.38
Lysine, %	0.36
Histidine, %	0.20
Tryptophan, %	0.05
Arginine, %	0.41
Proline, %	0.46

EE: crude fat; Ash: crude ash; CF: crude fibre; CP: crude protein; ME: metabolisable energy; P: phosphorus

One hundred and ninety-two 35d Hordobagy geese from the Xiangtiange Family Farm in Ma’anshan City, Anhui Province, China were used in the experiment. The geese were divided into four groups, each having eight geese of equal gender distribution and six replicates. The control group was fed a basal diet consisting of corn (BD group), while the other groups were provided a mixture of the BD with 12% (FVR12 group), 24% (FVR24 group) or 32% (FVR32 group) dry mass of FVR, as a substitute for corn and a small amount of soybean meal. The BD was created in accordance with the NRC1994 standard and modified to satisfy the dietary needs of Chinese geese (Table 2). All geese were reared in enclosed goose sheds with a density of 0.5 m² per bird. The rearing method involved free-range on plastic wire mesh, and the temperature was maintained at room temperature. The poultry shed was well ventilated and natural light was provided from 8 am to 5 pm daily. The goose sheds were kept clean and sanitary throughout the entire experiment. During the trial, the geese had unrestricted access to feed and water. Regular monitoring of their health status and vaccination was carried out. The pre-feeding period lasted for 3 d, and the experiment spanned a duration of 28 d.

Table 2. Composition and nutrient level of experiment diets (air-dry basis).

Item	Groups
	BD	FVR12	FVR24	FVR32
Ingredient
Corn	67.92	57.37	46.74	39.72
Soybean meal	24.90	23.40	22.00	21.00
Flammulina velutipes residue	0.00	12.00	24.00	32.00
Soybean oil	2.00	2.00	2.00	2.00
Lysine	0.09	0.12	0.14	0.16
Methionine	0.09	0.10	0.10	0.10
Threonine	0.00	0.01	0.02	0.02
Premix^a	5.00	5.00	5.00	5.00
Total	100.00	100.00	100.00	100.00
Nutrient level^b
CP	16.00	15.99	16.01	16.00
ME (MJ/kg)	12.40	11.91	11.42	11.10
CF	2.56	4.05	5.56	6.56
Ca	0.79	0.78	0.79	0.79
P	0.51	0.51	0.52	0.51
Lysine	0.90	0.90	0.90	0.90
Methionine + Cysteine	0.66	0.66	0.66	0.66
Threonine	0.63	0.63	0.63	0.63
Tryptophan	0.20	0.18	0.18	0.18

BD: basal diet group; FVR12: 12% Flammulina velutipes residue; FVR24: 24% Flammulina velutipes residue; FVR32: 32% Flammulina velutipes residue;

CF: crude fibre; CP: crude protein; ME: metabolisable energy; P: phosphorus

^aOne kilogram of the premix contained the following: Fe 100 mg, Cu 8 mg, Mn 120 mg, Zn 100 mg, Se 0.4 mg, Co 1.0 mg, I 0.4 mg, VA 8330 IU, VB₁ 2.0 mg, VB₂ 0.8 mg, VB₆ 1.2 mg, VB₁₂ 0.03 mg, VD₃ 1440 IU, VE 30 IU, biotin 0.2 mg, folic acid 2.0 mg, pantothenic acid 20 mg, niacin acid 40 mg.

^bCrude protein, crude fibre, and metabolisable energy are actual values, while the rest are calculated values.

At the end of the experiment, geese with body weights close to the average were selected from each replicate and placed in digestion and metabolism cages. They were fed with the experimental diets, and their feed intake (FI) was recorded. A total collection method was used to collect faeces and urine mixture, and an oxygen bomb calorimetry method was employed to determine the gross energy (GE) of each diet and the total energy of the faeces and urine mixture (FE + UE).

Growth performance

The body weight and FI of each goose were noted at the beginning (35 d) and conclusion (63 d) of the experiment. These measurements were used to derive the parameters: ADG, ADFI and feed/gain ratio (F/G). Before being weighed, the geese had been fasting for 12 h. $$\text{ADFI}=\text{total}\text{feed}\text{intake}/\left(\text{test days}\times \text{total}\text{number}\text{of}\text{test}\text{geese}\right).$$ $$\text{ADG}=\left(\text{final}\text{body}\text{weight}-\text{initial}\text{body}\text{weight}\right)/\text{number}\text{of}\text{test days}.$$ $$\mathrm{F}/\mathrm{G}=\text{ADFI}/\text{ADG}.$$

Sample collection

Blood samples were taken from a single male goose from each cage at the end of the experiment. Four millilitres of blood were drawn from the wing vein, placed into vacuum-sealed tubes, and stored at 37 °C for 6 h. The blood was then centrifuged at 2, 263.95 g for 15 min to obtain the serum, which was analysed for several biochemical parameters using an automatic biochemical analyser (HITACHI 7,180, Tokyo, Japan). The parameters measured included total protein (TP), albumin (ALB), globulin (GLOB), glucose (GLU), burea nitrogen (BUN), total cholesterol (TC), triglycerides (TG), low-density lipoprotein cholesterol (LDL-C), high-density lipoprotein cholesterol (HDL-C), alanine aminotransferase (ALT), aspartate aminotransferase (AST) and alkaline phosphatase (AKP).

Slaughter performance

The geese were then bled to death humanely, and the slaughter performance was evaluated according to the NY/T 823–2020 method. The weight of the organs was also calculated by using the formula: Organ Parameters = Organ weight (g)/Final BW (kg).

16S rDNA sequencing

The DNA of the microorganisms in the caecal digesta was extracted using a DNA extraction kit from Tiangen (Beijing, China). The concentration of the extracted DNA was determined using a UV spectrophotometer from ThermoFisher (NanoDrop 2000, Waltham, MA). The purity of the DNA was confirmed using 1.0% agarose gel electrophoresis. The extracted DNA was then utilised as a template for PCR amplification, and the resulting products were purified, quantified, and normalised to form a sequencing library. This library was sequenced using the NovaSeq 6000 system (San Diego, CA) after dilution and quantification. Finally, the ASVs, diversity and difference analysis were performed on the generated sequence information.

Statistical analysis

The data for goose growth performance and serum biochemical indicators were organised using Microsoft Excel 2007. The data was analysed using SPSS version 25.0 software (SPSS Inc, Chicago, IL), and a one-way ANOVA test was conducted. The results were expressed as the mean ± standard deviation, and a significant difference was indicated by p < 0.05.

The quality of the original caecal microbial sequencing data was controlled using QIIME version 2.0 software（Flagstaff, USA）. The optimised sequences were obtained through sequence splicing, filtering and removal of chimaeras. The ASVs were clustered and analysed using USEARCH version 7.0 software (Edgar, 2010). The community composition of each sample was counted at the classification levels of phylum, class, order, family, genus and species, using Greengenes data ASVs taxonomic analysis. Principal coordinate analysis (PCoA) of the caecum was completed using the R language, and the data was visually displayed using STAMP version 2.1.3 software (Nova Scotia, Canada). α-diversity indices, including Chao1 index, Observed species index, Shannon index, Simpson index, Faith’s PD index and Pielou’s evenness index, were calculated using Mothur version 1.30.2 software (Ann Arbor, USA).

Results

Growth performance

Table 3 shows that there was no significant difference in initial BW between the groups. However, when compared to the BD group, the final BW in the FVR12 and FVR24 groups was significantly higher (p < 0.05). In addition, compared to the BD group, the ADFI was higher in each group (p < 0.05). There was no significant difference between the FVR12 and FVR24 groups and the BD group in F/G, but compared to the BD group, the F/G was significantly higher (p < 0.05). Furthermore, neither the mortality rate nor the elimination rate between the groups showed any differences.

Table 3. The effect of replacing corn with Flammulina velutipes residue (FVR) on the growth performance of geese^a.

Items	Groups
	BD	FVR12	FVR24	FVR32	p Value
Initial BW, g	2781.67 ± 243.28	2746.04 ± 223.76	2756.67 ± 262.89	2775.50 ± 198.45	0.825
Final BW, g	4590.42 ± 518.77^b	4877.60 ± 530.42^a	4907.29 ± 431.16^a	4778.00 ± 527.20^ab	0.008
ADG, g/d	64.60 ± 13.17^b	76.13 ± 13.50^a	76.81 ± 16.48^a	71.52 ± 16.27^a	<0.01
ADFI, g/d	440.70 ± 29.64^c	557.95 ± 21.57^a	518.86 ± 34.62^b	537.69 ± 22.16^ab	<0.01
F/G	6.86 ± 0.43^bc	7.34 ± 0.49^ab	6.77 ± 0.21^c	7.77 ± 0.47^a	0.001
Elimination rate, %	8.33 ± 9.13	5.56 ± 8.61	8.33 ± 9.13	5.56 ± 8.61	0.898
Mortality rate, %	13.89 ± 6.80	11.11 ± 8.61	13.89 ± 6.80	16.67 ± 10.54	0.724

^abcThe data in the table are compared in the same row, and different lowercase letters indicate that the difference has reached a significant level (p < 0.05).

BD: basal diet group; FVR12: 12% Flammulina velutipes residue; FVR24: 24% Flammulina velutipes residue; FVR32: 32% Flammulina velutipes residue; BW: body weight; ADG: average daily weight gain; ADFI: average daily feed intake; F/G: feed/gain

Serum biochemical indicators

As seen in Table 4, although there was a tendency for the levels of TP and GLOB in the FVR24 group to rise relative to the BD group, this difference was not statistically significant. When compared to the BD and FVR12 groups, the level of ALB in the FVR24 group was significantly higher (p < 0.05). Regarding serum lipid and protein metabolism, TC levels were higher in the FVR24 and FVR32 groups were higher compared to the BD group (p > 0.05) and HDL-C levels in the FVR24 group were significantly higher compared to the BD group (p < 0.05).

Table 4. The effect of replacing corn with Flammulina velutipes residue (FVR) on the serum biochemical indicators of geese.

Items	Groups
	BD	FVR12	FVR24	FVR32	p Value
TP, g/L	32.90 ± 8.65	34.95 ± 7.50	45.33 ± 10.51	40.57 ± 4.40	0.060
ALB, g/L	11.65 ± 2.73^b	12.22 ± 1.75^b	14.62 ± 1.84^a	14.15 ± 1.49^ab	0.049
GLOB, g/L	21.25 ± 6.00	22.73 ± 6.12	30.72 ± 8.90	26.42 ± 3.13	0.078
GLU, mmol/L	7.28 ± 0.84	7.27 ± 1.62	8.47 ± 0.76	7.52 ± 0.69	0.186
BUN, mmol/L	0.33 ± 0.08	0.43 ± 0.29	0.42 ± 0.26	0.38 ± 0.10	0.842
UA, umol/L	135.00 ± 36.39	128.33 ± 31.95	133.83 ± 37.13	121.00 ± 23.02	0.874
TC, mmol/L	2.70 ± 0.46	3.02 ± 0.78	3.43 ± 0.58	3.63 ± 0.69	0.084
TG, mmol/L	1.00 ± 0.27	0.73 ± 0.30	0.82 ± 0.30	1.08 ± 0.25	0.147
HDL-C, mmol/L	1.70 ± 0.16^c	1.98 ± 0.42^bc	2.48 ± 0.20^a	2.31 ± 0.24^ab	<0.01
LDL-C, mmol/L	0.95 ± 0.42	0.98 ± 0.36	0.93 ± 0.46	1.12 ± 0.30	0.817
ALT, IU/L	244.83 ± 53.10	172 ± 28.47	198.33 ± 48.44	216.83 ± 61.17	0.532
AST, IU/L	8.50 ± 2.59	9.50 ± 3.08	9.67 ± 3.33	7.50 ± 2.17	0.367
AKP, IU/L	20.50 ± 7.89	20.50 ± 10.45	28.00 ± 8.25	21.17 ± 6.94	0.106

^abcThe data in the table are compared in the same row, and different lowercase letters indicate that the difference has reached a significant level (p < 0.05).

BD: basal diet group; FVR12: 12% Flammulina velutipes residue; FVR24: 24% Flammulina velutipes residue; FVR32: 32% Flammulina velutipes residue;TP: total protein; ALB: albumin; GLOB: globuli, GLU: glucose; BUN: blood urea nitrogen; TC: total cholesterol; TG: triglycerides; UA: uric acid; LDL-C: low-density lipoprotein cholesterol; HDL-C: high-density lipoprotein cholesterol; ALT: alanine aminotransferase; AST: aspartate aminotransferase; AKP: alkaline phosphatase

Slaughter performance

As shown in Table 5, there were no significant differences in slaughter performance and organ parameters between the groups.

Table 5. The effect of replacing corn with Flammulina velutipes residue (FVR) on the slaughter performance of geese.

Items	Groups
	BD	FVR12	FVR24	FVR32	p Value
Slaughter rate, %	82.43 ± 1.63	81.95 ± 2.16	83.19 ± 3.48	80.13 ± 2.13	0.200
Half-bore rate, %	72.59 ± 2.16	72.43 ± 2.61	72.55 ± 2.27	70.00 ± 4.36	0.382
Full-bore rate, %	58.70 ± 1.41	59.54 ± 3.34	59.01 ± 2.90	57.61 ± 2.57	0.647
Breast muscle rate, %	14.39 ± 1.56	15.28 ± 1.43	15.06 ± 1.80	15.19 ± 0.94	0.717
Leg muscle rate, %	14.05 ± 1.13	15.34 ± 1.21	14.61 ± 1.93	14.24 ± 2.02	0.541
Abdominal fat rate, %	3.74 ± 1.02	3.18 ± 0.92	3.80 ± 0.87	3.71 ± 0.90	0.638
Myogastric index	34.16 ± 6.08	34.49 ± 2.51	36.59 ± 3.98	30.76 ± 5.38	0.224
Adenogastric index	18.56 ± 1.52	17.86 ± 2.72	17.38 ± 1.38	15.25 ± 2.07	0.443
Heart index	0.65 ± 0.39	0.59 ± 0.20	0.67 ± 0.23	0.57 ± 0.17	0.151
Liver index	6.10 ± 0.30	6.37 ± 0.39	5.89 ± 0.97	5.54 ± 0.56	0.052
Spleen index	2.66 ± 0.38	2.73 ± 0.31	2.90 ± 0.51	2.52 ± 0.41	0.898

BD: Basal diet group; FVR12: 12% Flammulina velutipes residue; FVR24: 24% Flammulina velutipes residue; FVR32: 32% Flammulina residue.

Gut microbial diversity

Based on the above results, 24% FVR substitute for corn is the best effect on goose growth performance and serum biochemical indicators. As a result, we proceeded to examine the variations in caecal microbiota composition between the BD group and the FVR24 group. Figure 1(A) shows the α-diversity of the microorganisms in the caecum, comparing the BD and FVR24 groups. Our results revealed that the Observed Species Index, Shannon Index, Simpson Index and Pielou’s Evenness Index values were significantly higher in the FVR24 group (p < 0.05), indicating that the addition of 24% FVR in the diet enhanced the richness, diversity and evenness of the caecal microorganisms. The β-diversity of the caecal microbiota is shown in Figure 1(B) and was assessed using the Bray–Curtis distance algorithm. The results indicated that the differences between the BD and FVR24 groups were more pronounced than the differences within each group (p < 0.05).

Figure 1. Effects of adding Flammulina velutipes residue (FVR) to the dietary on the caecal microbiota of geese (A) α-diversity; (B) β-diversity; (C) Phylum-level composition; (D) Genus-level composition; (E) Biomarker species; (F) Spearman analysis.

Gut microbiome composition

In the caecum (Figure 1(C)), the dominant phyla (top 10) of BD group and FVR24 group were Firmicutes (54.93% and 60.70%), Bacteroidetes (22.51% and 21.12%), Proteobacteria (16.66% and 14.50), Actinobacteria (3.38% and 0.60%), Verrucomicrobia (0.43% and 1.47%), Tenericutes (1.21% and 0.66%), Cyanobacteria (0.32% and 0.34%), Synergistetes (0.24% and 0.21%), Elusimicrobia (0.07% and 0.08%) and Fusobacteria (0.02% and 0.08%), the dominant genera (top 10) were Desulfovibrio (15.44% and 12.85%), Bacteroidaceae_Bacteroides (6.78% and 10.09%), Phascolarctobacterium (3.76% and 4.36%), Oscillospira (2.80% and 5.31%), Subdoligranulum (3.76% and 2.93%), Faecalibacterium (1.46% and 4.04%), (Prevotella) (5.12% and 0.02%), Ruminococcus (0.91% and 2.35%), (Ruminococcus) (0.97% and 1.99%) and Bamnesiella (1.55% and 1.00%) (Figure 1(D)).

Gut microbiome difference

The Linear discriminant analysis effect size was performed to identify robustly distinct species (biomarkers) between the two groups. Faecalibacterium, Ruminococcus, Akkermansia, (Ruminococcus), Coprococcus and Coprobacillus were the biomarkers of the HSW24 group, while YRC22, and Lactobacillus were biomarkers for the BD group (Figure 1(E)).

Correlation analysis between biomarkers and measured parameters

Our analysis utilising Spearman correlation showed a correlation between the top 20 biomarkers in terms of abundance and growth performance as well as serum biochemical indicators (Figure 1(F)). Results indicated that Faecalibacterium, Ruminococcus, Akkermansia and Coprococcus were positively related to ADFI. Additionally, Akkermansia was found to have a negative correlation with the F/G. In regards to serum protein and lipid metabolism levels, these same four bacteria species were positively correlated with ALB and HDL-C. Furthermore, Ruminococcus and Akkermansia were positively related to TP, GLOB and UA levels.

Discussion

ADFI is an important parameter to assessing the health and productivity of animals, and the palatability of the feed can reflect the quality of the feed is generally positively correlated with the ADFI (Brown et al. 2016; Silva et al. 2021). The mushrooms contain a aromatic smell due to their volatile substances (Zhang et al. 2018), which may increase the ADFI. The study showed that sheep diets contain 25–30% FVR can improve ADG and ADFI (Hwangbo 2014), Animals that ingest feed containing high level of crude fibre require more time and effort to digesting, which causes them to feel fuller more quickly. As a result, animals can stop eating before consuming enough nutrients. High crude fibre diets may not have a good effect on the growth of pigs and chickens because of the poor nutrient consumption (Chu et al. 2012; Mahfuz, He, et al. 2019; Mahfuz, Song, et al. 2019). Recent research suggests that herbivorous animals can consume feed with higher levels of crude fibre without experiencing any negative effects on the growth performance (Rahayu et al. 2022). Additionally, data from studies show that adding up to 10% crude fibre to goose diets has no negative effects on the birds’ performance (Jin et al. 2020). In this experiment, ADFI is highest in the FVR12 group and FVR32 group. In the FVR12 group, geese may not be able to effectively digest and utilise the extra feed. The excess feed will be excreted, resulting in feed wastage. On the other hand, adding 32% FVR reduces the feed’s metabolic energy, requiring geese to consume more feed to meet their nutritional requirements. This indicates that adding 24% FVR is a balanced level, partial substitution of corn at 24% FVR had no negative impact on the growth performance of geese.

Serum protein levels can reveal crucial details about the health of the birds. ALB is the most abundant protein in serum, and a fair increase can help transport hormones, fatty acids and drugs in the blood (Czub et al. 2019; Linciano et al. 2022). GLOB can help with immunological function (Bunglavan et al. 2014), and an increase within a certain range indicates an improvement in the animal’s health. Polysaccharides extracted from the fruiting body of F-velutipes are bioactive compounds that have been shown to improve the immune function of animals (Hao et al. 2021; Liang et al. 2022). In mice, 4% F-velutipes mycorrhizae can improve hepatic fatty acid transport (Luo et al. 2022). Additionally, the F-velutipes antioxidant properties may help protect cells from oxidative stress and inflammation (Ma et al. 2021), which can increase protein turnover and contribute to changes in blood protein levels (Anderson 2010). Edible mushrooms are rich in amino acids (Li et al. 2021), and amino acids play an important role as metabolic intermediates in nutrition, immune responses and growth performance (Wu et al. 2015). In this experiment, we analysed the amino acid composition of FVR and found that it contains high levels of glutamic acid (Table 1). Glutamic acid supplementation has been shown to improve the content of TP in the serum of cows (Li et al. 2022). Additionally, glutamic acid is known to promote the synthesis of arginine, improve liver metabolism and prevent liver cell apoptosis (Huang et al. 2019). Arginine is considered an essential amino acid for poultry (Khajali et al. 2018), as it can promote muscle protein synthesis, production of polyamines and hormones, and improve the content of TG and TP in geese serum (Chen et al. 2023). The HDL-C has been shown to help transport cholesterol from peripheral tissues back to the liver, where it can be eliminated from the body or used for other metabolic processes (Kontush and Chapman 2006). Adding FVR to pig or chicken diets can improve serum lipid metabolism (Mahfuz, He, et al. 2019; Mahfuz, Song, et al. 2019; Mahfuz et al. 2020), this may be attributed to the presence of bioactive compounds in FVR, such as polysaccharides and triterpenoids (Liang et al. 2022). These bioactive compounds have demonstrated the ability to enhance the expression of pivotal genes responsible for the synthesis and transport of HDL-C (Remesova and Denisova 1999; Ren et al. 2017).

Slaughter performance is an important indicator of nutrient deposition and a crucial trait in poultry breeding (Chen et al. 2019). Currently, there are limited studies investigating the impact of FVR on slaughter performance. The study on dietary addition with FVR in goose diets found that it had no negative impact on slaughter performance. This indicates that the inclusion of 24% FVR as a replacement for corn did not alter the overall nutritional balance. Furthermore, we observed that geese have good digestive capacity for agricultural by-products, as the supplementation of defatted rice bran and cottonseed meal in goose diets did not affect their slaughter performance (Chen et al. 2019; Yu et al. 2020). Based on previous findings and considering growth performance, serum biochemical indicators and slaughter performance, we believe that a 24% FVR can effectively substitute corn to achieve the greatest results.

Animal gut microbiota is important for host health and nutrition utilisation. They are involved in several key functions, such as the fermentation of dietary fibre, the synthesis of vitamins and essential amino acids and the modulation of host immune function (Blachier and Wu 2022; Gerasimidis et al. 2022; Jiang et al. 2022). In this study, the Shannon index and the number of observed species of the FVR24 group were significantly higher than those of the BD group, indicating that substituting corn with 24% FVR significantly increased the diversity and richness of caecal microbiota. Diversity and richness reflect the stability and health of intestinal microbiota, which is beneficial for the host (Salonen et al. 2012). Moreover, PCoA analysis revealed a significant difference between the two groups, indicating that replacing corn with 24% FVR changed the microbial composition of the goose caecum. Adding FVR to laying hens’ diet significantly increased the abundance of Clostridium, Sutterella, and the short-chain fatty acids (SCFAs) (Wei et al. 2023). This finding is consistent with our experiment where we compared species abundance between two groups using LEfSe analysis. Our results showed that the abundance of Clostridium, Sutterella, Faecalibacterium, Ruminococcus and Akkermansia were significantly increased. Notably, Faecalibacterium, Ruminococcus and Akkermansia are all SCFA-producing bacteria. Faecalibacterium is one of the main producers of butyrate in the gut (Nakashima et al. 2021). Butyrate has numerous physiological functions in the gut, including promoting the growth and proliferation of intestinal epithelial cells, regulating immune responses, maintaining the intestinal mucosal barrier function and reducing intestinal inflammation (Canani et al. 2011; Hamer et al. 2008). Furthermore, earlier research has demonstrated that giving Faecalibacterium to high-fat-fed mice can improve lipid metabolism (Munukka et al. 2017). This is consistent with our findings, which show a positive correlation between Faecalibacterium and serum HDL-C levels. Ruminococcus obtain nutrients from host’s gut by breaking down cellulose. Long-term consumption of high-fibre foods promotes the degradation of complex carbohydrates by Ruminococcus, resulting in the production of acetate esters, propionate and butyrate (Morrison and Preston 2016), which correspond to the differences in crude fibre between the two groups. Previous studies have linked fermentable fibre to appetite with appetite regulation management (Daud et al. 2014; Pedersen et al. 2013), Propionate, one of the SCFAs, is believed to improve appetite by regulating the secretion of PYY and GLP-1 (Chambers et al. 2015). In this experiment, we noticed a positive correlation between the addition of SCFA-producing bacteria and ADFI, which is consistent with these findings. Akkermansia can also repair the intestinal barrier and lower serum and cholesterol levels (Belzer and De 2012; Dao et al. 2016). In this experiment, substituting corn with FVR in the diet increased the abundance of SCFA-producing bacteria in the caecum. SCFAs have been shown to lower plasma cholesterol and GLU levels, and increase fatty acid oxidation to prevent metabolic diseases, such as Cardiometabolic disorders (De et al. 2021).

Conclusions

In this experiment, substituting 24% of corn in the diet of geese with FVR did not have negative effects on growth performance, and improved serum protein, lipid metabolism and the abundance of SCFA-producing bacteria in the caecum.

Author contributions

Conceptualisation, Huiying Wang and Daqian He. Data Collection, Xianze Wang, Yi Liu, Yunzhou Yang, Cui Wang and Shaoming Gong, writing – original draft preparation, G.L.; writing – review and editing, H.W. All authors have read and agreed to the published version of the manuscript.

Disclosure statement

The authors declare no conflict of interest.

Data availability statement

The data that support the findings of this study are available on request from the corresponding author, Daqian-He. RNA sequencing data has been uploaded to National Centre for Biotechnology Information with the accession number PRJNA935670.

Additional information

Funding

This research was funded by the Climbing Plan of Shanghai Academy of Agricultural Sciences (PG21171), SAAS Program for Excellent Research Team (2022-021) and China Agriculture Research System of MOF and MARA (CARS-42-35).