Effects of different rearing systems on carcase traits, physicochemical properties, basic chemical composition, fatty acid profiles and amino acid profiles of Gangba lamb

Abstract

This study aimed to explore the influence of feeding regimens on carcase traits and meat quality of Gangba lambs. Thirty healthy Gangba ram lambs at nine months of age and an average body weight of 14.08 ± 0.79 kg were randomly distributed into three treatment groups (10 replicates per group). The groups are as follows: a grazing (G) group without any supplementation and housing; a semi-grazing (SG) group provided with 200–300 g of concentrates and free access to oat hay off-pasture; and a stall-feeding (SF) group with 400–500 g of concentrates and free access to oat hay. The experiment lasted 85 d, comprising a 10-d adaptation period and a 75-d experimental period. Results showed that significant differences in carcase weight existed among groups, respectively, with the SF group having the highest weights and the G group having the lowest weights (p < 0.05). The pH_45min and pH_24h in the G group were significantly higher than that in the SG group (p < 0.05). Muscles from the G and SG groups had higher erucic acid (22:1n-9), α-linolenic acid (C18:3n3), and conjugated linoleic acids (CLA-c9t11 and CLA-t10c12) than the SF group (p < 0.05). The G group had a lower concentration of proline (Pro) than the SF group (p < 0.05). In conclusion, the feeding systems had no effects on chemical composition and little influence on amino acid composition. The traditional grazing rearing and SG systems improved lamb meat quality by increasing the presence of beneficial fatty acids. In contrast, the SF regimen improved the carcase weight of Gangba lambs without increasing their meat quality compared to the grazing rearing and SG systems. The directions of future efforts for breeders are to improve carcase traits (like carcase weight) of lambs in both natural grazing and SG systems, as well as the meat quality of lambs raised in feedlots.

Highlights

•The grazing system improved lamb meat quality without improving carcase traits.

•The semi-grazing (SG) system improved meat quality as well as carcase traits.

•The stall-feeding (SF) regimen only improved the carcase traits.

Keywords:

• Rearing systems
• carcase traits
• physiochemical properties
• fatty acid profile
• amino acid profile

Introduction

As is well known, sheep meat is a good source of protein and beneficial fatty acids for human consumption worldwide. With the continuous improvement of people’s living standards, the focus of meat production is shifting from quantity to quality (Zhang et al. 2017). Meat quality, including elements of basic chemical composition, physicochemical properties and fatty acid and amino acid profiles, significantly affect consumers’ meat purchasing decisions (Weng et al. 2021). Sheep meat produced on the pasture feeding system, which is a traditional management practice for raising sheep, is thought to produce high-quality meat products (De Brito et al. 2017). However, pastureland is frequently under degradation pressure from domestic overgrazing (Zhang et al. 2022; 2022). With particular focus on protecting the environment, the Chinese government has implemented polices to mitigate pasture degradation and conserve grasslands, which are gradually transforming the traditional grazing modes of livestock to semi-grazing (SG) and feedlots modes (Wang et al. 2018).

The different feeding regimens are an important factor in determining sheep carcase traits and meat quality. In terms of carcase traits, lambs finished on pasture show lower slaughter and carcase weights than lambs fed concentrates on feedlots (Wang et al. 2018; Gallo et al. 2019; Zhang et al. 2022; 2022). Furthermore, the amount of intramuscular fat (IMF) in meat from grazed lambs was found to be lower than that from concentrate-fed lambs, while the pH_24h of meat in pasture groups was higher than that of meat in feedlots group (Wang et al. 2018; Luo et al. 2019; Karaca et al. 2016). Meat of pasture-fed sheep had a significantly higher concentration of polyunsaturated fatty acids (PUFAs) than that of sheep raised in a feedlot, including α-linolenic acid (C18:3n-3), docosahexaenoic acid (DHA), eicosapentaenoic acid (EPA) and conjugated linoleic acid (CLA) isomers (De Brito et al. 2017; Prache et al. 2022). However, the effects of different rearing systems on amino acid composition have not been found to be consistent across studies, which may be due to the different breeding methods of experimental animals.

Gangba sheep is an endemic species of Xigaze and derives its name from its location in Kamba County, Xigaze city in Tibet, China, where the average altitude is 4700 m above sea level, accompanied by the mean annual rainfall of 431.2 mm and a mean annual temperature of 6.3 °C (Paltridge et al. 2009). Gangba mutton is a typical breed found in the Qinghai-Tibet Plateau region which is the result of long-term natural selection in a harsh local environment. The traditional rearing system for Gangba sheep involves an extensive grazing regimen, although SG and feedlot systems have also been recommended in recent years. Our research team has reported the effects of various feeding systems (grazing, SG, and barn feeding systems) on the growth performance and rumen bacterial diversity of Gangba lambs (Zhang et al. 2022; 2022), and results showed that certain bacterial relative abundance and rumen fermentation parameters varied markedly under different feeding strategies. In fact, physiological changes of rumen of lambs have been found to finally influence the carcase traits and quality of lamb products, especially for lamb meat quality (Wang et al. 2021). However, the effects of different feeding regimens on carcase traits and meat quality of Gangba lambs have not yet been evaluated.

Therefore, the aim of this study was to investigate the response of carcase traits and meat quality (physiochemical properties, basic chemical composition, fatty acid profiles, and amino acid profiles) of Gangba lambs to three feeding systems (grazing, SG, and barn feeding systems). The research results will serve as a theoretical basis and support for the improvement of carcase traits and meat quality of Gangba lambs through optimising rearing modes.

Material and methods

Experimental design and animal management

The experimental protocol was approved by the Institutional Animal Care and Use Committee of the Chinese Academy of Agricultural Sciences, and the treatment, housing, husbandry, and slaughtering conditions conformed to the Experimental Animal Care and Use Guidelines issued by Chinese Science and Technology Committee. The experiment was conducted in Gangba county, Xigaze city, Tibet (88°8′20″–88°56′47″E、27°56′32″–28°45′27″N).

Thirty healthy Gangba ram lambs (single birth) with an average age of nine months and average body weight of 14.08 ± 0.79 kg were randomly distributed into three treatment groups (n = 10): a grazing (G, control) group, a SG group and a stall-feeding (SF) group. Lambs of the G group were grazed in the alpine meadow steppe dominated by Artemisia minor Jacquem.ex Besser, Iris collettii Hook.f., Festuca wallichanica E. Alexeev, Kobresia deasgi C. B. Clarke and Kobresia capillifolia (Decne.) C. B. Clarke, without any supplementation from 10:00 to 18:00 h; lambs in the SG group were grazed in the same steppe from 10:00 to 15:00 h and supplemented with 200–300 g of concentrates and free access to oat hay when off-pasture in individual pens; and lambs of the SF group housed in individual pens were provided with 400–500 g concentrates and free access to oat hay. Concentrate and oat hay supplementation were increased in the SG and SF groups as body weight increased. Daily adjustments were made to the supplemented oat hay depending on the previous day’s consumption, allowing for a 20% refusal rate. The daily ratio was formulated according to the Chinese Feed Standard of Meat-Producing Sheep and Goats (NY-T816-2004; Ministry of Agriculture and Rural Affairs of the People’s Republic of China, 2004). Water was available ad libitum for experimental lambs throughout the entire trial period. The experiment lasted 85 d, comprising a 10-d adaptation period and a 75-d experimental period. The processes of forage sample and basal diet collection, and the method to determine basal diet’s nutrient composition and nutrient level (%, dry matter) of basal diet, forage (oat hay and natural grasses) shown in Table 1, were described in detail in our previous study (Zhang et al. 2022; 2022).

Table 1. Ingredients composition, nutrient level of the basal diet (%, dry matter) and fatty acids content of the concentrate and pasture (g 100 g⁻¹ of fatty acid methyl esters, FAMEs).

Ingredient	Content	Nutrient level	Content
			Concentrate	Oat hay	Pasture
Chopped maize	55.00	Dry matter	88.30	90.03	89.99
Barley	10.00	Digestible energy^b, MJ/kg	15.10	12.40	–
Pea	23.50	Crude protein	16.10	10.06	8.93
Wheat bran	10.00	Neutral detergent fiber	8.68	52.89	59.82
Limestone	1.00	Acid detergent fiber	6.01	28.72	48.01
Premix^a	0.50	Calcium	0.54	0.40	2.27
		Total phosphorus	0.38	0.27	0.12
		Fatty acids
		C16:0	17.53		17.90
		C18:0	2.27		2.44
		C20:0	0.52		1.44
		C18:1n-9	24.37		2.17
		C18:2n-6	44.28		16.41
		C18:3n-3	7.47		51.12

^a Additive: Vitamin A, 10,500 IU; vitamin D3, 2110 IU; vitamin E, 43 mg; Mn, 40 mg; Fe, 32 mg; Zn, 95 mg; Cu 16 mg (per kilogram of dry matter provided).

^b Digestible energy was calculated value.

Carcase traits and meat physicochemical properties

Six lambs with similar weights to the average group body weight in each group were selected and slaughtered following a 24-h fasting period. Carcase properties were determined after the slaughter of 45 min. The carcase weight was determined after removing the head, hooves (including all distal parts of the members from carpus or tarsus), skin and viscera. The dressing percentage was calculated as the ratio of carcase weight to live weight before slaughter. The GR value, measuring the tissue thickness between the 12th and 13th ribs of sheep at 11 cm from the midline of the dorsal spine, was measured by vernier calliper.

The lambs’ carcases were stored at 4 ± 1 °C for 24 h, then specimens of the left lateral longissimus dorsi muscle (LDM) between the 12th and 13th ribs and biceps femoris muscle (BFM) were collected for subsequent analysis. Each LDM (six samples/treatments) was divided into two portions: one portion for meat physical parameters measurement after 24 h of chilling, and the other portion stored at −20 °C after vacuum packing was for proximate chemical analysis, fatty acid and amino acid profile. While BFM (six samples/treatments) being vacuum packed and stored at −20 °C was only for proximate chemical analysis, fatty acid and amino acid composition. Meat physical quality – including pH_45 min, pH_24 h, drip loss and cooking loss of only LDM – was determined by the method described by Honikel. (1998). An appropriate amount of frozen muscle sample (both LDM and BFM) mentioned above was cut into 1–2 cm pieces and immediately minced using a meat grinder (Shangyuan, SYP-MM 12, Guangdong, China), then dried in a vacuum lyophilizer (Yetuo, YTLG-12C, Shanghai, China) at −70 to −80 °C and mashed using a mortar and pestle. The obtained powder samples were stored at −20 °C to measure chemical composition, fatty acid and amino acid profiles.

Chemical composition measurement of lamb meat

The routine nutritional composition of lamb meat (LDM and BFM) was determined by the recognised Association of Official Agricultural Chemists (AOAC) methods (2005). In detail, the moisture content was calculated by vacuum freezing and drying in an oven. The content of crude protein and crude fat was determined by the Kjeldahl method and the Soxhlet extraction method, respectively. Total ash content was determined via high-temperature burning.

Fatty acid and amino acid profiles analyses

Fatty acid profile analysis

From 1.0 g of lyophilised LDM or BFM sample, total lipids were extracted using chloroform-methanol (2:1, v/v) according to Folch et al. (1957). Aliquots of lipids were methylated using acid (5% methanolic HCl) and base (0.5 N sodium methoxide) catalysis independently (Kramer et al. 2008). Before the FA was methylated, 1 mL of henedecanoic acid methyl ester (11:0) was employed as an internal reference (1 mg/mL). FA methyl esters (FAME) were analysed using a Varian 450-GC gas chromatograph (Varian Chromatography Systems, Walnut Creek, CA) equipped with a flame-ionisation detector and a fused silica capillary column (SP-2560, 100 m, 0.25 mm internal diameter and 0.20 µm film thickness; Supelco Inc., Bellefont, PA). The injector and detector temperatures were kept at 260 °C. The initial oven temperature of 120 °C was maintained for 5 min, increased at 3 °C/min to 230 °C and maintained for 3 min, and increased at 1.5 °C/min to 240 °C and maintained for 13 min. As a carrier gas, 1 mL/min of nitrogen was utilised, and 1 µL of the sample was injected. An automatic split injector with a split ratio of 1:30. Individual FAME was identified by comparing their retention times to those of authentic standards (FAME mix components from Supelco Inc.; c9t11- and t10c12-CLAs from Larodan Fine Chemicals, Solna, AB, Sweden), and their retention times were calculated according to Vahmani et al. (2017). Table 4 includes only FAMEs comprising > 0.01% of total FAMEs.

Amino acid profile analysis

The amino acid content of the LDM and BFM meats was measured using an amino acid analyser (Hitachi L-8900, Tokyo, Japan) with certain modifications, as described by Xu et al. (2019). In brief, 50 mg (exactly 0.1 mg) of the freeze-dried and ground muscle sample (LDM and BFM) was transferred to a glass bottle, and 10 mL of 6 mol HCl was added. The mixture was hydrolysed at 110 °C for 22 h after being filled with nitrogen. The hydrolysate was then transferred to a 50 mL volumetric flask and diluted in a calibrated tube with ultrapure water. A 0.22 µm membrane filter was used to filter the solution into an autosampler vial.

Statistical analysis

The experimental data was composed of carcase traits, and pH, drip loss and cooking loss of LDM, and proximate chemical analysis, fatty acids and amino acids of both LDM and BFM, and sample numbers of all measured parameters were six. The mixed linear model in SAS software version 9.4 (SAS Inc., Cary, NC) was used for the analysis of carcase traits, and pH, drip loss and cooking loss of LDM, with the system (G, SG and SF) being fixed effects and animal ID being a random factor, followed by LSmeans to display results with standard errors of the mean (SEM). Statistical analysis for the data of proximate chemical analysis, fatty acids and amino acids of both LDM and BFM was performed using by a mixed linear model (SAS version 9.4; SAS Inc). In the mixed effects model, the system (G, SG and SF), muscle (LDM and BFM) and the interaction effects of system and muscle are treated as fixed factors, and animal ID is treated as a random factor with body weight of lambs as a covariate, and results presented as LSmeans with SEM. Differences were significant when p < 0.05 and had a tendency when 0.05 < p < 0.10. If the effects of system × muscle were < 0.05 for specific indicators, interaction plots were drawn with GraphPad Prism version 9 software (GraphPad Software, Inc., La Jolla, CA) according to Lsmeans of these indicators comparisons for effects of system × muscle.

Results

Carcase traits and meat physicochemical properties

Carcase traits and meat physicochemical properties are shown in Table 2. The greatest carcase weight was found in the SF group, compared to these in the control and the SG groups (p < 0.05). The pH_45min and pH_24h of LDM in the G group was significantly higher than that of LDM in the SG group (p < 0.05); however, there was no significant difference for the SF group compared to the G and SG groups (p > 0.05).

Table 2. Effects of different rearing systems on carcase traits and meat physicochemical properties of Gangba lambs.

Items	System^1			SEM	p Value
	G	SG	SF
Carcass traits
Carcass weight, kg	10.23^c	11.79^b	13.56^a	0.50	0.005
Dressing percentage, %	42.25	45.75	45.17	0.89	0.315
GR, mm	10.22	12.45	14.07	0.57	0.086
Meat physicochemical properties
pH45 min	6.83^a	6.52^b	6.62^ab	0.05	0.046
pH24 h	5.81^a	5.26^b	5.55^ab	0.08	0.028
Drip loss, %	9.11	6.58	9.06	1.59	0.776
Cooking loss, %	33.96	34.84	34.12	1.92	0.978

¹ G: grazing; SG: semi-grazing; SF: stall-feeding.

² GR: Total tissue thickness between the 12th and 13th rib, 11 cm from the midline.

^a,b,c Values in the same row with different superscript letters are statistically different at p < 0.05.

Basic chemical composition analysis

The results of the proximate chemical analysis of lamb meat are shown in Table 3. There was a significant difference in the effect of system × muscle on the fat in meat (p > 0.05), which demonstrated SG-BFM had lower fat content than SG-LDM (p = 0.038, Figure 1(A)). In terms of position, ash in BFM was significantly higher than that in LDM (p < 0.05).

Figure 1. Interaction effects between the system and the muscle on fat content (A), the concentration of C18:1n-9 (B), MUFA (C), Pro (D) and the ratio of EAA: NEAA (E); G: grazing group; SG: semi-grazing group; SF: stall-feeding group; LDM: the longissimus dorsi muscle; BFM: the biceps femoris muscle.

Table 3. Effects of different rearing systems on meat proximate chemical analysis of Gangba sheep (%, DM basis).

Items	System^1			Muscle^2		SEM	p Value
	G	SG	SF	LDM	BFM		System	Muscle	System × Muscle
Moisture	73.30	73.93	73.04	72.98	73.87	0.59	0.622	0.241	0.876
Protein	21.97	21.24	21.57	22.05	21.13	0.50	0.649	0.215	0.885
Fat	2.41	2.05	2.64	2.54	2.20	0.31	0.502	0.100	0.035
Ash	0.90	0.85	1.01	0.71^b	1.12^a	0.17	0.451	0.011	0.336

¹ G: grazing; SG: semi-grazing; SF: stall-feeding.

² LDM: the longissimus dorsi muscle; BFM: the biceps femoris muscle.

^a,b Values in the same row with different superscript letters are statistically different at p < 0.05 but within systems or muscles.

Fatty acid profile

The data of determined fatty acids in lamb meat is displayed in Table 4. A total of 29 fatty acids were identified in this study, and 13, 6 and 10 fatty acids were classified as being saturated fatty acids (SFA), monounsaturated fatty acids (MUFA) and PUFA, respectively, commonly for all groups. The dominant SFAs were palmitic acid (C16:0) and stearic acid (C18:0) in lamb meat, while the dominant MUFA was oleic acid (C18:1), and the dominant PUFAs were linoleic acid (C18:2n-6), C18:3n-3, and arachidonic acid (C20:4n-6), commonly across all groups of system treatments and different kinds of muscle. A system × muscle interaction was found for the concentration of both C18:1n-9 (p = 0.045) and MUFA (p = 0.041), where SG-BFM had a lower concentration of C18:1n-9 (p = 0.012, Figure 1(B)) or MUFA (p = 0.025, Figure 1(C)), respectively, as compared to SG-LDM. Concerning the system, the ratio of n-6/n-3 in G and SG lamb meat was significantly lower than that in SF lamb meat (p < 0.05). In contrast, compared to SF lamb meat, G and SG lamb meat had significantly higher concentrations of arachidic acid (C20:0), erucic acid (C22:1n-9), C18:3n-3, CLA-c9t11 and CLA-t10c12 (p < 0.05). However, levels of and gadoleic acid (C20:1) in G lamb meat were significantly higher than those in SF lamb meat, and C16:1 in SG lamb meat was significantly lower than that in G and SG lamb meats (p < 0.05). In terms of the muscle, pentadecanoic acid (C15:0), C16:0, margaric acid (C17:0), C20:1, C21:0, C22:1n-9, C18:2n-6, C18:3n-3, CLA-t10c12, C20:4n-6, C20:5n-3, C22:6n-3, the total of PUFA, P/S, n-3 and n-6 fatty acids in LDM were significantly lower than those in BFM (p < 0.05); however, C16:0 had a contrasting result to these above-mentioned fatty acids between LDM and BFM (p < 0.05).

Table 4. Effects of different rearing systems on fatty acids profile in the meat of Gangba sheep (g 100 g⁻¹ of fatty acid methyl esters (FAMEs).

Fatty acids^1	System^2			Muscle^3		SEM	p Value
	G	SG	SF	LDM	BFM		System	Muscle	System × Muscle
C8:0	0.02	0.02	0.02	0.02	0.02	<0.01	0.376	0.262	0.834
C10:0	0.14	0.14	0.14	0.15	0.14	0.01	0.924	0.629	0.936
C12:0	0.12	0.12	0.13	0.11	0.13	0.02	0.990	0.357	0.981
C14:0	2.27	2.24	2.49	2.33	2.34	0.19	0.712	0.968	0.845
C15:0	0.37	0.36	0.37	0.34^b	0.40^a	0.02	0.877	0.006	0.594
C16:0	24.24	24.39	27.24	26.01^a	24.57^b	0.65	0.057	0.040	0.940
C17:0	1.15	1.13	1.26	1.12^b	1.25^a	0.04	0.153	0.017	0.715
C18:0	18.60	19.79	18.11	18.89	18.78	0.83	0.333	0.852	0.314
C20:0	0.19^a	0.17^a	0.13^b	0.16	0.17	0.01	0.004	0.345	0.787
C21:0	0.60	0.60	0.51	0.50^b	0.63^a	0.05	0.562	0.047	0.544
C22:0	0.10	0.09	0.06	0.08	0.09	0.01	0.081	0.065	0.406
C23:0	0.14	0.13	0.13	0.12	0.14	0.01	0.830	0.066	0.561
C24:0	0.12^a	0.12^a^b	0.09^b	0.10	0.11	0.01	0.202	0.101	0.798
SFA	47.91	49.32	50.67	50.15	48.45	0.83	0.267	0.071	0.792
C14:1	0.08	0.07	0.08	0.07	0.08	0.01	0.423	0.105	0.870
C16:1	1.87^a	1.57^b	1.79^a	1.68	1.81	0.08	0.048	0.177	0.860
C18:1n-9	39.69	38.71	39.68	39.60	39.12	1.02	0.794	0.092	0.045
C20:1	0.14^a	0.12^a^b	0.10^b	0.11^b	0.13^a	<0.01	0.019	0.023	0.865
C22:1n-9	0.05^a	0.04^a	0.03^b	0.04	0.04	<0.01	0.009	0.487	0.705
C24:1	0.10^a	0.09^a	0.08^b	0.08^b	0.10^a	0.01	0.229	0.053	0.581
MUFA	41.99	40.60	41.70	41.57	41.29	1.06	0.707	0.274	0.041
C18:2n-6	5.28	5.43	4.22	4.43^b	5.62^a	0.32	0.117	0.012	0.454
C18:3n-3	1.15^a	1.03^a	0.65^b	0.85^b	1.03^a	0.09	0.040	0.024	0.720
CLA c9t11	0.21^a	0.24^a	0.13^b	0.19	0.21	0.01	0.001	0.157	0.488
CLA t10c12	0.11^a	0.11^a	0.07^b	0.09^b	0.11^a	<0.01	0.004	0.048	0.620
C20:3n-6	0.18	0.25	0.23	0.20	0.24	0.02	0.160	0.076	0.064
C20:3n-3	0.03	0.03	0.02	0.02^b	0.03^a	<0.01	0.275	0.093	0.200
C20:4n-6	2.38	2.18	1.86	1.85^b	2.43^a	0.18	0.353	0.024	0.532
C20:5n-3	0.63	0.54	0.34	0.44^b	0.57^a	0.07	0.151	0.044	0.453
C22:2	0.09	0.08	0.08	0.08	0.08	<0.01	0.085	0.146	0.696
C22:6n-3	0.19	0.17	0.11	0.13^b	0.19^a	0.02	0.056	0.023	0.459
PUFA	10.25	10.06	7.72	8.27^b	10.42^a	0.64	0.099	0.015	0.464
P/S	0.21	0.21	0.15	0.17^b	0.22^a	0.01	0.072	0.012	0.547
n-3	2.00	1.77	1.12	1.45^b	1.82^a	0.17	0.065	0.030	0.555
n-6	8.16	8.21	6.52	6.75^b	8.51^a	0.48	0.125	0.014	0.449
n-6/n-3	4.13^b	4.69^b	5.86^a	4.93	4.86	0.26	0.006	0.812	0.849

¹ SFA: saturated fatty acids (sum of C8:0, C10:0, C12:0, C14:0, C15:0, C16:0, C17:0, C18:0, C20:0, C21:0, C22:0, C23:0 and C24:0); MUFA: monounsaturated fatty acids (sum of C14:1, C16:1, C18:1n9c, C20:1, C22:1n9 and C24:1); PUFA: polyunsaturated fatty acids (sum of C18:2n-6c, C18:3n-3, CLA-c9t11, CLA-t10c12, C20:3n-6, C20:3n-3, C20:4n-6, C20:5n-3, C22:2, C22:6n-3), n-3 = n-3 PUFA (sum of C18:3n-3, C20:3n-3, C20:5n-3 and C22:6n-3), n-6 = n-6 PUFA (sum of C18:2n-6c, CLA-c9t11, CLA-t10c12, C20:3n-6 and C20:4n-6).

² G: grazing; SG: semi-grazing; SF: stall-feeding.

³ LDM: the longissimus dorsi muscle; BFM: the biceps femoris muscle.

^a,b Values in the same row with different superscript letters are statistically different at p < 0.05 but within systems or muscles.

Amino acid profile

The results of identified amino acids in lamb meat are shown in Table 5. In this study, 17 amino acids were found in lamb meat. A system × position interaction was observed on proline (Pro) (p = 0.011) with SG-BFM having the higher concentration of Pro, compared to G-BFM (p = 0.001), SF-BFM (p = 0.016) and SG-LDM (p = 0.004) (Figure 1(D)), respectively. Similarly, a system × muscle interaction was also observed on EAA/NEAA (p = 0.020), where the ratio of EAA/NEAA in SG-BFM was significantly lower than those in G-BFM (p < 0.001), SG-LDM (p < 0.001) and SF-BFM (p = 0.007). EAA/NEAA in SF-LDM was higher than that in SF-BFM (p = 0.009) (Figure 1(E)). In terms of the muscle, valine (Val), isoleucine (Ile), phenylalanine (Phe) and histidine (His) in LDM were significantly higher than those in BFM (p < 0.05).

Table 5. Effects of different rearing systems on amino acid profile in the meat of Gangba sheep (g/100 g DM basis).

Amino acids^1	System^2			Muscle^3		SEM	p Value
	G	SG	SF	LDM	BFM		System	Muscle	System × Muscle
Asp	7.09	7.17	7.06	7.14	7.08	0.10	0.698	0.608	0.691
Thr	3.57	3.59	3.56	3.59	3.56	0.05	0.902	0.283	0.374
Ser	3.01	3.01	2.98	2.99	3.01	0.05	0.927	0.773	0.326
Glu	12.67	12.83	12.55	12.61	12.75	0.18	0.661	0.072	0.590
Pro	2.47	2.64	2.53	2.52	2.58	0.04	0.028	0.218	0.011
Gly	3.34	3.53	3.33	3.33	3.47	0.07	0.139	0.087	0.095
Ala	4.73	4.85	4.72	4.74	4.80	0.07	0.500	0.271	0.318
Cys	0.17	0.16	0.16	0.16	0.17	0.01	0.763	0.179	0.457
Val	3.89	3.92	3.87	3.97^a	3.81^b	0.06	0.866	<0.001	0.445
Met	2.08	2.07	2.13	2.13	2.06	0.04	0.641	0.239	0.589
Ile	3.62	3.58	3.52	3.64^a	3.51^b	0.03	0.965	0.001	0.184
Leu	6.05	6.14	6.15	6.14	6.08	0.09	0.819	0.214	0.107
Tyr	2.84	2.86	2.85	2.88	2.81	0.05	0.976	0.084	0.185
Phe	3.67	3.74	3.75	3.81^a	3.63^b	0.05	0.577	0.009	0.485
His	3.60	3.69	3.82	3.86^a	3.54^b	0.07	0.319	0.002	0.632
Lys	6.79	6.84	6.79	6.86	6.76	0.09	0.925	0.098	0.202
Arg	4.37	4.44	4.34	4.38	4.39	0.05	0.426	0.896	0.679
TAA	74.06	75.05	74.16	74.75	74.10	1.07	0.817	0.231	0.132
EAA	29.64	29.89	29.71	30.13	29.36	0.30	0.644	0.075	0.891
NEAA	44.23	45.19	44.35	44.62	44.56	0.44	0.264	0.862	0.443
EAA/NEAA	0.67	0.66	0.67	0.67	0.66	<0.01	0.005	<0.001	0.020

¹ TAA: total amino acids; EAA: essential amino acids (sum of Val, Met, Ile, Leu, Phe, Lys and Thr); NEAA: non-essential amino acids (sum of Asp, Ser, Glu, Pro, Gly, Ala, Cys, Tyr, His and Arg).

²G: grazing; SG: semi-grazing; SF: stall-feeding.

³ LDM: the longissimus dorsi muscle; BFM: the biceps femoris muscle.

^a,b Values in the same row with different superscript letters are statistically different at p < 0.05 but within systems or muscles.

Discussion

Carcase traits and meat physicochemical properties

Carcase traits are of economic importance in meat production due to the relevance of these parameters to economic profits for animal-raising farmers and enterprises. Carcase traits generally consist of live weight before slaughter, carcase weight, dressing percentage and GR (rib tissue thickness), and are affected by various rearing systems (Zhang et al. 2022; 2022). The results of this study are like those found in Yao (2021) and Joy et al. (2008), who demonstrated that the carcase weight of lambs in the grazing group were lower than in the barn feeding group. This may be attributed to the dietary supplementation of concentrate in the SG system. Compared to the G group, the SG and SF groups had higher carcase weight, due to higher energy intake and optimal balance of energy and protein in concentrates (Turner et al. 2014). Based on the theory above, supplying lambs grazed on pasture with appropriate amounts of concentrate to achieve higher carcase weight was recommended (Wang et al. 2021).

Meat physicochemical properties, such as pH, cooking loss and drip loss are closely related to the sensory evaluation of cooked meat and affect the quality of meat during storage. Meat pH, an essential post-slaughter factor, plays a significant role in meat quality traits, such as tenderness and juiciness (Lambertz et al. 2014). The decreased pH results from post-mortem glycolysis in muscle, positively affecting meat tenderness (Ziauddin et al. 1994). Influences of feeding systems on meat pH (15 min and 24 h) reported in studies were not always consistent. Some studies reported the pH_24 h of LDM of the grazed lambs was higher than that of the feedlot-feeding lambs, for meat produced from pastured animals was reported to have a lower content of glycogen, which is used as the glycolytic substrate to produce lactic acid in muscle tissue, thus leading to a higher ultimate pH (Ramírez-Retamal et al. 2014; De Brito et al. 2017). Some other studies demonstrated that feeding systems (grazing feeding vs. feedlot feeding) had no effects on meat quality (Ripoll et al. 2012; Wang et al. 2021), similar to our results. The different results of these studies on effects of feeding systems on meat pH may be attributed to different animal breeds, diet composition and inter-individual differences in stress before slaughter.

Overall, the SF and SG can improve carcase traits through increasing carcase weight, and the G and SG groups had affected meat pH (45 min and 24 h).

Basic chemical composition in meat

Protein and fat contents are of great importance to the nutritional value and sensory characteristics of lamb meat. In this study, there was no significant difference in the contents of moisture, protein, fat, and ash in lamb meat across the three groups, which agrees with results reported by Majdoub-Mathlouthi et al. (2015). In BFM, ash percentage – expressing muscle mineral content – was significantly higher than that of LDM. A possible reason may be that ash content is closely related to the amount of muscle exercise; the more muscle exercise, the higher the ash content, as minerals in body tissues affect hormonal secretion, enzyme activity and muscle function (Peters and Mahan 2008). A system × muscle interaction was observed with SG-BFM possessing lower fat content than SG-LDM. In general, there are metabolic differences between various types of muscles, as BFM is more prone to use fat as an important energy source for more movement, resulting in lower fat content in BFM than in LDM. In addition, SG feeding and management strategies are intermediate between G and SF. Therefore, the diversity and complexity of the nutrients, the growing environment and the amount of movement could become more pronounced to have a combined effect, leading to a greater disparity in the fat content of BFM and LDM in SG, which could be a possible reason to explain why the interaction effect was reflected on fat content in various muscle of the only SG group above mentioned.

In a word, the feeding regimens have no effects on the chemical composition of lamb meat.

Fatty acid profile

Fatty acids in lamb meat, especially essential fatty acids, are critical to human health and closely related to the flavour of lamb meat, because some fatty acids are precursors of flavour compounds. Feeding regimens (G, SG and SF) can affect the fatty acid composition of lamb meat, as the dietary fatty acid composition (from grass, concentrate or a combination) varies within different feeding systems, manipulating the final fatty acids composition in lamb meat. Regarding the effects of rearing systems on SFA in lamb meat, SFA – like C20:0 – in the pasture is higher than those in concentrates. Synthesis of a SFA in ruminants is inhibited if diets are rich in this SFA (Chilliard 1993). Furthermore, de novo synthesis of SFA is increased with a higher dietary energy intake (Aurousseau et al. 2007). Thus, C20:0 should be lower in G and SG groups as expected. However, contrary to the principle in this study. C20:0 in G and SG lamb meat were significantly higher than that in SF lamb meat. Further studies are needed to determine the cause of these results. The elongation of oleic acid (C18:1n-9) forms eicosenoic acid (C20:1n-9), and further elongation produces erucic acid (C22:1n-9). However, levels of C20:1n-9 and C22:1n-9 in the G group were significantly higher than those in the SF group, though their precursor (C18:1n-9) was not different within groups. A system × muscle interaction effect was observed regarding C18:1n-9 and MUFA, such that SG-BFM had lower C18:1n-9 and MUFA than SG-LDM. IMF content is related to the composition of fatty acids, including C18:1n-9 and other MUFAs. Higher levels of IMF generally lead to higher concentrations of MUFAs like oleic acid (C18:1n-9) (Da Silva et al. 2018). The higher fat content in SG-LDM compared to SG-BFM discussed above may elucidate the effect of interaction on the content of C18:1n-9 and MUFA.

For the effects of rearing systems on PUFA, in many livestock production systems, diets of pasture and forage are common sources of n-3 PUFA (Ponnampalam et al. 2021). Festuca wallichanica, Kobresia deasgi and Kobresia capillifolia are three dominant pasture species in Gangba County; the first one belongs to the Festuca genus, while the last two are within the Kobresia genus. The average content of C18:3n-3 in Festuca and Kobresia genus grasses are up to 38.87% and 47.16%, respectively (Guo et al. 2012; Noviandi et al. 2012; Cui et al. 2016), and grasses mainly composed of these pastures used for feeding lambs contain up to 51.12% C18:3n-3. In addition, bioactive compounds like flavonoids and polysaccharides in grasses can inhibit microbial hydrogenation in the rumen (Durmic et al. 2008), leading to certain PUFA (like C18:3n-3) escaping hydrogenation in the rumen microbiome, and finally being absorbed in the small intestine. The CLAs proportion in ruminant fats is up to 2%, and CLA-c9t11 is the major CLA isomer (on average, 67% of total CLA measured within groups in this study; Kuhnt et al. 2011). CLA-c9t11 originates either from C18:2n-6 biohydrogenation in the rumen or from endogenous Δ9-desaturation of vaccenic acid (C18:1t11), which derives from C18:2n-6 and C18:3n-3 biohydrogenation (Agradi et al. 2020). Thus, the higher concentration of C18:3n-3 in the pasture of G and SG indirectly leads to a higher concentration of CLA-c9t11 in lambs’ meat. Another study also confirmed that a higher concentration of C18:3n-3 in the ruminant diet leads to a higher concentration of CLA-c9t11 in ruminant products (Agradi et al. 2020). De Brito et al. (2017) found that ruminants grazed on pasture had a higher concentration of CLA-c9t11 in meat, which agrees with this study’s result. For the summary index of fatty acids within groups, the ratio of n-6 and n-3 PUFA is the most critical parameter to evaluate the nutritional value of meat. The ratio of n-6/n-3 PUFA of lamb meat in the G and SG groups was closer to the value of 4:1 recommended by the European Food Safety Authority (EFSA, 2009), indicating meat of the G and SG lambs was more beneficial to human health compared to that of the SF lambs. SG can be an alternative feeding system to G based on the fatty acid composition in meat, and meat in both systems is healthier for humans compared to that in the SF system for the abundantly important n-3 PUFA (C18:3n-3). In addition, various strategies are recommended for the intensive rearing system to improve the concentration of health-claimed fatty acids through manipulating the nutrient composition of basic ruminant diets, such as supplementing plant extracts and essential oils.

In terms of the effects of different kinds of muscles on fatty acid profiles, previous studies showed that there were significant differences in the fatty acid profile in meat from various parts of the sheep carcase, and the results of the differences in fatty acid profiles in the same studied muscles within different experiments are not always consistent due to different breeds, ages and diets (Bolte et al. 2002; Ge 2019; Wang et al. 2021). In this study, SFA (C15:0; C17:0 and C21:0), UFA (unsaturated fatty acids) belonging to n-6 (C18:2n-6 and C20:4n-6) and n-3 (C18:3n-3, C20:5n-3 and C22:6n-3), MUFA (C20:1), and summary parameters (PUFA, P/S, n-3 and n-6) in LDM was significantly lower than those in BFM. The reason for this may be that higher PUFA and MUFA are stored in slow-oxidative muscle fibres of BFM compared to being stored in fast glycolytic muscle fibres of LDM, and PUFA and MUFA can mediate insulin receptors to improve glucose disposal in BFM to generate energy for rapid and transient movement compared to that of LDM (Storlien et al. 1995; Martínez-González et al. 2008). However, C16:0 in LDM was significantly higher than that in BFM.

In summary, G and the SG feeding regimens can produce lamb meat with high nutritional value due to the higher deposition of the beneficial fatty acid (especially C18:3n-3) and the better compositional structure of fatty acids in muscles.

Amino acid profile

Amino acids are essential for meat flavour and play crucial roles in physiological function and human health. The primary amino acid profile of lamb meat was not significantly affected by different feeding regimes. As for the effects of the various muscles on amino acid profiles, levels of Val, Ile, Phe and His in LDM were significantly higher than those in BFM. The variations in amino acid composition between these two tissue types could be attributed to their distinct functional roles, fibre type distribution and metabolic demands, which might influence the utilisation and synthesis of specific amino acids. In addition, Val, Ile, Phe and His as EAA can promote good growth performance in humans. Therefore, the amino acid profile shows that LDM has a more excellent nutritional value than BFM. The EAA/NEAA ratio is around 0.51, a low limit considered adequate for good dietary quality based on amino acid content (Brown and Jeffrey 1992). In this trial, the range of EAA/NEAA ratios within systems and different muscles is between 0.66 and 0.67, indicating it is of good nutritional quality for human health. Similar to the reasons for the system × muscle interaction effects on the content of fat in meat, combined effects of various nutrient intake and differential muscle metabolism types may explain the exited system × muscle interaction effects on the concentration of Pro and the EAA/NEAA, and the accurate mechanism explaining the interaction effect is needed.

All in all, feeding regimens had little effect on amino acid content.

Conclusions

The feeding systems had no effects on chemical composition and little influence on amino acid composition. The traditional grazing rearing and SG systems improved lamb meat quality by increasing the presence of beneficial fatty acids. In contrast, the SF regimen improved the carcase weight of Gangba lambs without increasing their meat quality compared to the grazing rearing and SG systems. The directions of future efforts for breeders are to improve carcase traits (like carcase weight) of lambs in both natural grazing and SG systems and the meat quality of lambs raised in feedlots.

Ethical Approval

The experimental protocol was approved by the Institutional Animal Care and Use Committee of the Chinese Academy of Agricultural Sciences, and the treatment, housing, husbandry, and slaughtering conditions conformed to the Experimental Animal Care and Use Guidelines issued by Chinese Science and Technology Committee.

Acknowledgements

The authors thank the staff of the Mengde village cooperative in Gangba County for their technical support in slaughtering and preparing carcasses.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Data availability statement

The data that support the findings of this study are available from the corresponding authors upon reasonable request.

Additional information

Funding

This work was supported by the Key Research Projects (No. XZ202001ZY0037N) and the Science and Technology Major Projects (No. XZ202101ZD0001N) from Tibet Autonomous Region and the Central Public-interest Scientific Institution Basal Research Fund (No. 110233160007016) and the Inner Mongolia Autonomous Region.