Effects of Dietary Protein Levels on Growth Performance, Carcass Traits, Serum Metabolites, and Meat Composition of Tibetan Sheep during the Cold Season on the Qinghai-Tibetan Plateau
by
Xungang Wang
1,2, 
Tianwei Xu
1,
Xiaoling Zhang
1,2,
Yuanyue Geng
1,2,
Shengping Kang
1,2 and
Shixiao Xu
1,* 1
Northwest Institute of Plateau Biology, Chinese Academy of Sciences, Xining 810001, China
2
University of Chinese Academy of Sciences, Beijing 100049, China
*
Author to whom correspondence should be addressed.
Animals 2020, 10(5), 801; https://doi.org/10.3390/ani10050801
Submission received: 14 April 2020
/
Revised: 2 May 2020
/
Accepted: 4 May 2020
/
Published: 6 May 2020
(This article belongs to the Special Issue Feeds and Feeding Programs in Functional Meat Production)
Abstract
:Simple Summary
The Tibetan sheep (Ovis aries) is an ovine breed well adapted to the harsh plateau environment. For a long period of time, Tibetan sheep farming has been an important pillar industry for native herders on the Qinghai-Tibetan Plateau. With the increasing demand for sheep meat and products, nutrition research has gained increasing importance. In this study, the effects of three different dietary protein levels (10.1%, 12.1%, and 14.1%) on growth performance, carcass traits, serum metabolites, and meat composition were investigated in Tibetan sheep during the cold season. The results showed that the diets containing 12.1% and 14.1% protein were better than a diet containing 10.1% protein for enhancing the growth performance, carcass performance, and meat products of the Tibetan sheep.
Abstract
Dietary protein is a critical nutrient that directly influences the health and production of livestock. Recent studies showed that protein supplements could enhance the growth performance of Tibetan sheep. However, there is a lack of information regarding the influence of dietary protein levels on carcass traits and meat composition. This study investigated the effects of dietary protein levels on growth performance, carcass traits, serum metabolites, and meat composition in Tibetan sheep during the cold season on the Qinghai-Tibetan Plateau. A total of eighteen 1-year-old, healthy, castrated Tibetan sheep with similar initial body weights (31.7 ± 0.72 kg) were randomly divided into three treatment groups with different dietary protein level (low protein (LP, 10.1%); medium protein (MP, 12.1%); high protein (HP, 14.1%)) diets. The results indicated that the Tibetan sheep fed with the MP and HP diets had greater final body weights (BWs), average daily gains (ADGs), and average daily feed intakes (ADFIs) (p < 0.05). The MP and HP diets also improved the hot carcass weight, net meat (including the fat) weight, and bone weight of the sheep significantly (p < 0.05). Besides, the dietary protein levels could significantly affect the serum concentrations of growth hormone (p < 0.05). The diameter of muscle fibers in the MP group was significantly greater than that in the LP group (p < 0.05), while the density of muscle fibers showed the opposite trend. The dietary protein levels only significantly (p < 0.05) influenced the ether extract content and profile content of the longissimus dorsi muscle but had no effect on other parameters of meat composition. In summary, our results indicate that dietary protein levels affect growth performance, carcass traits, and meat composition and that diets containing 12.1% and 14.1% protein are recommended to obtain better production performance and meat products in Tibetan sheep, rather than a diet containing 10.1% protein, during the cold season on the Qinghai-Tibetan Plateau.
1. Introduction
The Qinghai-Tibetan Plateau (QTP) is a special ecosystem with an extreme environment, including a high altitude, a low temperature, and strong UV radiation [1,2]. Tibetan sheep (Ovis aries) are an important livestock resource, raised at an altitude above 3000 m on the QTP [3]. At present, there are more than fifty million Tibetan sheep well adapted to the harsh environment and that provide meat and other economic production for about five million native Tibetan herders [4,5,6]. Based on traditional livestock management, Tibetan sheep graze on the natural grazing lands all year-round [7]. However, during the long periods of cold season, there is a desperate shortage of grassland productivity and herbage nutrition, and Tibetan sheep often lose live-weight [8,9]. In recent years, a new production system is being adopted on the QTP. During the warm season (June to October, average temperature approximately −2 to 12 °C) sheep are largely dependent on natural grazing lands, but in the cold season (November to the following May, average temperature from approximately −5 to −15 °C), the sheep are housed and fed in sheds to ensure normal growth [10]. Under this novel production system, the growth and development of sheep can be improved effectively. Therefore, a better understanding of how to efficiently feed sheep would be beneficial for livestock production on the QTP.
As an important nutrient in diets, protein is a crucial for livestock’s nutrient digestibility and production performance [11]. Previous studies showed that feeding protein supplements could significantly promote growth performance, feed efficiency, and economic benefits in Tibetan sheep [12]. Furthermore, several studies reported that supplementing Tibetan sheep during the cold season could also increase rumen microbial growth and improve rumen epithelium development and absorptive capability [7,13]. However, these studies focused on the growth performance and rumen function of sheep, with less attention to carcass traits, serum metabolites, muscle fiber characteristics, and meat composition. Hence, the objective of this study was to evaluate the effects of feeding different levels of dietary protein to Tibetan sheep on their growth performance, serum metabolites, carcass traits, and meat composition during the cold season on the QTP.
2. Materials and Methods
2.1. Ethics Statement
The animal procedures in this study were performed according to the Guideline for the Care and Use of Laboratory Animals in China. This study was approved by the Experimental Animal Use Ethics Committee of the Northwest Institute of Plateau Biology, CAS (Permit No. NWIPB20160302).
2.2. Experimental Design
Eighteen 1-year-old, healthy, castrated Tibetan sheep with similar initial body weights (BWs) of 31.7 ± 0.72 kg were selected from Haibei Demonstration Zone of Plateau Modern Ecological Husbandry Science and Technology in Qinghai Province (China) for the feeding trial. The sheep were randomly divided into three dietary treatment groups, with each group containing 6 sheep. The protein levels of the three diets were 10.1% (low protein, LP), 12.1% (medium protein, MP), 14.1% (high protein, HP). The diets were designed according to the National Research Council [14] and were isoenergetic (10.1 MJ metabolizable energy (ME)/kg). The ingredients and nutrient compositions of three diets are shown in Table 1 and the analysis of nutrient composition in the diets was performed according to the Association of Official Analytical Chemists (AOAC) procedures [15]. All diets had the same forage to concentrate ratio of 50:50. The concentrate and oat hay were manually mixed and fed (dry matter basis) at 3.5% BW of sheep [16]. The sheep were fed twice daily at 8:00 and 17:00 with the same amount, and each sheep was maintained in an individual pen. Fresh water was provided ad libitum throughout the experiment. The whole formal experiment took place over 105 d after 15 d of adaption to the experimental diets. Sheep were weighted on d 0, d 35, d 70, and d 105 before feeding in the morning to calculate the average daily gain (ADG), and feed intake was recorded each day to calculate the average daily feed intake (ADFI) and feed/gain ratio (F/G).
2.3. Carcass Traits
At the end of the experiment, four sheep from each group were selected randomly and transported to a commercial abattoir located 16 km away from the experimental site. Sheep were fasted for 24 h before slaughter. At the commercial abattoir, the sheep were stunned and slaughtered humanely according to standard commercial procedures (NY 467-2001, The Ministry of Agriculture of the People’s Republic of China). The hot carcass weight, net meat (including the fat) weight, and bone weight were recorded and used to calculate the carcass traits. These parameters were calculated as follows: % carcass yield = hot carcass weight/live weight × 100; % net meat (including the fat) yield = net meat (including the fat) weight/live weight × 100; bone/meat = bone weight/net meat (including the fat) weight.
2.4. Serum Metabolites
At the end of the experiment, 10 mL of blood was collected from the jugular vein of each sheep before feeding in the morning, and the serum was separated by centrifugation at 2000× g for 10 min at 4 °C. The concentration of serum growth hormone (GH) was determined by the sheep GH ELISA kit (CV% < 15%, CUSABIO Biotech Co. Ltd., Wuhan, China) according to the instruction manual, and the levels of total protein (TP), albumin (ALB), glucose (GLU), globulin (GLO), total cholesterol (TCH), triglyceride (TG), glutamic-pyruvic transaminase (ALT), and glutamic oxaloacetic transaminase (AST) in the serum were determined by using the Catalyst One Biochemical Analyzer (Idexx Laboratories, Westbrook, ME, USA).
2.5. Muscle Fiber Characteristics
After slaughter, samples of longissimus dorsi muscle adjacent to the 13th thoracic vertebra (approximately 1 cm3) from each sheep were collected and fixed in tissue fixation fluid overnight. After dehydration in a series of ethanol gradient solutions (70%, 80%, 90%, and then 95% anhydrous alcohol for 2 min at each solution) and inducing transparency with xylene, samples were embedded in paraffin and were sectioned in serial transverse sections (5 μm thick). Dewaxed serial sections were stained with the traditional hematoxylin and eosin (HE) method to show the histological characteristics of the muscle fibers [17]. The morphological characteristics of the muscle fibers (e.g., diameter, perimeter, area, and density) were measured using CaseViewer 2.2 (3DHISTECH Ltd., Budapest, Hungary) under an electron microscope (Axio IMAGE Z2, Leica microsystems Ltd., Wetzlar, Germany).
2.6. Meat Composition
At the time of slaughter, samples of longissimus dorsi muscle between the 9th and 11th ribs (approximately 200 g) were collected from each sheep to measure nutrient contents. Dry matter, crude protein, ether extract, and crude ash contents were assayed according to the AOAC procedures [15]. The concentrations of 17 common amino acids were determined with an automatic amino acid analyzer (S433D, Sykam Ltd., Munich, Germany) according to the methods described by Peterson et al. [18].
2.7. Statistical Analyses
All the data in this study are presented as the mean values and the standard errors of the mean (SEM), and analyzed by using one-way ANOVA and Tukey post hoc tests in IBM SPSS 22.0 (SPSS Inc., Chicago, IL, USA). In this study, the diet was treated as the main effect, and the sheep was the experimental unit. Significance was declared at p < 0.05.
3. Results
3.1. Growth Performance
The effects of dietary protein levels on the BW, ADG, ADFI, and F/G of Tibetan sheep are shown in Table 2. At the first feeding stage (1–35 d), the dietary protein levels did not significantly (p > 0.05) affect the final BW, ADG, and F/G of the Tibetan sheep. During the second feeding stage (36–70 d), the final BW in the LP group was significantly lower than that in the MP group (p < 0.05). The ADG and F/G were significantly different between groups commencing during the last feeding stage (71–105 d), and the LP group had the lowest ADG and the greatest value of F/G (p < 0.05). During the whole experiment (1–105 d), the LP group had the lowest final BW, ADG, and ADFI and the greatest value of F/G (p < 0.05).
3.2. Carcass Traits
The effects of dietary protein levels on carcass traits are shown in Table 3. The live weight, hot carcass weight, net meat (including the fat) weight, and bone weight in the LP group were significantly lower than those in the MP and HP groups (p < 0.05). The HP group had the greatest value for the bone/meat ratio value (p < 0.05). By contrast, the dietary protein levels did not significantly (p > 0.05) influence the carcass yield and net meat (including the fat) yield of the groups of Tibetan sheep.
3.3. Serum Metabolites
The effects of dietary protein levels on serum metabolites are shown in Table 4. The level of GH in the LP group was significantly lower than that in the MP and HP groups (p < 0.05). Nevertheless, dietary protein levels had no significant effect on serum TP, ALB, GLU, GLO, TCH, TG, ALT, and AST content (p > 0.05).
3.4. Muscle Fiber Characteristics
As shown in Figure 1, the diameter of muscle fibers in the LP group was significantly lower than that in the MP group (p < 0.05), while no significant difference was detected between the MP and HP groups (p > 0.05) or between the LP and HP groups (p > 0.05). For the density of muscle fibers, the greatest value was detected in the LP group. Dietary protein levels did not significantly (p > 0.05) influence the perimeter and area of muscle fibers.
3.5. Nutrient Contents of the Longissimus Dorsi Muscle
The ether extract was significantly lower in the longissimus dorsi muscle of sheep in the LP group than in the MP group (p < 0.05) (Table 5). Dietary protein levels had no significant influence on the dry matter, crude protein, and crude ash contents of longissimus dorsi muscle (p > 0.05).
3.6. Amino Acid Profile of Longissimus Dorsi Muscle
As shown in Table 6, eight essential amino acids (EAA) and nine nonessential amino acids (NEAA) in the longissimus dorsi muscle of Tibetan sheep were detected by an automatic amino acid analyzer. The content of proline was significantly lower in the LP group than that in the MP group (p < 0.05), but no differences between groups were observed in other amino acids.
4. Discussion
4.1. Growth Performance
Recent studies had showed that dietary nutrient level was closely related to the growth performance of livestock [19,20,21]. Besides, it is reported that the proportion of concentrate to forage could also affect the BW, ADG, and F/G of calves and Tibetan sheep [16,22,23]. In the present study, the dietary protein levels did not significantly influence the BW and ADG of Tibetan sheep during the first feeding stage (1–35 d). During the whole experiment (1–105 d), the greater final BW, ADG, and ADFI observed in the MP and HP groups indicates that these diets are optimal for achieving the best growth performance of Tibetan sheep during the cold season on the QTP. Furthermore, the LP group had a greater value of F/G than other two groups, indicating that the LP diet had the lowest feed conversion efficiency of these three diets. Similar findings were observed by Estrada-Angulo et al. [24], and it was reported that increasing the dietary protein level could increase the ADG and gain efficiency of Pelibuey × Katahdin lambs. Karlsson and Martinsson [11] also found that the lambs fed with high protein supplements had a greater total gain and ADG and more efficient feed conversion. Based on these previous reports and our findings, we speculate that an appropriate dietary protein level could enhance protein availability and increase amino acid absorption in animals and eventually result in increased growth performance [25,26].
4.2. Carcass Traits
In recent years, carcass traits are crucial indices reflecting livestock production in animal husbandry [27,28,29]. Francisco et al. [30] showed that the live BW and diet composition were two main factors associated with carcass traits, and these observations were also found in our study. As the LP diet contained lower levels of nutrients than other two diets, the sheep in the LP group exhibited poorer growth performance, as shown by the lower hot carcass weight, net meat (including the fat) weight, and bone weight. Furthermore, Cortese et al. [31] reported that the carcass yield of Charolais bulls was not affected by increased dietary protein levels. Luo et al. [28] also showed that there were no differences in backfat thickness and carcass yield in fattening pigs fed with different levels of β-glucan supplementation. The above results were consistent with the results of this study. Although the hot carcass weight changed with the dietary protein levels, the carcass yield and net meat (including the fat) yield were independent of the respective dietary protein.
4.3. Serum Metabolites
Serum metabolites are important biochemical parameters reflecting the health status of an animal and its metabolic activity [32]. In recent years, serum biomarkers have been used as diagnostic standards for assessing animal health due to their convenient and economical features [7,33,34]. Recent research had reported that greater GH levels enhance lipid mobilization in animals, which is essential in promoting muscle and bone growth [35,36]. Our study found that the GH levels in sheep in the LP group were significantly lower than in sheep in the MP and HP groups. The results for the serum concentrations of TP, ALB, GLU, GLO, TCH, TG, ALT, and AST from the sheep in all three groups were within the normal physiological range, but no differences among treatments were detected. This is consistent with the previous findings that dietary concentrate levels had no significant effect on most blood parameters in Holstein heifers [37]. Our results also showed that providing the Tibetan sheep with adequate nutrition under the cold season could ensure their normal metabolism and physiological functions.
4.4. Muscle Fiber Characteristics
Muscle fiber structure is a quantitative index to evaluate the meat composition at the cellular level [38]. In the present study, we found that the histological characteristics of the longissimus dorsi muscle fibers in Tibetan sheep could significantly affected by the dietary protein levels, and the diameter of muscle fibers was negatively correlated with density. Şirin et al. [39] reported that there was a strong relationship between muscle fiber composition and the growth performance of lambs. Fahey et al. [40] showed that the diet composition and nutritional status could alter the muscle fiber development of newborn lambs. Furthermore, the effects of a high nutritional level may involve an increase in and prolongation of myoblast proliferation [41]. In our study, the sheep fed the LP diet had the lowest diameters of muscle fibers, possibly due to poorer growth performance and lower dietary nutrition intake. Unfortunately, observations regarding the different types of muscle fiber (e.g., Type I, Type IIA, and Type IIB) were not recorded in the present study, which would help to understand whether dietary protein levels had any deeper effects on the muscle fibers of Tibetan sheep.
4.5. Meat Composition
Previous studies have indicated that dietary nutrients play a pivotal role in regulating the meat composition of livestock. For instance, increased dietary energy increased the content of intramuscular fat of Holstein-Friesians bulls [42]. Moreover, dietary supplementation with sea buckthorn pomace increased the crude fat content of lambs, but had no significant influence on other nutrient contents [43]. In the present study, we found that dietary protein levels significantly affect the ether extract content of Tibetan sheep, and the MP group had the greatest value. A previous study reported that diet composition, particularly the protein/energy ratio, could influence fatness [44]. In our study, the MP and HP diets had higher abundances of protein components (e.g., soybean meal and rapeseed meal) and contributed to the greater ADFI of Tibetan sheep. In this sense, the greater ether extract content may also be associated with the elevated nutrient intake. Yin et al. [45] reported that the composition and content of amino acids are critical evaluation indices, which are associated with the flavor and nutritional value of meat. Our results showed that the meat of Tibetan sheep was rich in a variety of essential and nonessential amino acids like other livestock (e.g., Hu sheep, the Hengshan goat, and Yanbian cattle) distributed in the low-altitude areas of China [46,47,48]. It indicated that Tibetan sheep meat appears to be an excellent quality protein food source for native residents living at altitudes greater than 3000 m on the QTP. Besides, these results showed that the content of amino acids in longissimus dorsi muscle may not be directly related to dietary protein levels, and the specific reasons for this still need to be explored in further depth.
5. Conclusions
Based on the results, Tibetan sheep fed with the MP diet (containing 12.1% protein) and HP diet (containing 14.1% protein) had better growth performance, associated with elevated serum GH but no differences in other serum biochemical parameters. Furthermore, dietary protein levels could affect the histological characteristics of the longissimus dorsi muscle in Tibetan sheep. The results suggest that changes in the diet composition may affect the ether extract content of the longissimus dorsi muscle by altering the food intake of the Tibetan sheep. This study could facilitate applications in Tibetan sheep production during the cold season on the QTP.
Author Contributions
Conceptualization, X.W. and S.X.; Investigation, X.W. and S.X.; Methodology, T.X., X.Z. and Y.G.; Project administration, X.W. and Y.G.; Resources, S.K.; Writing—original draft, X.W.; Writing—review and editing, T.X. and S.X. All authors have read and agreed to the published version of the manuscript.
Funding
This work was supported by the “Strategic Leading Science & Technology Program” of the Chinese Academy of Sciences (XDA23060603, XDA2005010406), National Key R&D Plan (2016YFC0501905, 2016YFC0501805), “Key Technology Support Program” of Qinghai Province (2019-SF-149, 2017-NK-153, 2019-NK-173).
Conflicts of Interest
The authors declare no conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.
References
- Huang, J.Q.; Li, Y.J.; Luo, Y.Z. Bacterial community in the rumen of Tibetan sheep and Gansu alpine fine-wool sheep grazing on the Qinghai-Tibetan Plateau, China. J. Gen. Appl. Microbiol. 2017, 63, 122–130. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Xue, B.; Zhao, X.Q.; Zhang, Y.S. Seasonal changes in weight and body composition of yak grazing on alpine-meadow grassland in the Qinghai-Tibetan plateau of China. J. Anim. Sci. 2005, 83, 1908–1913. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhou, J.W.; Guo, X.S.; Degen, A.A.; Zhang, Y.; Liu, H.; Mi, J.D.; Ding, L.M.; Wang, H.C.; Qiu, Q.; Long, R.J. Urea kinetics and nitrogen balance and requirements for maintenance in Tibetan sheep when fed oat hay. Small Ruminant Res. 2015, 129, 60–68. [Google Scholar] [CrossRef]
- Li, J.B.; Zhu, W.Z.; Luo, M.R.; Ren, H.H.; Tang, L.; Liao, H.H.; Wang, Y. Molecular cloning, expression and purification of lactoferrin from Tibetan sheep mammary gland using a yeast expression system. Protein Expr. Purif. 2015, 109, 35–39. [Google Scholar] [CrossRef] [PubMed]
- Dong, S.K.; Long, R.J.; Kang, M.Y.; Pu, X.P.; Guo, Y.J. Effect of urea multinutritional molasses block supplementation on liveweight change of yak calves and productive and reproductive performances of yak cows. Can. J. Anim. Sci. 2003, 83, 141–145. [Google Scholar] [CrossRef]
- Sun, Y.; Angerer, J.P.; Hou, F.J. Effects of grazing systems on herbage mass and liveweight gain of Tibetan sheep in Eastern Qinghai-Tibetan Plateau, China. Rangeland J. 2015, 37, 181–190. [Google Scholar] [CrossRef] [Green Version]
- Jing, X.P.; Peng, Q.H.; Hu, R.; Zou, H.W.; Wang, H.Z.; Yu, X.Q.; Zhou, J.W.; Degen, A.; Wang, Z.S. Dietary supplements during the cold season increase rumen microbial abundance and improve rumen epithelium development in Tibetan sheep. J. Anim. Sci. 2018, 96, 293–305. [Google Scholar] [CrossRef]
- Long, R.J.; Apori, S.O.; Castro, F.B.; Orskov, E.R. Feed value of native forages of the Tibetan Plateau of China. Anim. Feed Sci. Technol. 1999, 80, 101–113. [Google Scholar] [CrossRef]
- Zhao, X.Q.; Zhou, X.M. Ecological basis of Alpine meadow ecosystem management in Tibet: Haibei Alpine Meadow Ecosystem Research Station. Ambio 1999, 28, 642–647. [Google Scholar] [CrossRef]
- Zhao, X.Q.; Zhao, L.; Li, Q.; Chen, H.; Zhou, H.K.; Xu, S.X.; Dong, Q.M. Using balance of seasonal herbage supply and demand to inform sustainable grassland management on the Qinghai–Tibetan Plateau. Front. Agr. Sci. Eng. 2018, 5, 1–8. [Google Scholar] [CrossRef] [Green Version]
- Karlsson, L.; Martinsson, K. Growth performance of lambs fed different protein supplements in barley-based diets. Livest. Sci. 2011, 138, 125–131. [Google Scholar] [CrossRef]
- Xu, T.W.; Xu, S.X.; Hu, L.Y.; Zhao, N.; Liu, Z.; Ma, L.; Liu, H.J.; Zhao, X.Q. Effect of dietary types on feed intakes, growth performance and economic benefit in Tibetan sheep and yaks on the Qinghai-Tibet plateau during cold season. PLoS ONE 2017, 12, e0169187. [Google Scholar] [CrossRef] [PubMed]
- Jing, X.P.; Peng, Q.H.; Hu, R.; Wang, H.Z.; Yu, X.Q.; Degen, A.; Zou, H.W.; Bao, S.K.; Zhao, S.N.; Wang, Z.S. Effect of supplements during the cold season on the reproductive system in prepubertal Tibetan sheep ewes. Anim. Sci. J. 2017, 88, 1269–1278. [Google Scholar] [CrossRef] [PubMed]
- NRC. Nutrient Requirements of Small Ruminants: Sheep, Goats, Cervids, and New World Camelids; National Research Council; National Academies Press: Washington, DC, USA, 2007. [Google Scholar]
- AOAC. Official Methods of Analysis, 18th ed.; Association of Official Analytical Chemists: Gaithersburg, MD, USA, 2007. [Google Scholar]
- Liu, H.; Xu, T.; Xu, S.; Ma, L.; Han, X.; Wang, X.; Zhang, X.; Hu, L.; Zhao, N.; Chen, Y.; et al. Effect of dietary concentrate to forage ratio on growth performance, rumen fermentation and bacterial diversity of Tibetan sheep under barn feeding on the Qinghai-Tibetan plateau. Peer J. 2019, 7, e7462. [Google Scholar] [CrossRef] [Green Version]
- Siqin, Q.; Nishiumi, T.; Yamada, T.; Wang, S.; Liu, W.; Wu, R.; Borjigin, G. Relationships among muscle fiber type composition, fiber diameter and MRF gene expression in different skeletal muscles of naturally grazing Wuzhumuqin sheep during postnatal development. Anim. Sci. J. 2017, 88, 2033–2043. [Google Scholar] [CrossRef] [Green Version]
- Peterson, M.B.; Ferguson, A.G.; Lesch, M. A method for the determination of amino acid incorporation into protein and the specific activity of tissue amino acid in small cardiac muscle samples. J. Mol. Cell. Cardiol. 1973, 5, 547–552. [Google Scholar] [CrossRef]
- Zhang, H.B.; Wang, Z.S.; Peng, Q.H.; Tan, C.; Zou, H.W. Effects of different levels of protein supplementary diet on gene expressions related to intramuscular deposition in early-weaned yaks. Anim. Sci. J. 2014, 85, 411–419. [Google Scholar] [CrossRef]
- Peng, Q.H.; Khan, N.A.; Xue, B.; Yan, T.H.; Wang, Z.S. Effect of different levels of protein concentrates supplementation on the growth performance, plasma amino acids profile and mTOR cascade genes expression in early-weaned yak calves. Asian Australas. J. Anim. Sci. 2018, 31, 218–224. [Google Scholar] [CrossRef] [Green Version]
- Balasubramanian, B.; Park, J.H.; Shanmugam, S.; Kim, I.H. Influences of enzyme blend supplementation on growth performance, nutrient digestibility, fecal microbiota and meat-quality in grower-finisher pigs. Animals 2020, 10, 386. [Google Scholar] [CrossRef] [Green Version]
- Castells, L.; Bach, A.; Aris, A.; Terre, M. Effects of forage provision to young calves on rumen fermentation and development of the gastrointestinal tract. J. Dairy Sci. 2013, 96, 5226–5236. [Google Scholar] [CrossRef] [Green Version]
- Miller-Cushon, E.K.; DeVries, T.J. Effect of early feed type exposure on diet-selection behavior of dairy calves. J. Dairy Sci. 2011, 94, 342–350. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Estrada-Angulo, A.; Castro-Pérez, B.I.; Urías-Estrada, J.D.; Ríos-Rincón, F.G.; Arteaga-Wences, Y.J.; Barreras, A.; López-Soto, M.A.; Plascencia, A.; Zinn, R.A. Influence of protein level on growth performance, dietary energetics and carcass characteristics of Pelibuey × Katahdin lambs finished with isocaloric diets. Small Ruminant Res. 2018, 160, 59–64. [Google Scholar] [CrossRef]
- Tayengwa, T.; Chikwanha, O.C.; Dugan, M.E.R.; Mutsvangwa, T.; Mapiye, C. Influence of feeding fruit by-products as alternative dietary fibre sources to wheat bran on beef production and quality of Angus steers. Meat Sci. 2020, 161, 107969. [Google Scholar] [CrossRef] [PubMed]
- Rivera-Mendez, C.; Plascencia, A.; Torrentera, N.; Zinn, R.A. Effect of level and source of supplemental tannin on growth performance of steers during the late finishing phase. J. Appl. Anim. Res. 2017, 45, 199–203. [Google Scholar] [CrossRef] [Green Version]
- Silva, L.H.P.; Assis, D.E.F.; Estrada, M.M.; Assis, G.J.F.; Zamudio, G.D.R.; Carneiro, G.B.; Valadares Filho, S.C.; Paulino, M.F.; Chizzotti, M.L. Carcass and meat quality traits of Nellore young bulls and steers throughout fattening. Livest. Sci. 2019, 229, 28–36. [Google Scholar] [CrossRef]
- Luo, J.; Zeng, D.; Cheng, L.; Mao, X.; Yu, J.; Yu, B.; Chen, D. Dietary beta-glucan supplementation improves growth performance, carcass traits and meat quality of finishing pigs. Anim. Nutr. 2019, 5, 380–385. [Google Scholar] [CrossRef]
- Wang, W.; Chen, D.; Yu, B.; Huang, Z.; Luo, Y.; Zheng, P.; Mao, X.; Yu, J.; Luo, J.; He, J. Effect of dietary inulin supplementation on growth performance, carcass traits, and meat quality in growing-finishing pigs. Animals 2019, 9, 840. [Google Scholar] [CrossRef] [Green Version]
- Francisco, A.E.; Janíček, M.; Dentinho, T.; Portugal, A.P.V.; Almeida, J.M.; Alves, S.P.; Fialho, L.; Jerónimo, E.; Bessa, R.J.B.; Santos-Silva, J. Effects of alfalfa particle size and starch content in diets on feeding behaviour, intake, rumen parameters, animal performance and meat quality of growing lambs. Meat Sci. 2020, 161, 107964. [Google Scholar] [CrossRef]
- Cortese, M.; Segato, S.; Andrighetto, I.; Ughelini, N.; Chinello, M.; Schiavon, E.; Marchesini, G. The effects of decreasing dietary crude protein on the growth performance, feed efficiency and meat quality of finishing Charolais bulls. Animals 2019, 9, 906. [Google Scholar] [CrossRef] [Green Version]
- Ding, L.M.; Chen, J.Q.; Degen, A.A.; Qiu, Q.; Liu, P.P.; Dong, Q.M.; Shang, Z.H.; Zhang, J.J.; Liu, S.J. Growth performance and hormonal status during feed restriction and compensatory growth of Small-Tail Han sheep in China. Small Ruminant Res. 2016, 144, 191–196. [Google Scholar] [CrossRef]
- Burçak, E.; Yalçın, S. Effects of dietary sepiolite usage on performance, carcass characteristics, blood parameters and rumen fluid metabolites in Merino cross breed lambs. Appl. Clay Sci. 2018, 163, 291–298. [Google Scholar] [CrossRef]
- Wang, S.; Ma, T.; Zhao, G.; Zhang, N.; Tu, Y.; Li, F.; Cui, K.; Bi, Y.; Ding, H.; Diao, Q. Effect of age and weaning on growth performance, rumen fermentation, and serum parameters in lambs fed starter with limited ewe-lamb interaction. Animals 2019, 9, 825. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abribat, T.; Deslauriers, N.; Brazeau, P.; Gaudreau, P. Alterations of pituitary growth hormone-releasing factor binding sites in aging rats. Endocrinology 1991, 128, 633–635. [Google Scholar] [CrossRef] [PubMed]
- Hornick, J.L.; Van Eenaeme, C.; Gérard, O.; Dufrasne, I.; Istasse, L. Mechanisms of reduced and compensatory growth. Domest. Anim. Endocrinol. 2000, 19, 121–132. [Google Scholar] [CrossRef]
- Zhang, J.; Shi, H.; Wang, Y.; Li, S.; Zhang, H.; Cao, Z.; Yang, K. Effects of limit-feeding diets with different forage-to-concentrate ratios on nutrient intake, rumination, ruminal fermentation, digestibility, blood parameters and growth in Holstein heifers. Anim. Sci. J. 2018, 89, 527–536. [Google Scholar] [CrossRef]
- Werner, C.; Riegel, J.; Wicke, M. Slaughter performance of four different turkey strains, with special focus on the muscle fiber structure and the meat quality of the breast muscle. Poult. Sci. 2008, 87, 1849–1859. [Google Scholar] [CrossRef]
- Şirin, E.; Aksoy, Y.; Uğurlu, M.; Çiçek, Ü.; Önenç, A.; Ulutaş, Z.; Şen, U.; Kuran, M. The relationship between muscle fiber characteristics and some meat quality parameters in Turkish native sheep breeds. Small Ruminant Res. 2017, 150, 46–51. [Google Scholar] [CrossRef]
- Fahey, A.J.; Brameld, J.M.; Parr, T.; Buttery, P.J. The effect of maternal undernutrition before muscle differentiation on the muscle fiber development of the newborn lamb. J. Anim. Sci. 2005, 83, 2564–2571. [Google Scholar] [CrossRef]
- Brigitte, P.; Louis, L.; Cécile, B.; Michel, J.D. Muscle fibre ontogenesis in farm animal species. Reprod. Nutr. Dev. 2002, 42, 415–431. [Google Scholar] [CrossRef] [Green Version]
- Wang, H.; Li, H.; Wu, F.; Qiu, X.; Yu, Z.; Niu, W.; He, Y.; Su, H.; Cao, B. Effects of dietary energy on growth performance, rumen fermentation and bacterial community, and meat quality of Holstein-Friesians bulls slaughtered at different ages. Animals 2019, 9, 1123. [Google Scholar] [CrossRef] [Green Version]
- Qin, X.; Zhang, T.; Cao, Y.; Deng, B.; Zhang, J.; Zhao, J. Effects of dietary sea buckthorn pomace supplementation on skeletal muscle mass and meat quality in lambs. Meat Sci. 2020, 166, 108141. [Google Scholar] [CrossRef] [PubMed]
- Gómez, R.S.; Lewis, A.J.; Miller, P.S.; Chen, H.Y.; Diedrichsen, R.M. Body composition and tissue accretion rates of barrows fed corn-soybean meal diets or low-protein, amino acid-supplemented diets at different feeding levels. J. Anim. Sci. 2002, 80, 654–662. [Google Scholar] [CrossRef] [PubMed]
- Yin, H.D.; Gilbert, E.R.; Chen, S.Y.; Wang, Y.; Zhang, Z.C.; Zhao, X.L.; Zhang, Y.; Zhu, Q. Effect of hybridization on carcass traits and meat quality of erlang mountainous chickens. Asian Australas. J. Anim. Sci. 2013, 26, 1504–1510. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiao, Y.; Liu, Y.; Quek, S.Y. Systematic evaluation of nutritional and safety characteristics of Hengshan goat leg meat affected by multiple thermal processing methods. J. Food Sci. 2020, 85, 1344–1352. [Google Scholar] [CrossRef] [PubMed]
- Wang, Q.; Wang, Y.; Hussain, T.; Dai, C.; Li, J.; Huang, P.; Li, Y.; Ding, X.; Huang, J.; Ji, F.; et al. Effects of dietary energy level on growth performance, blood parameters and meat quality in fattening male Hu lambs. J. Anim. Physiol. Anim. Nutr. 2020, 104, 418–430. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.X.; Jin, H.G.; Yan, C.G.; Seo, K.S.; Zhang, L.C.; Ren, C.Y.; Jin, X. Association of CAST gene polymorphisms with carcass and meat quality traits in Yanbian cattle of China. Mol. Biol. Rep. 2013, 40, 1875–1881. [Google Scholar] [CrossRef]
Figure 1.
Effects of the three different dietary protein levels on the histological characteristics of longissimus dorsi muscle in Tibetan sheep. (A) Diameter of muscle fibers. (B) Perimeter of muscle fibers. (C) Area of muscle fibers. (D) Density of muscle fibers. a, b Indicate significant differences among three groups.
Figure 1.
Effects of the three different dietary protein levels on the histological characteristics of longissimus dorsi muscle in Tibetan sheep. (A) Diameter of muscle fibers. (B) Perimeter of muscle fibers. (C) Area of muscle fibers. (D) Density of muscle fibers. a, b Indicate significant differences among three groups.
Table 1.
Ingredients and nutrient levels of the experimental diets with three different protein levels (on a dry matter basis).
Table 1.
Ingredients and nutrient levels of the experimental diets with three different protein levels (on a dry matter basis).
| Item | Diet 1 | ||
|---|---|---|---|
| LP | MP | HP | |
| Ingredients, g/kg | |||
| Oat hay | 500 | 500 | 500 |
| Corn grain | 210 | 165 | 120 |
| Wheat grain | 135 | 120 | 105 |
| Wheat bran | 70 | 75 | 80 |
| Soybean meal | 35 | 55 | 75 |
| Rapeseed meal | 25 | 60 | 95 |
| NaCl | 5 | 5 | 5 |
| CaHPO4·2H2O | 3 | 3 | 3 |
| Bentonite | 5 | 5 | 5 |
| CaCo3 | 4.5 | 4.5 | 4.5 |
| NaHCO3 | 2.5 | 2.5 | 2.5 |
| Premix 2 | 5 | 5 | 5 |
| Nutrient levels 3 | |||
| CP (%) | 10.1 | 12.1 | 14.1 |
| ME (MJ/kg) | 10.1 | 10.1 | 10.1 |
| EE (%) | 2.7 | 2.8 | 2.9 |
| NDF (%) | 37.5 | 38.5 | 39.5 |
| ADF (%) | 19.1 | 20.1 | 21.1 |
| Ca (%) | 0.6 | 0.7 | 0.7 |
| P (%) | 0.4 | 0.5 | 0.5 |
1 LP: low protein; MP: medium protein; HP: high protein. 2 Premix provided per kg of feed: Vitamin A, 50,000 IU; Vitamin D3, 12,500 IU; Vitamin E, 1000 IU; Cu, 250 mg; Fe, 12,000 mg; Zn, 1000 mg; Mn, 1000 mg; and Se, 7.5 mg. 3 ME: metabolizable energy = total digestible nutrients × 0.04409 × 0.82, according the National Research Council [14]; CP: crude protein; EE: ether extract; NDF: neutral detergent fiber; ADF: acid detergent fiber.
Table 2.
Effects of three different dietary protein levels on growth performance in Tibetan sheep (n = 6 per group).
Table 2.
Effects of three different dietary protein levels on growth performance in Tibetan sheep (n = 6 per group).
| Parameter 1 | Treatments | SEM 2 | p-Value | ||
|---|---|---|---|---|---|
| LP | MP | HP | |||
| 1–35 d | |||||
| Initial BW, kg | 31.6 | 32.1 | 31.3 | 0.17 | 0.123 |
| Final BW, kg | 36.3 | 38.1 | 37.2 | 0.42 | 0.221 |
| ADG, g/d | 133.8 | 169.8 | 167.9 | 13.26 | 0.488 |
| ADFI, g/d | 797 c | 926 a | 870 b | 0.01 | 0.000 |
| F/G | 5.99 | 5.55 | 5.24 | 0.33 | 0.669 |
| 36–70 d | |||||
| Initial BW, kg | 36.3 | 38.1 | 37.2 | 0.42 | 0.221 |
| Final BW, kg | 41.4 b | 45.3 a | 42.7 ab | 0.58 | 0.010 |
| ADG, g/d | 144.8 | 204.5 | 155.5 | 13.12 | 0.139 |
| ADFI, g/d | 1268 b | 1465 a | 1289 b | 0.03 | 0.001 |
| F/G | 8.74 | 7.28 | 8.30 | 0.27 | 0.063 |
| 71–105 d | |||||
| Initial BW, kg | 41.4 b | 45.3 a | 42.7 ab | 0.58 | 0.010 |
| Final BW, kg | 47.8 b | 55.7 a | 52.8 a | 1.00 | 0.001 |
| ADG, g/d | 184.3 b | 297.1 a | 291.0 a | 17.39 | 0.004 |
| ADFI, g/d | 1518 b | 1880 a | 1783 a | 0.04 | 0.000 |
| F/G | 8.39 a | 6.43 b | 6.19 b | 0.35 | 0.011 |
| 1–105 d | |||||
| Initial BW, kg | 31.6 | 32.1 | 31.3 | 0.17 | 0.123 |
| Final BW, kg | 47.8 b | 55.7 a | 52.8 a | 1.00 | 0.001 |
| ADG, g/d | 154.3 b | 223.8 a | 204.8 a | 9.51 | 0.002 |
| ADFI, g/d | 1195 c | 1424 a | 1314 b | 23.13 | 0.000 |
| F/G | 7.87 a | 6.33 b | 6.53 b | 0.27 | 0.033 |
Values are expressed as means. 1 BW, body weight; ADG, average daily gain; ADFI, average daily feed intake; F/G, feed/gain ratio. 2 SEM = standard error of the mean. a, b, c Values within a row with different superscripts differ significantly at p < 0.05.
Table 3.
Effects of three different dietary protein levels on carcass traits in Tibetan sheep (n = 4 per group).
Table 3.
Effects of three different dietary protein levels on carcass traits in Tibetan sheep (n = 4 per group).
| Parameter | Treatments | SEM 1 | p-Value | ||
|---|---|---|---|---|---|
| LP | MP | HP | |||
| Live weight, kg | 47.8 b | 54.0 a | 53.5 a | 0.993 | 0.002 |
| Hot carcass weight, kg | 22.20 b | 26.91 a | 26.19 a | 0.747 | 0.005 |
| Carcass yield, % | 46.48 | 49.82 | 48.97 | 0.732 | 0.156 |
| Net meat (including the fat) weight, kg | 17.41 b | 21.05 a | 19.95 a | 0.568 | 0.009 |
| Net meat (including the fat) yield, % | 36.46 | 38.96 | 37.31 | 0.588 | 0.224 |
| Bone weight, kg | 4.79 b | 5.86 a | 6.24 a | 0.205 | 0.001 |
| Bone/meat | 0.27 b | 0.28 b | 0.31 a | 0.006 | 0.001 |
Values are expressed as means. 1 SEM = standard error of the mean. a, b Values within a row with different superscripts differ significantly at p < 0.05.
Table 4.
Effects of three different dietary protein levels on serum metabolites in Tibetan sheep (n = 6 per group).
Table 4.
Effects of three different dietary protein levels on serum metabolites in Tibetan sheep (n = 6 per group).
| Parameter | Treatments | SEM 1 | p-Value | ||
|---|---|---|---|---|---|
| LP | MP | HP | |||
| Growth hormone (GH), ng/mL | 32.5 b | 36.1 a | 35.5 a | 2.05 | 0.001 |
| Total protein (TP), g/L | 69.0 | 69.2 | 70.9 | 2.55 | 0.136 |
| Albumin (ALB), g/L | 35.4 | 36.4 | 36.1 | 1.63 | 0.342 |
| Glucose (GLU), mmol/L | 4.68 | 4.82 | 4.81 | 0.35 | 0.561 |
| Globulin (GLO), g/L | 33.6 | 32.8 | 34.8 | 2.97 | 0.236 |
| Total cholesterol (TCH), mmol/L | 1.46 | 1.67 | 1.66 | 0.29 | 0.140 |
| Triglyceride (TG), mmol/L | 0.29 | 0.32 | 0.30 | 0.08 | 0.664 |
| Glutamic-pyruvic transaminase (ALT), U/L | 19.6 | 17.2 | 19.3 | 5.02 | 0.458 |
| Glutamic-oxalacetic transaminase (AST), U/L | 108.8 | 115.2 | 102.7 | 22.85 | 0.420 |
Values are expressed as means. 1 SEM = standard error of the mean. a, b Values within a row with different superscripts differ significantly at p < 0.05.
Table 5.
Effects of three different dietary protein levels on the nutrient contents of the longissimus dorsi muscle in Tibetan sheep (n = 4 per group).
Table 5.
Effects of three different dietary protein levels on the nutrient contents of the longissimus dorsi muscle in Tibetan sheep (n = 4 per group).
| Parameter | Treatments | SEM 1 | p-Value | ||
|---|---|---|---|---|---|
| LP | MP | HP | |||
| Dry matter, % | 24.09 | 26.39 | 24.86 | 0.465 | 0.113 |
| Crude protein, % | 18.63 | 19.38 | 19.27 | 0.205 | 0.287 |
| Ether extract, % | 2.48 b | 3.43 a | 2.68 ab | 0.169 | 0.033 |
| Crude ash, % | 1.02 | 1.09 | 0.99 | 0.024 | 0.236 |
Values are expressed as means. 1 SEM = standard error of the mean. a, b Values within a row with different superscripts differ significantly at p < 0.05.
Table 6.
Effects of three different dietary protein levels on the amino acid profile of longissimus dorsi muscle in Tibetan sheep (n = 4 per group).
Table 6.
Effects of three different dietary protein levels on the amino acid profile of longissimus dorsi muscle in Tibetan sheep (n = 4 per group).
| Amino Acid 1 | Treatments | SEM 2 | p-Value | ||
|---|---|---|---|---|---|
| LP | MP | HP | |||
| Threonine, % | 3.89 | 3.77 | 4.03 | 0.05 | 0.101 |
| Valine, % | 4.26 | 4.13 | 4.19 | 0.04 | 0.495 |
| Methionine, % | 2.15 | 2.21 | 2.22 | 0.04 | 0.821 |
| Leucine, % | 4.13 | 4.02 | 4.15 | 0.05 | 0.582 |
| Leucine, % | 6.96 | 6.83 | 7.16 | 0.09 | 0.325 |
| Phenylalanine, % | 3.51 | 3.46 | 4.03 | 0.14 | 0.208 |
| Histidine, % | 4.20 | 3.88 | 3.84 | 0.09 | 0.197 |
| Lysine, % | 7.29 | 7.55 | 7.58 | 0.09 | 0.393 |
| Asparticacid, % | 7.80 | 7.64 | 8.00 | 0.09 | 0.284 |
| Serine, % | 3.29 | 3.18 | 3.44 | 0.05 | 0.050 |
| Glutamicacid, % | 14.77 | 14.22 | 15.00 | 0.19 | 0.235 |
| Glycine, % | 3.51 | 3.44 | 3.62 | 0.05 | 0.255 |
| Alanine, % | 4.82 | 4.70 | 4.90 | 0.06 | 0.365 |
| Cystine, % | 0.23 | 0.18 | 0.16 | 0.02 | 0.236 |
| Tyrosine, % | 3.04 | 2.91 | 3.40 | 0.12 | 0.249 |
| Arginine, % | 5.14 | 4.92 | 5.32 | 0.08 | 0.159 |
| Proline, % | 2.75 bc | 2.73 b | 2.98 a | 0.04 | 0.004 |
| EAA, % | 36.38 | 35.85 | 37.20 | 0.31 | 0.218 |
| NEAA, % | 45.36 | 43.90 | 46.82 | 0.56 | 0.091 |
| TAA, % | 78.99 | 77.02 | 81.04 | 0.82 | 0.134 |
Values are expressed as means. 1 EAA, essential amino acids; NEAA, nonessential amino acids; TAA, total amino acids. 2 SEM = standard error of the mean. a, b, c Values within a row with different superscripts differ significantly at p < 0.05.
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Wang, X.; Xu, T.; Zhang, X.; Geng, Y.; Kang, S.; Xu, S. Effects of Dietary Protein Levels on Growth Performance, Carcass Traits, Serum Metabolites, and Meat Composition of Tibetan Sheep during the Cold Season on the Qinghai-Tibetan Plateau. Animals 2020, 10, 801. https://doi.org/10.3390/ani10050801
AMA Style
Wang X, Xu T, Zhang X, Geng Y, Kang S, Xu S. Effects of Dietary Protein Levels on Growth Performance, Carcass Traits, Serum Metabolites, and Meat Composition of Tibetan Sheep during the Cold Season on the Qinghai-Tibetan Plateau. Animals. 2020; 10(5):801. https://doi.org/10.3390/ani10050801
Chicago/Turabian StyleWang, Xungang, Tianwei Xu, Xiaoling Zhang, Yuanyue Geng, Shengping Kang, and Shixiao Xu. 2020. "Effects of Dietary Protein Levels on Growth Performance, Carcass Traits, Serum Metabolites, and Meat Composition of Tibetan Sheep during the Cold Season on the Qinghai-Tibetan Plateau" Animals 10, no. 5: 801. https://doi.org/10.3390/ani10050801
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