Please wait a minute...
Journal of Integrative Agriculture  2025, Vol. 24 Issue (4): 1296-1309    DOI: 10.1016/j.jia.2023.11.035
Section 3: Diet components and feed additives Advanced Online Publication | Current Issue | Archive | Adv Search |
Inclusion of sorghum grain rich in condensed tannins in the diet of steers did not affect the nitrogen utilization efficiency but increased the urine nitrous oxide emissions
Biao Xie, Changfa Mao, Xu Shen, Yufeng Liu, Qingyue Liang, Guangyong Zhao#

State Key Laboratory of Animal Nutrition and Feeding, College of Animal Science and Technology, China Agricultural University, Beijing 100193, China

 Highlights 
Dietary inclusion of sorghum grain increased faecal nitrogen excretion in steers.
Dietary inclusion of sorghum grain did not affect nitrogen utilization efficiency in steers.
Dietary inclusion of sorghum grain increased steer urine N2O emission.
Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

试验旨在研究日粮中添加富含缩合单宁(CT[18.9 g kg-1 干物质(DM]的高粱对肉牛氮(N)代谢和尿液氧化亚氮N2O)排放的影响。试验1选用6利木赞×鲁西杂交阉牛(初始体重为245 ± 18.70 kg作为试验动物采用有重复的3×3拉丁方试验设计,日粮中高粱含量分别为0167338 g kg-1 DM试验2采用静态土壤培养技术测定试验1中尿样的N2O排放量。试验1的结果表明,日粮中添加高粱线性增加N排泄量(P=0.001)、总N排泄量(P=0.010)和粪N/采食N比例P=0.021),但没有影响尿N排泄量、沉积NN积率(P>0.10)。血浆代谢组数据显示,日粮中添加高粱上调了酚酸(N1,N5,N10-tris-trans-p-coumaroylspermine and prenyl cis-caffeate)和肉碱(3-hydroxyisovalerylcarnitine and linoelaidyl carnitine)的相对浓度。试验1结果还显示,随着日粮中高粱比例的提高,肉牛的尿素排泄量线性增加(P=0.001),尿囊素排泄量有线性降低的趋势P=0.051,尿液嘌呤衍生物排泄量(P=0.041)及根据尿液嘌呤衍生物估测的瘤胃微生物N流量线性降低P=0.012)。试验2的结果表明,随着日粮中高粱比例的提高土壤的整个培养期的平均pH没有显著变化(P>0.10),但是土壤NH4+-NP=0.012)、NO2--NP=0.009)、NO3--NP=0.001)和无机NP<0.001平均浓度线性提高土壤静态培养果还显示,随着日粮中高粱比例的提高,尿液N2O-N排放量(P=0.001)、N2O-N放/尿N施加量比例(P=0.038)和尿液N2O-N估测排放量(P=0.021)均线性提高。综上所述,日粮中添加富含CT的高粱167 338 g kg-1 DM不影响肉牛的N沉积率,但可增加尿液N2O-N排放量分别达5.7%31.4%为了减少向环境中排放的氧化亚氮数量,不建议在肉牛日粮中添加高水平的高粱。



Abstract  
The objectives of this study which included two experiments were to investigate the effects of dietary inclusion of sorghum grain rich in condensed tannins (CT) (18.9 g kg–1 dry matter (DM)) on nitrogen (N) metabolism and urine nitrous oxide (N2O) emissions of beef steers.  In experiment 1, six Limousin×Luxi crossbreed steers with an initial liveweight of (245.0±18.7) kg were used as experimental animals.  Three levels of sorghum grain, i.e., 0, 167 and 338 g kg–1 DM were included in diets as experimental treatments.  The animals and the treatments were randomly assigned to a replicated 3×3 Latin square design.  In experiment 2, static incubation technique was used to determine the N2O emissions of the urine samples collected in experiment 1.  The results of experiment 1 showed that dietary inclusion of sorghum grain linearly increased the faecal N excretion (P=0.001), the total N excretion (P=0.010) and the faecal N to N intake ratio (P=0.021), but it did not affect the N retention and the N utilization efficiency (P>0.10).  The plasma metabolomic data showed that dietary inclusion of sorghum grain increased the relative concentrations of phenolic acid (N1, N5, N10-tris-trans-p-coumaroylspermine and prenyl cis-caffeate) and carnitine (3-hydroxyisovalerylcarnitine and linoelaidyl carnitine).  The results also showed that dietary inclusion of sorghum grain linearly increased the urinary urea excretion (P=0.010) and decreased the urinary excretion of purine derivatives (P=0.041) as well as the estimated rumen microbial N supply (P=0.012) based on urinary purine derivatives.  The results of experiment 2 showed that including sorghum grain in the diet linearly increased the average concentrations of NH4+-N (P=0.012), NO2-N (P=0.009), NO3-N (P=0.001) and the total inorganic N (P<0.001) in the soil enriched with urine samples.  The urine sample N2O-N flux (P=0.001), the estimated steer urine N2O-N flux (P=0.021) and the N2O-N to urinary N ratio (P=0.038) linearly increased with increasing inclusion of sorghum grain in the diet.  In conclusion, dietary inclusion of sorghum grain containing high CT at 167 and 338 g kg–1 DM did not affect the N utilization efficiency of steers but increased the urine N2O-N emissions by 5.7 and 31.4%, respectively.  For reducing the N2O emissions to the environment, high levels of sorghum grain should not be included in the diet of steers.


Keywords:  cattle        nitrogen retention        nitrous oxide        sorghum        urine  
Received: 08 March 2023   Accepted: 29 October 2023
Fund: The study was supported by the National Natural Science Foundation of China (31572428).
About author:  #Correspondence Guangyong Zhao, E-mail: zhaogy@cau.edu.cn

Cite this article: 

Biao Xie, Changfa Mao, Xu Shen, Yufeng Liu, Qingyue Liang, Guangyong Zhao. 2025. Inclusion of sorghum grain rich in condensed tannins in the diet of steers did not affect the nitrogen utilization efficiency but increased the urine nitrous oxide emissions. Journal of Integrative Agriculture, 24(4): 1296-1309.

Adejoro F A, Hassen A, Akanmu A M. 2019. Effect of lipid-encapsulated Acacia tannin extract on feed intake, nutrient digestibility and methane emission in sheep. Animals9, 836.

Aguerre M J, Capozzolo M C, Lendoni P, Cabral C, Wattiaux M A. 2016. Effect of quebracho-chestnut tannin extracts at 2 dietary crude protein levels on performance, rumen fermentation, and nitrogen partitioning in dairy cows. Journal of Dairy Science99, 4476–4486.

Ahnert S, Dickhoefer U, Schulz F, Susenbeth A. 2015. Influence of ruminal quebracho tannin extract infusion on apparent nutrient digestibility, nitrogen balance, and urinary purine derivatives excretion in heifers. Livestock Science177, 63–70.

Ainsworth E A, Gillespie K M. 2007. Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin-Ciocalteu reagent. Nature Protocols2, 875–877.

Ambus P, Petersen S O , Soussana J F. 2007. Short-term carbon and nitrogen cycling in urine patches assessed by combined carbon-13 and nitrogen-15 labelling. AgricultureEcosystems & Environment121, 84–92.

AOAC (Association of Official Analytical Chemists). 2005. Official Methods of Analysis. 18th ed. Association of Official Analytical Chemists, Gaithersburg, MD, USA.

Ávila S C, Kozloski G V, Orlandi T, Mezzomo M P, Stefanello S. 2015. Impact of a tannin extract on digestibility, ruminal fermentation and duodenal flow of amino acids in steers fed maize silage and concentrate containing soybean meal or canola meal as protein source. Journal of Agricultural Science153, 943–953.

Baggs E M. 2010. A review of stable isotope techniques for N2O source partitioning in soils, recent progress, remaining challenges and future considerations. Rapid Communications in Mass Spectrometry22, 1664–1672.

Bao Y, Zou K, Zhao G Y. 2018. Nitrous oxide emissions from the urine of beef cattle as regulated by dietary crude protein and gallic acid. Journal of Animal Science96, 3699–3711.

Belton P S, Delgadillo I, Halford N G, Shewry P R. 2006. Kafirin structure and functionality. Journal of Cereal Science44, 272–286.

Bertram J E, Clough T J, Sherlock R R, Condron L M, O’callaghan M, Wells N S, Ray J L. 2009. Hippuric acid and benzoic acid inhibition of urine derived N2O emissions from soil. Global Change Biology15, 2067–2077.

Carulla J E, Kreuzer M, Machmuller A, Hess H D. 2005. Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Australian Journal of Agricultural Research56, 961–970.

Chen X B, Gomes M J. 1992. Estimation of Microbial Protein Supply to Sheep and Cattle Based on Urinary Excretion of Purine Derivatives - An Overview of Technical Details. Rowett Research Institute, Aberdeen. pp. 1–21.

Cusack D F, Kazanski C E, Hedgpeth A, Chow K, Cordeiro A L, Karpman J, Ryals R. 2021. Reducing climate impacts of beef production: A synthesis of life cycle assessments across management systems and global regions. Global Change Biology27, 1721–1736.

Dijkstra J, Oenema O, Groenigen J, Spek J W, Bannink A. 2013. Diet effects on urine composition of cattle and N2O emissions. Animal7, 292–302.

Dong R L, Zhao G Y, Chai L L, Beauchemin K A. 2014. Prediction of urinary and fecal nitrogen excretion by beef cattle. Journal of Animal Science92, 4669–4681.

Dykes L, Rooney L W. 2006. Sorghum and millet phenols and antioxidants. Journal of Cereal Science44, 236–251.

Dykes L, Rooney L W, Waniska R D, Rooney W L. 2005. Phenolic compounds and antioxidant activity of sorghum grains of varying genotypes. Journal of Agricultural Food and Chemistry53, 6813–6818.

Ebert P J, Bailey E A, Shreck A L, Jennings J S, Cole N A. 2017. Effect of condensed tannin extract supplementation on growth performance, nitrogen balance, gas emissions, and energetic losses of beef steers. Journal of Animal Science95, 1345–1355.

Feng Y L. 2000. The Nutrient Requirements and Feeding Standards of Beef Cattle. China Agricultural University Press, Beijing, China. (in Chinese)

Focant M, Froidmont E, Archambeau Q, Dang V Q, Larondelle Y. 2019. The effect of oak tannin (Quercus robur) and hops (Humulus lupulus) on dietary nitrogen efficiency, methane emission, and milk fatty acid composition of dairy cows fed a low-protein diet including linseed. Journal of Dairy Science102, 1144–1159.

Girard A L, Awika J M. 2018. Sorghum polyphenols and other bioactive components as functional and health promoting food ingredients. Journal of Cereal Science84, 112–124.

Grainger C T, Clarke M J, Auldist K A, Beauchemin S M, Waghorn G C, Eckard R J. 2009. Potential use of Acacia mearnsii condensed tannins to reduce methane emissions and nitrogen excretion from grazing dairy cows. Canadian Journal of Animal Science89, 241–251.

Hinds A A, Lowe L E. 1980. Application of the berthelot reaction to the determination of ammonium-N in soil extracts and soil digests. Communications in Soil Science and Plant Analysis11, 469–475.

Hristov A N, Meinen R, Montes F, Firkins J, Dell C, Adesogan C. 2013. Mitigation of Greenhouse Gas Emissions in Livestock Production - A Review of Technical Options for Non-CO2 Emission. Food and Agriculture Organization of the United Nations Animal Production and Health, Rome, Italy.

Hristov A N, Ropp J K. 2003. Effect of dietary carbohydrate composition and availability on utilization of ruminal ammonia nitrogen for milk protein synthesis in dairy cows. Journal of Dairy Science86, 2416–2427.

IPCC (Intergovernmental Panel on Climate Change). 2019. Chapter 10: Emissions from Livestock and Manure Management. 2019 Refinement to the 2006 Intergovernmental Panel on Climate Change Guidelines for National Greenhouse Gas Inventories. Intergovernmental Panel on Climate Change. p. 225.

Jackson R D, Oates L G, Schacht W H, Klopfenstein T J, Undersander D J, Greenquist M A, Bell M M, Gratton C. 2015. Nitrous oxide emissions from cool-season pastures under managed grazing. Nutrient Cycling in Agroecosystems101, 1–12.

Johnson J A, Sutherland B D, McKinnon J J, McAllister T A, Penner G B. 2020. Effect of feeding barley or corn silage with dry-rolled barley, corn, or a blend of barley and corn grain on rumen fermentation, total tract digestibility, and nitrogen balance for finishing beef heifers. Journal of Animal Science98, a2.

Khosravi M, Rouzbehan Y, Rezaei M, Rezaei J. 2018. Total replacement of corn silage with sorghum silage improves milk fatty acid profile and antioxidant capacity of Holstein dairy cows. Journal of Dairy Science101, 10953–10961.

Kool D M, Hoffland E, Hummelink E, Groenigen J. 2006. Increased hippuric acid content of urine can reduce soil N2O fluxes. Soil Biology and Biochemistry38, 1021–1027.

Kumar N, Goel N. 2019. Phenolic acids: natural versatile molecules with promising therapeutic applications. Biotechnology Reports24, e370.

Kwon W B, Soto J A, Stein H H. 2020. Effects on nitrogen balance and metabolism of branched-chain amino acids by growing pigs of supplementing isoleucine and valine to diets with adequate or excess concentrations of dietary leucine. Journal of Animal Science98, a346.

Leroy B, Meur, Q D, Moulin C, Wegria, G, Wattiez R. 2015. New insight into the photoheterotrophic growth of the isocytrate lyase-lacking purple bacterium Rhodospirillum rubrum on acetate. Microbiology (Reading), 161, 1061–1072.

Li M, Xu T, Zheng W, Gao B, Yu L L. 2021.Triacylglycerols compositions, soluble and bound phenolics of red sorghums, and their radical scavenging and anti-inflammatory activities. Food Chemistry340, 128123.

Licitra G T, Hernandez M, Van Soest P. 1996. Standardization of procedures for nitrogen fractionation of ruminant feeds. Animal Feed Science and Technology57, 347–358.

Liu C, Wu H, Liu S, Chai S, Zhou Z. 2019. Dynamic alterations in yak rumen bacteria community and metabolome characteristics in response to feed type. Frontiers in Microbiology10, 1116.

Levy-Booth D J, Prescott C E, Grayston S J. 2014. Microbial functional genes involved in nitrogen fixation, nitrification and denitrification in forest ecosystems. Soil Biology & Biochemistry75, 11–25.

Maciel I C F, Barbosa F A, Alves B J R, Alvarenga R C, Tomich T R, Campanha M M, Rowntree J E, Alves F C, Lana  M Q. 2021. Nitrous oxide and methane emissions from beef cattle excreta deposited on feedlot pen surface in tropical conditions. Agricultural Systems187, 102995.

Mertens D R. 2002. Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: collaborative study. Journal of AOAC International85, 1217–1240.

Nichols K L, Del G, Derner J D, Follett R F, Archibeque S L, Delgado J A, Paustian K H. 2018. Nitrous oxide and ammonia emissions from cattle excreta on shortgrass steppe. Journal of Environmental Quality47, 419–426.

Norman R J, Edberg J C, Stucki J W. 1985. Determination of nitrate in soil extracts by dual-wavelength ultraviolet spectrophotometry. Soil Science Society of America Journal49, 1182–1185.

Norris A B, Crossland W L, Tedeschi L O, Foster J L, Muir J P, Pinchak W E, Fonseca M A. 2020. Inclusion of quebracho tannin extract in a high-roughage cattle diet alters digestibility, nitrogen balance, and energy partitioning. Journal of Animal Science98, a47.

NRC (National Research Council). 2001. Nutrient Requirements of Dairy Cattle. 7th ed. National Academy of Sciences, Washington, D.C., USA.

Oliveira L N, Pereira M A N, Oliveira C D S, Oliveira C C, Silva R B, Pereira R A N, DeVries T J, Pereira M N. 2023. Effect of low dietary concentrations of Acacia mearnsii tannin extract on chewing, ruminal fermentation, digestibility, nitrogen partition, and performance of dairy cows. Journal of Dairy Science106, 3203–3216.

Olukoya I A, Bellmer D, Whiteley J R, Aichele, C P. 2015. Evaluation of the environmental impacts of ethanol production from sweet sorghum. Energy for Sustainable Development24, 1–8.

Orlandi T, Kozloski G V, Alves T P, Mesquita F R, Ávila S C. 2015. Digestibility ruminal fermentation and duodenal flux of amino acids in steers fed grass forage plus concentrate containing increasing levels of Acacia mearnsii tannin extract. Animal Feed Science and Technology210, 37–45.

Pan L, Shang Q H, Wu Y, Ma X K, Long S F, Liu L, Li D F, Piao X S. 2017. Concentration of digestible and metabolizable energy, standardized ileal digestibility, and growth performance of pigs fed diets containing sorghum produced in the United States or corn produced in China. Journal of Animal Science95, 4880–4892.

Sanchez-Martín L, Beccaccia A, De Blas C, Sanz-Cobena A, García-Rebollar P, Estellés F. 2017. Diet managementto effectively abate N2O emissions from surface appliedpig slurry. AgricultureEcosystems & Environment239, 1–11.

Satoh S, Shindoh M, Min J Z, Toyo Oka T, Fukushima T, Inagaki S. 2008. Selective and sensitive determination of lipoyllysine (protein-bound α-lipoic acid) in biological specimens by high-performance liquid chromatography with fluorescence detection. Analytica Chimica Acta618, 210–217.

Stewart E K, Beauchemin K A, Dai X, MacAdam J W, Christensen R G, Villalba J J. 2019. Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle. Journal of Animal Science97, 3286–3299.

Streeter M N, Wagner D G, Hibberd C A. 1990. Comparison of corn with four sorghum grain hybrids: Site and extent of digestion in steers. Journal of Animal Science68, 3429–3440.

Sun H X, Gao T S, Zhong R Z, Fang Y, Di G L, Zhou D W. 2018. Effects of corn replacement by sorghum in diets on performance, nutrient utilization, blood parameters, antioxidant status, and meat colour stability in lambs. Canadian Journal of Animal Science98, 723–731.

Terrill T H, Rowan A M, Douglas G B, Barry T N. 1992. Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. Journal of the Science of Food and Agriculture58, 321–329.

Tian H, Xu R, Canadell J G, Thompson R L, Yao Y. 2020. A comprehensive quantification of global nitrous oxide sources and sinks. Nature586, 248–256.

Tierling J, Kuhlmann H. 2018. Emissions of nitrous oxide (N2O) affected by pH-related nitrite accumulation during nitrification of N fertilizers. Geoderma310, 12–21.

Wang B, Ma M P, Diao Q Y, Tu Y. 2019. Saponin-induced shifts in the rumen microbiome and metabolome of young cattle. Frontiers in Microbiology10, 356.

Watanabe T, Osada T, Yoh M, Tsuruta H. 1997. N2O and NO emissions from grassland soils after the application of cattle and swine excreta. Nutrient Cycling in Agroecosystems49, 35–39.

Xie B, Yang X, Yang L, Wen X J, Zhao G Y. 2021. Adding polyethylene glycol to steer ration containing sorghum tannins increases CP digestibility and shifts nitrogen excretion from feces to urine. Animal Nutrition7, 779–786.

Xiong Y, Zhang P, Warner R D, Fang Z X. 2019. Sorghum grain: from genotype, nutrition, and phenolic profile to its health benefits and food applications. Comprehensive Reviews in Food Science and Food Safety18, 2025–2046.

Zhou K, Bao Y, Zhao G. 2019. Effects of dietary crude protein and tannic acid on nitrogen excretion, urinary nitrogenous composition and urine nitrous oxide emissions in beef cattle. Journal of Animal Physiology and Animal Nutrition103, 1675–1683.

Zhu H, Wang Y, Liu Y, Xia Y, Tang T. 2010. Analysis of flavonoids in Portulaca oleracea L. by UV–Vis spectrophotometry with comparative study on different extraction technologies. Food Analytical Methods3, 90–97.

[1] Yuan Gao, Fuxia Bai, Qi Zhang, Xiaoya An, Zhaofei Wang, Chuzhao Lei, Ruihua Dang. Dynamic transcriptome profiles and novel markers in bovine spermatogenesis revealed by single-cell sequencing[J]. >Journal of Integrative Agriculture, 2024, 23(7): 2362-2378.
[2] Keanning Li, Bingxing An, Mang Liang, Tianpeng Chang, Tianyu Deng, Lili Du, Sheng Cao, Yueying Du, Hongyan Li, Lingyang Xu, Lupei Zhang, Xue Gao, Junya LI, Huijiang Gao.

Prescreening of large-effect markers with multiple strategies improves the accuracy of genomic prediction [J]. >Journal of Integrative Agriculture, 2024, 23(5): 1634-1643.

No Suggested Reading articles found!