Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE

Nitrogen metabolism and recycling in yaks (Bos grunniens) offered a forage–concentrate diet differing in N concentration

X. S. Guo A B F , Y. Zhang C F , J. W. Zhou C , R. J. Long A C E , G. S. Xin D , B. Qi A , L. M. Ding A B and H. C. Wang C
+ Author Affiliations
- Author Affiliations

A International Centre for Tibetan Plateau Ecosystem Management, Lanzhou University, No. 222 Tianshui South Road, Lanzhou, 730000, PR China.

B State Key Laboratory of Pastoral Agricultural Ecosystem, Institute of Arid Agroecology, School of Life Sciences, Lanzhou University, 222 Tianshui South Road, Lanzhou 730000, PR China.

C State Key Laboratory of Pastoral and Agricultural Ecosystems, College of Pastoral Agriculture Science and Technology, Lanzhou University, 768 Jiayuguan West Road, Lanzhou, 730000, PR China.

D College of Life Science, Ningxia University, 489 Henanshan West Road, Xixia District, Yinchuan, 750021, PR China.

E Corresponding author. Email: longrj@lzu.edu.cn

F The first two authors contributed equally to this work.

Animal Production Science 52(5) 287-296 https://doi.org/10.1071/AN11208
Submitted: 28 September 2011  Accepted: 6 January 2012   Published: 20 March 2012

Abstract

An experiment was conducted to characterise N use efficiency and quantify urea fluxes in yaks offered four levels of dietary N (1.43%, 1.97%, 2.45% and 2.90% of diet DM) in a 4 × 4 Latin square design. The incremental increase in N intake linearly increased N retention (P = 0.003) and the excretion of urinary N (P < 0.001), but no difference (P > 0.05) in faecal N excretion was observed in growing yaks fed any of the four diets. Microbial N production had quadratic (P < 0.001) responses to dietary N, characterised by the highest microbial N production occurring in the 1.97% N diet (P < 0.05). As the N content of the diet increased, the urinary excretion of urea increased from 13% to 27% of urea entry rate (quadratic, P < 0.001), whereas gastrointestinal entry urea returned to ornithine cycling decreased from 46% to 40% (linear, P < 0.001), and the gastrointestinal entry urea used for anabolism increased from 50% to 56% (linear, P < 0.001). Gastrointestinal entry urea incorporated into bacterial N decreased linearly (P < 0.001) with incremental increase in N intake, and the greatest concentration (23.5%) of bacterial N originating from plasma urea N was in yaks fed the 1.43% N diet. As much as 87% of the urea synthesised in the liver was returned to the gastrointestinal tract when the yaks were fed a diet with 1.43% N (1.1 times the maintenance N level). Moreover, constantly greater urea production than the intake of digestible N, and the gastrointestinal-urea clearance than the kidney-urea clearance were observed, respectively, in the growing yaks, regardless of the level of N intake. These results suggest that yaks might be more efficient at utilising N under harsh environment than are cattle.

Additional keywords: dietary N, protein, urea recycling, yak.


References

AOAC (1990) ‘International official methods of analysis.’ 16th edn. (Association of Official Analytical Chemists: Arlington, VA)

Archibeque SL, Burns JC, Huntington GB (2001) Urea flux in beef steers: effects of forage species and N fertilization. Journal of Animal Science 79, 1937–1943.

Archibeque SL, Burns JC, Huntington GB (2002) Nitrogen metabolism of beef steers fed endophyte-free tall fescue hay: effects of ruminally protected methionine supplementation. Journal of Animal Science 80, 1344–1351.

Brenna JT, Corso TN, Tobias HJ, Caimi RJ (1997) High-recision continuous-flow isotope ration mass spectrometry. Mass Spectrometry Reviews 16, 227–258.
High-recision continuous-flow isotope ration mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVKmtLo%3D&md5=64b5194ca80fd31f0e50380fcd9098b1CAS |

Broderick GA, Kang JH (1980) Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media. Journal of Dairy Science 63, 64–75.
Automated simultaneous determination of ammonia and total amino acids in ruminal fluid and in vitro media.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsValu7s%3D&md5=9a75bd692819a6f68b63f74a59e01d0dCAS |

Bunting LD, Boling JA, MacKown CT (1989) Effect of dietary protein level on nitrogen metabolism in the growing bovine: I. Nitrogen recycling and intestinal protein supply in calves. Journal of Animal Science 67, 810–819.

Cabrita ARJ, Dewhurst RJ, Abreu JMF, Fonseca AJM (2006) Evaluation of the effects of synchronizing the availability of N and energy on rumen function and production responses of dairy cows – a review. Animal Research 55, 1–24.
Evaluation of the effects of synchronizing the availability of N and energy on rumen function and production responses of dairy cows – a review.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XislGgtr0%3D&md5=d89e0d45a517c9e9ef1aabd1a602ed14CAS |

Chen XB, Gomes MJ (1992) ‘Estimation of microbial protein supply to sheep and cattle based on urinary excretion of purine derivatives and overview of the technical details.’ Occasional Publication. (International Feed Resources Unit, Rowett Research Institute: Aberdeen, UK) Available at http://www.macaulay.ac.uk/IFRU/pdf/chema.pdf [verified 2 May 2010].

Chizzotti ML, Valadares SC, Tedeschi LO, Chizzotti FHM, Carstens GE (2007) Energy and protein requirements for growth and maintenance of F1 Nellore × Red Angus bulls, steers, and heifers. Journal of Animal Science 85, 1971–1981.
Energy and protein requirements for growth and maintenance of F1 Nellore × Red Angus bulls, steers, and heifers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXot1Ohtbw%3D&md5=22bd2902e44d9f7e012428dd6e355a64CAS |

Dewhurst RJ, Davies DR, Merry RJ (2000) Microbial protein supply from the rumen. Animal Feed Science and Technology 85, 1–21.
Microbial protein supply from the rumen.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjs1GksL8%3D&md5=2e4eb86b4c6f5afe8990412d6032fa4dCAS |

Durmowicz AG, Hofmeister S, Kadyraliev TK, Aldashev AA, Stenmark KR (1993) Functional and structural adaptation of the yak pulmonary circulation to residence at high altitude. Journal of Applied Physiology 74, 2276–2285.

Elrod CC, Butler WR (1993) Reduction of fertility and alteration of uterine pH in heifers fed excess ruminally degradable protein. Journal of Animal Science 71, 694–701.

Faix S, Leng L, Szanyionva M, Boda K (1988) Effect of dietary energy intake on tubular reabsorption of urea in sheep. Physiologia Bohemoslovaca 37, 493–501.

Firkins JL, Hristov AH, Hall MB, Varga GA, St-Pierre NR (2006) Integration of ruminal metabolism in dairy cattle. Journal of Dairy Science 89, E31–E51.
Integration of ruminal metabolism in dairy cattle.Crossref | GoogleScholarGoogle Scholar |

Han XT, Hu LH, Xie AY, Shi CY, Wang QL (1998) The content of ribonucleic acid and the ration of ribonucleic acid to bacteria nitrogen in the bacteria mixture separated from the yak rumen. Acta Zoonutrimenta Sinica 10, 35–39.

Harmeyer J, Martens H (1980) Aspects of urea metabolism in ruminants with reference to goat. Journal of Dairy Science 63, 1707–1728.
Aspects of urea metabolism in ruminants with reference to goat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3MXislOqsQ%3D%3D&md5=7046fe3fa976b32c1b1f39f9b598fb04CAS |

Heath D, Williams D, Dickinson J (1984) The pulmonary arteries of the yak. Cardiovascular Research 18, 133–139.
The pulmonary arteries of the yak.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7ls1eqtQ%3D%3D&md5=13fa5f33cf61226b5c57fd64b34a2e97CAS |

Henning PH, Steyn DG, Meissner HH (1993) Effect of synchronization of energy and nitrogen supply on ruminal characteristics and microbial growth. Journal of Animal Science 71, 2516–2528.

Hu L, Liu SS, Chai S (2000) Advances in yak nutrition research. In ‘Yak production in central Asian highlands’. Proceedings of the 3rd international congress on yak, Lhasa, PR China. (Eds JL Han, C Richard, O Hanotte, C McVeigh, JEO Rege) pp. 237–250.

Huntington GB, Zetina EJ, Whitt JM, Potts W (1996) Effects of dietary concentrate level on nutrient absorption, liver metabolism and urea kinetics of beef steers fed isonitrogenous and isoenergetic diets. Journal of Animal Science 74, 908–916.

Huntington GB, Magee K, Matthews A, Poore M, Burns J (2009) Urea metabolism in beef steers fed tall fescue, orchardgrass, or gamagrass hays. Journal of Animal Science 87, 1346–1353.
Urea metabolism in beef steers fed tall fescue, orchardgrass, or gamagrass hays.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFKis7s%3D&md5=e8c153f41234ccbca41d32a06953a978CAS |

Kennedy PM, Milligan LP (1980) Transfer of urea from the blood to the rumen of sheep. The British Journal of Nutrition 40, 149–154.
Transfer of urea from the blood to the rumen of sheep.Crossref | GoogleScholarGoogle Scholar |

Lammers BP, Heinrichs AJ, Kensinger RS (1999) The effects of accelerated growth rates and estrogen implants in prepubertal Holstein heifers on growth, feed efficiency, and blood parameters. Journal of Dairy Science 82, 1746–1752.
The effects of accelerated growth rates and estrogen implants in prepubertal Holstein heifers on growth, feed efficiency, and blood parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXlsVykur0%3D&md5=c642322db87bae2a18d6fdacb5fb11a3CAS |

Lapierre H, Lobley GE (2001) Nitrogen recycling in the ruminant: a review. Journal of Dairy Science 84, E223–E236.
Nitrogen recycling in the ruminant: a review.Crossref | GoogleScholarGoogle Scholar |

Lobley GE, Bremner DM, Zuur G (2000) Effects of diet quality on urea fates in sheep as assessed by refined, non-invasive [15N15N] urea kinetics. The British Journal of Nutrition 84, 459–468.

Long RJ, Dong SK, Chen XB, Ørskov ER, Hu ZZ (1999) Preliminary studies on urinary excretion of purine derivatives and creatinine in yaks. The Journal of Agricultural Science 133, 427–431.
Preliminary studies on urinary excretion of purine derivatives and creatinine in yaks.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisFertb0%3D&md5=45324d56edaf83fcde94c58da93d2242CAS |

Marini JC, Attene-Ramos MS (2006) An improved analytical method for the determination of urea nitrogen isotopomers in biological samples utilizing continuous flow isotope ratio mass spectrometry. Rapid Communications in Mass Spectrometry 20, 3736–3740.
An improved analytical method for the determination of urea nitrogen isotopomers in biological samples utilizing continuous flow isotope ratio mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXit1ertg%3D%3D&md5=c1cc57094df1a2ad6226e07070e5344eCAS |

Marini JC, Van Amburgh ME (2003) Nitrogen metabolism and recycling in Holstein heifers. Journal of Animal Science 81, 545–552.

Marini JC, Klein JD, Sands JM, Van Amburgh EM (2004) Effect of nitrogen intake on nitrogen recycling and urea transporter abundance in lambs. Journal of Animal Science 82, 1157–1164.

Marsh WH, Fingerhut B, Kirsch E (1957) Determination of urea N with the diacetyl method and an automatic dialyzing apparatus. American Journal of Clinical Pathology 8, 681–688.

Mould ED, Robbins CT (1981) Nitrogen metabolism in elk. The Journal of Wildlife Management 45, 323–334.
Nitrogen metabolism in elk.Crossref | GoogleScholarGoogle Scholar |

Newbold JR, Rust SR (1992) Effect of asynchronous nitrogen and energy supply on growth of ruminal bacteria in batch culture. Journal of Animal Science 70, 538–546.

Preston RL, Kock SW (1973) In vivo prediction of body composition in cattle from urea space measurements. Proceedings of the Society for Experimental Biology and Medicine 143, 1057–1061.

Reynolds CK, Kristensen NB (2008) Nitrogen recycling through the gut and the nitrogen economy of ruminants: an asynchronous symbiosis. Journal of Animal Science 86, 293–305.

Sarraseca A, Milne E, Metcalf MJ, Lobley GE (1998) Urea recycling in sheep: effects of intake. The British Journal of Nutrition 79, 79–88.
Urea recycling in sheep: effects of intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXhtVCgsL8%3D&md5=823f7162231b379573145a336edfc44aCAS |

Shao BP, Long RJ, Ding YP, Wang JL, Ding LM, Wang HC (2010) Morphological adaptations of yak (Bos grunniens) tongue to the foraging environment of the Qinghai–Tibetan Plateau. Journal of Animal Science 88, 2594–2603.
Morphological adaptations of yak (Bos grunniens) tongue to the foraging environment of the Qinghai–Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpvVOrsbk%3D&md5=bbbfe3fe365a61ecd73ed9b8e2b35cc5CAS |

Shingfield KJ, Offer NW (1999) Simultaneous determination of purine metabolites, creatinine and pseudouridine in ruminant urine by reversed-phase high-performance liquid chromatography. Journal of Chromatography B: Biomedical Sciences and Application 723, 81–94.
Simultaneous determination of purine metabolites, creatinine and pseudouridine in ruminant urine by reversed-phase high-performance liquid chromatography.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhs1Ogsbc%3D&md5=d2634e6d1e5a675e29a2e12cd5f0944eCAS |

Siddons RC, Nolana JV, Beever DE, Macrae JC (1985) Nitrogen digestion and metabolism in sheep consuming diets containing contrasting forms and levels of N. The British Journal of Nutrition 54, 175–187.
Nitrogen digestion and metabolism in sheep consuming diets containing contrasting forms and levels of N.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL28%2FltFChug%3D%3D&md5=2a3a69fc0d74687da88b54e5e858fea3CAS |

Smith RH (1974) Nitrogen metabolism in the rumen and the composition and nutritive value of nitrogen compositions entering the duodenum. In ‘Digestion and metabolism in the ruminants’. (Eds IW Mcdonald, ACA Waner) pp. 399–415. (The University of New England Publishing Unit: Armidale, NSW)

St-Pierre NR (2001) Integrating quantitative finding from multiple studies using mixed model methodology. Journal of Dairy Science 84, 741–755.
Integrating quantitative finding from multiple studies using mixed model methodology.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXjtFyks78%3D&md5=ea55f5a87381fd790be859225ad698caCAS |

Sunny NE, Owens SL, Baldwin RL, El-Kadi SW, Kohn RA, Bequette BJ (2007) Salvage of blood urea nitrogen in sheep is highly dependent on plasma urea concentration and the efficiency of capture within the digestive tract. Journal of Animal Science 85, 1006–1013.
Salvage of blood urea nitrogen in sheep is highly dependent on plasma urea concentration and the efficiency of capture within the digestive tract.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXjslWksrk%3D&md5=21b6b8b1d4fe3846a61b1f3e7b6de1d0CAS |

Tebot I, Faix S, Szanyiova M, Cirio A, Leng L (1998) Micropuncture study on urea movements in the kidney cortical tubules of low protein fed sheep. Veterinary Research 29, 99–105.

Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
Methods for dietary fiber, neutral detergent fiber, and non-starch polysaccharides in relation to animal nutrition.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK38%2FnvVCltA%3D%3D&md5=2648256a724beb4754b35e474c24f1b0CAS |

Wang HC (2009) Urinary purine derivative excretion as a method for estimation of rumen microbial protein production of yak in Qing-hai Tibetan plateau. PhD Dissertation, Lanzhou University, Lanzhou, China.

Wang HC, Long RJ, Zhou W, Li XP, Zhou JW, Guo XS (2009) A comparative study on urinary purine derivative excretion for yak (Bos grunniens), indigenous cattle (Bos taurus) and crossbred (Bos grunniens × Bos taurus) in the Qinghai Tibetan plateau, China. Journal of Animal Science 87, 2355–2362.
A comparative study on urinary purine derivative excretion for yak (Bos grunniens), indigenous cattle (Bos taurus) and crossbred (Bos grunniens × Bos taurus) in the Qinghai Tibetan plateau, China.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXnvVCjtrY%3D&md5=a248482393f61950a7930119fdaac1e0CAS |

Wang HC, Long RJ, Liang JB, Guo XS, Ding LM, Shang ZH (2011) Comparison of nitrogen metabolism in yak (Bos grunniens) and indigenous cattle (Bos taurus) on the Qinghai–Tibetan Plateau. Asian-Australasian Journal of Animal Sciences 24, 766–773.
Comparison of nitrogen metabolism in yak (Bos grunniens) and indigenous cattle (Bos taurus) on the Qinghai–Tibetan Plateau.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXoslOkt74%3D&md5=cccecb647f58a15197953ec6d9852f4dCAS |

Wickersham TA, Titgemeyer EC, Cochran RC, Wickersham EE, Gnad DP (2008a) Effect of rumen-degradable intake protein supplementation on urea kinetics and microbial use of recycled urea in steers consuming low-quality forage. Journal of Animal Science 86, 3079–3088.
Effect of rumen-degradable intake protein supplementation on urea kinetics and microbial use of recycled urea in steers consuming low-quality forage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCnsbzM&md5=8780b4e03b0301c5227379ca94d89314CAS |

Wickersham TA, Titgemeyer EC, Cochran RC, Wickersham EE, Moore ES (2008b) Effect of frequency and amount of rumen-degradable intake protein supplementation on urea kinetics and microbial use of recycled urea in steers consuming low-quality forage. Journal of Animal Science 86, 3089–3099.
Effect of frequency and amount of rumen-degradable intake protein supplementation on urea kinetics and microbial use of recycled urea in steers consuming low-quality forage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlCnsbzN&md5=040ba30839178c879c5dd877b0dd7a70CAS |

Wiener G, Han JL, Long RJ (2003) ‘The yak.’ 2nd edn. (Regional Office for Asia and the Pacific, FAO, UN: Bangkok, Thailand)

Yarns DA, Putnam PA, Leffel EC (1965) Daily salivary secretion by beef steers. Journal of Animal Science 24, 173–176.

Zinn RA, Owens FN (1986) A rapid procedure for purine measurement and its use for estimating net ruminal protein synthesis. Canadian Journal of Animal Science 66, 157–166.
A rapid procedure for purine measurement and its use for estimating net ruminal protein synthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28Xkt1Whsr4%3D&md5=a848b2b3260cd1f530914d8b42f5bd5aCAS |