Recent advances in feed and nutrition of beef cattle in China — A review

The beef cattle industry in China has advanced remarkably since its reform and opening up; consequently, China has become the world’s third-largest beef cattle producer. China is also one of the countries with the most substantial research input and output in the field of beef cattle feed and nutrition. The progress and innovation by China in the research field of beef cattle feed and nutrition have undoubtedly promoted the development of the domestic beef cattle industry. This review summarizes recent advances in feed resource development, nutrient requirements, and nutritional regulation of beef cattle in China. Limitations in current research and perspectives on future work are also discussed.


INTRODUCTION
The vigorous development of beef cattle farming can alleviate the competition for grains between humans and livestock and help improve the dietary structure of humans. Additionally, beef cattle farming contributes to rural revitalization in China. Given these factors, China has been increasing support for beef cattle farming and related research over the past decades.
China has become the world's third-largest beef cattle producer, with an annual beef output of 6.72 million tonnes in 2020 [1]. At present, China's GDP ranks second in the world, with a per capita GDP of US $12,500. Brazil is the world's largest beef cattle producer, with a per capita GDP of US $8,000. However, the annual per capita consumption of beef in Brazil is 32.7 kg, more than four times that of China (Statista, https://www.statista. com). The low per capita beef consumption in China is due to the Chinese dietary habit of preferring pork and chicken. Beef cattle industry in China was established late. Before that, cattle, as important draught animals, were forbidden to be slaughtered without permission, which made it difficult to establish beef consumption habits. However, as machines have replaced cattle for ploughing in recent decades, slaughtering cattle for food is no longer restricted. Chinese people have gradually incorporated more beef into their diet, resulting in the sustained and rapid growth of per capita consumption of beef, highlighting China as a promising market. Driven by domestic beef consumption demand, the beef industry in China is expected to further develop and become more prominent in the global beef industry. However, China's beef cattle industry has been facing multiple issues that restrict its efficient and sustainable development ( Figure 1). The production efficiency of the beef cattle industry in China lags behind that of other developed countries, and the total yield of high-grade beef in China is much lower than domestic consumption. This is mainly because of the backward feeding management strategies and cattle breeding. Diets mainly consist of medium-and low-quality roughage, resulting in a low feed conversion rate and slow growth rate of beef cattle. Furthermore, according to the National Breed List of Livestock and Poultry Genetic Resources (2021 Edition), China has 80 beef cattle (Bos taurus) breeds, including 55 local breeds, 15 imported breeds, and 10 cultivated breeds. Local beef cattle breeds and their hybrid offspring make up the main body of the beef cattle farming industry in China. However, the body size and production efficiency of most of these breeds are poor. Beef cattle often face various environmental stresses, such as heat and cold stresses, which deteriorate animal welfare and farming profits [2][3][4]. In addition, beef cattle farming produces many pollutants, particularly methane [5]. In recent years, the Chinese government has promulgated a series of strict environmental protection laws that pose severe challenges to beef cattle farming in China.
Feed and nutrition research plays a vital role in resolving the abovementioned problems, thus promoting the transformation and modernization of the beef cattle industry in China. In this review, we summarize the research progress in this field over the past decade.

DEVELOPMENT OF FEED RESOURCES
In recent years, the rising costs of raw materials have led to an increase in the costs of feeding beef cattle in China. The agriculture, forestry, and food industry produce many byproducts that can be used as cheap feed resources to reduce feeding costs ( Figure 2).
Previous studies have reported the nutritional components of these by-products [6,7]. Moreover, numerous experiments have been conducted to evaluate the feeding value of these resources for beef cattle (Table 1). Notably, these resources have not been effectively utilized. The main factors restricting the utilization of these resources in beef cattle farming are their low nutritional value, poor palatability, difficult preservation, and presence of toxic substances and anti-nutritional factors. Therefore, these feed resources are often processed to compensate for their defects. For example, silage treatment is conducive to the long-term preservation of green forage, such as banana stems and leaves [8]. In addition, ammoniation [9] and microbial inoculation [10] can improve the feeding value of crops straw, thus expanding the application of these resources in beef cattle production.
its research on the nutrient requirements of beef cattle, mainly focusing on energy and protein requirements of growingfinishing beef cattle (Table 2). However, marginal information is available on the demand of growing-finishing beef cattle for other nutrients, such as minerals and vitamins. Additionally, Xu et al [11] showed that a phosphorus concentration of 0.37% in the diet can satisfy the phosphorus requirements of crossbred replacement beef heifers (Simmental×Chinese yellow cattle) with body weights of (369.5±37.8) kg.
We compared the conclusions of previous studies with the recommendations of the FSBC [12], and the results suggested that these recommendations may over-or underestimate the actual nutrient requirements for beef cattle (Table 3). For example, Zhang et al [13] reported that the crude protein requirements of Qinchuan cattle with body weights of (289.3±17.8) kg (with an average daily gain of 0 to 1.2 kg) were lower (29 to 132 g per cattle per day) than those recommended by the FSBC [12]. The formulation of FSBC is based on the research results before 2004. Since 2004, China has been vigorously promoting the improvement of beef cattle breeds. During this period, many changes have been made to the composition of beef cattle breeds. For example, China cultivated some new beef cattle breeds after 2004, such as Xianan cattle, Yanhuang cattle and Yunling cattle. In addition, the proportion of concentrate in beef cattle diets is gradually increased to improve their production efficiency. Therefore, the difference between FSBC and the research results may be due to the changes in breeding, feed composition, and feeding management, which can affect the nutritional requirements of beef cattle.

NUTRITIONAL REGULATION OF BEEF CATTLE
Nutritional regulation strategies to improve the growth and rumen fermentation of beef cattle The average production efficiency of beef cattle in China has been lower than that in developed countries for a long time, which reduces the profit and market competitiveness of the domestic beef cattle industry. Improving the production efficiency of beef cattle is thus a critical problem for the beef cattle industry in China.
The growth performance of beef cattle can be improved by adjusting the feed composition in the diet and adding functional substances. For adjusting diet structure, it has been reported that the growth performance and meat quality improved when beef cattle consumed high-quality roughage [14]. Moreover, increasing the dietary energy [15,16] and crude protein [17] levels can help improve the growth performance of beef cattle. Improved dietary nutrient levels may improve the growth performance of beef cattle, but can also cause adverse effects on rumen function, the viscera, and body metabolism of beef cattle [18]. Functional additives, such as probiotics and plant extracts, can improve the growth performance of beef cattle without exhibiting these negative effects (Table 4).
In addition, the rumen, the main digestive organ of ruminants, provides 70% to 80% of the energy requirements for growth. Previous studies have reported that regulating dietary energy [19] and crude protein [20] levels and roughage combinations [21] can affect the rumen fermentation of beef cattle. Diets supplemented with 2-methylbutyrate [22], and folic acid [23] can promote rumen nutrient degradation and mycoprotein synthesis in beef cattle. Moreover, the addition of live yeast [24] and inulin [25] in the diet can increase the ratio of propionic acid to acetic acid in the rumen fluid, thus improving the energy utilization of feed in beef cattle. Additionally, beef cattle are usually fed a high-concentrate diet during the fattening period, which can easily induce subacute ruminal acidosis (SRAS). Dietary supplementation with inulin [25], and niacin [26] can effectively relieve SRAS and improve the rumen fermentation of beef cattle.

Nutritional regulation strategies to improve the meat quality of beef cattle
Beef quality is one of the most important factors affecting price and consumers' purchase behavior. In China, the emphasis on the nutritional regulation of beef quality is for improving the intramuscular fat (IMF) content and optimization of meat fatty acid composition. Previous studies reported that increased dietary energy levels can increase the transcription and translation of adipogenic genes, promote the differentiation of preadipocytes into adipocytes, and decrease transcription and translation of lipidolytic genes, thus promoting the accumulation of IMF in beef [27,28]. In addition, dietary supplementation with daidzein [29], nicotinic acid [30], and conjugated linoleic acid [31] can also promote IMF deposition of beef cattle.
Unsaturated fatty acids (UFA), which as an important component of meat, are important for human health [32].   1) rDE, requirements of digestible energy; ∆W, daily weight gain in kilograms; rME, requirements of metabolizable energy; rME m , metabolizable energy requirements for maintenance; BW, body weight in kilograms; rNE, requirements of net energy; rNE mf , requirements of combined net energy. 2) rMP m , metabolizable protein requirements for maintenance; rNP m , net protein requirements for maintenance; rCP, requirements of crude protein; rDCP, requirements of digestible crude protein; rIDCP, requirements of intestine digestible crude protein. Transport stress can lead to an imbalance in rumen flora, nutritional metabolism, and immunity of beef cattle [3,49]. It has been reported that dietary supplementation with Astragalus polysaccharides [50] and creatine pyruvate [51] can alleviate transport stress in beef cattle.

Nutritional regulation strategies for reduction of pollutant emissions from beef cattle farming
High pollutant emission is a basic characteristic of the current beef cattle farming industry in China. Stricter environmental protection constraints in recent years have thus resulted in severe challenges for the beef cattle industry in China.
Methane (CH 4 ) is one of the main pollutants released from beef cattle farming. In 2009, methane emissions from beef cattle farming in China accounted for nearly two-thirds of all CH 4 produced by domestic ruminant farming [5]. In addition, CH 4 emissions from ruminants account for 2% to 12% of total dietary energy [52]. Therefore, mitigating CH 4 emissions is particularly important for the efficient and sustainable development of the beef cattle industry. The nutritional regulation strategies for mitigating CH 4 emissions can be mainly divided into optimizing the diet structure and adding functional substances to the diet (Table 5).
In addition to CH 4 , beef cattle farming also produces other pollutants such as nitrogen, organic matter, and nitrous oxide (N 2 O). A recent study reported that balancing the dietary ratio of nitrogen to sulfur can help increase nitrogen reten-   [55], and N-carbamylglutamate [56] can also increase nitrogen retention and reduce urinary nitrogen content of beef cattle. Although the addition of tannic acid [57] and gallic acid [58] to the diets of beef cattle cannot affect the nitrogen balance, but they can attenuate the urine N 2 O-N emissions by transferring nitrogen from the urine to the feces. Additionally, Gao et al [59] showed that adding red cabbage extract to the diet reduced urine N 2 O-N emissions of beef cattle by increasing urinary hippuric acid excretion.

CURRENT UNDERSTANDING AND FUTURE PERSPECTIVES
China has abundant unconventional feed resources; however, these resources are not utilized effectively. Therefore, it is necessary to further evaluate the nutritional and feeding values of these resources and study appropriate processing and storage technologies to expand their application in beef cattle farming.
Because of the improvements in intensive beef cattle farming in China, the original extensive feeding management strategy has been gradually replaced with precision feeding techniques. Understanding the precise nutrient requirements of beef cattle is the premise of precision feeding. We compared the conclusions of previous studies with the recommendations of the FSBC [12]. The results suggested that these recommendations may over-or underestimate the actual nutrient requirements for indigenous beef cattle in China. Therefore, the nutrient requirements of indigenous beef cattle should be investigated further to establish precision farming techniques that can prevent potential growth deficiencies and minimize pollutant emissions from beef cattle.
Nutritional regulation plays an essential role in beef cattle farming. Functional additives, especially plant extracts and probiotics, have been the focus of research in China in recent years. In addition, based on the importance of the IMF deposition of beef, numerous studies have been conducted on the relationship between nutrition intervention and IMF deposition [27,29]. However, these studies mainly focused on the effects of nutrition intervention on the apparent meat quality traits, while there were relatively few studies on the regulatory mechanism of IMF deposition. It is necessary to explore the biological and nutritional regulation mechanisms of IMF deposition in the future. In addition, carbon peak and carbon neutrality have become popular topics in political and economic activities in China. Therefore, achieving low-carbon beef cattle farming through nutritional intervention is a promising research area in the future.

CONCLUSION
In general, China has a relatively solid foundation of research in the field of beef cattle feed and nutrition that strongly supports the development of domestic beef cattle industry. However, there are still many limitations in current research, which restrict the efficient and sustainable development of beef cattle industry. In the future, more studies should focus on developing unconventional feed resources, studying the regulation mechanisms for efficient feed utilization and highquality beef production, and establishing technologies of precision nutrition and low-carbon farming for beef cattle.

CONFLICT OF INTEREST
We certify that there is no conflict of interest with any financial organization regarding the material discussed in the manuscript.