Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep
J. E. Carulla A , M. Kreuzer B , A. Machmüller B and H. D. Hess B CA Department of Animal Production, National University of Colombia, Bogotá, Colombia.
B Institute of Animal Science, Animal Nutrition, Swiss Federal Institute of Technology (ETH), ETH Center/LFW, CH-8092 Zurich, Switzerland.
C Corresponding author. Email: dieter.hess@alp.admin.ch
Australian Journal of Agricultural Research 56(9) 961-970 https://doi.org/10.1071/AR05022
Submitted: 24 January 2005 Accepted: 4 July 2005 Published: 28 September 2005
Abstract
The objective of this experiment was to assess the effects of a partial replacement of ryegrass (Lolium perenne) by red clover (Trifolium pratense) or alfalfa (Medicago sativa) supplemented with 0 or 41 g Acacia mearnsii extract (containing 0.615 g/g condensed tannins)/kg dietary dry matter on nitrogen turnover and methane release by sheep, using the respiration chamber technique. Across all variables, there was no significant interaction between basal diet and tannin supplementation. The partial replacement of the grass by the legumes remained without effect on the amounts of nitrogen excreted through faeces or urine. Nitrogen and energy utilisation was lower (P < 0.05) with ryegrass–alfalfa than with ryegrass alone, and methane release (kJ/MJ gross energy intake) was higher (P < 0.05) with ryegrass–red clover than with ryegrass alone. Tannin supplementation decreased (P < 0.05) ruminal ammonia concentration and urinary nitrogen excretion without affecting body nitrogen and energy retention, and reduced (P < 0.001) methane release by 13% on average. The results suggest that supplemented Acacia mearnsii tannins can be useful in mitigating methane and potential gaseous nitrogen emissions, whereas a replacement of grass by legumes obviously shows no advantage in this respect.
Additional keywords: energy expenditure, feed additives, grass–legume associations, lucerne, ruminant.
Acknowledgments
This study was supported by the State Secretariat for Education and Research (SER) and the Swiss Agency for Development and Cooperation (SDC). The authors are grateful to H. Leuenberger, A. Moses, and B. Schneider for their assistance in this study.
Alén R,
Jännäri P, Sjöström E
(1985) Gas-liquid chromatographic determination of volatile fatty acids C1–C6, and lactic acid as their benzyl esters on a fused-silica capillary column. Finnish Chemical Letters 1985, 190–192.
Barry TN, McNabb WC
(1999) The implications of condensed tannins on the nutritive value of temperate forages fed to ruminants. The British Journal of Nutrition 81, 263–272.
| PubMed |
Benchaar C,
Pomar C, Chiquette J
(2001) Evaluation of dietary strategies to reduce methane production in ruminants: a modelling approach. Canadian Journal of Animal Science 81, 563–574.
Ben Salem H,
Atti N,
Priolo A, Nefzaoui A
(2002) Polyethylene glycol in concentrate or feedblocks to deactivate condensed tannins in Acacia cyanophylla Lindl. foliage 1. Effects on intake, digestion and growth by Barbarine lambs. Animal Science 75, 127–135.
Bhatta R,
Shinde AK,
Vaithiyanathan S,
Sankhyan SK, Verma DL
(2002) Effect of polyethylene glycol-6000 on nutrient intake, digestion and growth of kids browsing Prosopis cineraria. Animal Feed Science and Technology 101, 45–54.
| Crossref | GoogleScholarGoogle Scholar |
Broderick GA, Albrecht KA
(1997) Ruminal in vitro degradation of protein in tannin-free and tannin-containing forage legume species. Crop Science 37, 1884–1891.
Broderick GA,
Walgenbach RP, Sterrenburg E
(2000) Performance of lactating dairy cows fed alfalfa or red clover silage as the sole forage. Journal of Dairy Science 83, 1543–1551.
| PubMed |
Brouwer E
(1965) Report of sub-committee on constants and factors. ‘Energy metabolism’. (Ed. KL Blaxter)
pp. 441–443. (Academic Press: London, UK)
Carulla J,
Lascano C, Klopfenstein T
(2001) Reduction of tannin level in a tropical legume (Desmodium ovalifolium) with polyethylene glycol (PEG): effects on intake and N balance, digestion and absorption by sheep. Archivos Latinoamericanos de Producción Animal 9, 17–24.
Field JA,
Kortekaas S, Lettinga G
(1989) The tannin theory of methanogenic toxicity. Biological Wastes 29, 241–262.
| Crossref | GoogleScholarGoogle Scholar |
Fievez V,
Piattoni F,
Mbanzamihigo L, Demeyer D
(1999) Reductive acetogenesis in the hindgut and attempts to its induction in the rumen — a review. Journal of Applied Animal Research 16, 1–22.
Fraser DL,
Hamilton BK, Poppi DP
(1990) Effect of duodenal infusion of protein or amino acids on nitrogen retention of lambs consuming fresh herbage. Proceedings of the New Zealand Society of Animal Production 50, 43–47.
Getachew G,
Makkar HPS, Becker K
(2001) Method of polyethylene glycol application to tannin-containing browses to improve microbial fermentation and efficiency of microbial protein synthesis from tannin-containing browses. Animal Feed Science and Technology 92, 51–57.
| Crossref | GoogleScholarGoogle Scholar |
Hess HD,
Monsalve LM,
Lascano CE,
Carulla JE,
Díaz TE, Kreuzer M
(2003) Supplementation of a tropical grass diet with forage legumes and Sapindus saponaria fruits: effects on in vitro ruminal nitrogen turnover and methanogenesis. Australian Journal of Agricultural Research 54, 703–713.
| Crossref | GoogleScholarGoogle Scholar |
Hess HD,
Valencia FL,
Monsalve LM,
Lascano CE, Kreuzer M
(2004) Effects of tannins in Calliandra calothyrsus and supplemental molasses on ruminal fermentation in vitro. Journal of Animal and Feed Sciences 13(Suppl. 1), 95–98.
Hoffmann L, Klein M
(1980) Die Abhängigkeit der Harnenergie vom Kohlenstoff- und Stickstoffgehalt im Harn bei Rindern, Schafen, Schweinen und Ratten (The dependence of urinary energy on the carbon and nitrogen content of the urine of cattle, sheep, pigs and rats). Archives of Animal Nutrition 30, 743–750.
Makkar HPS
(2003) Effects and fate of tannins in ruminant animals, adaptation to tannins, and strategies to overcome detrimental effects of feeding tannin-rich feeds. Small Ruminant Research 49, 241–256.
| Crossref | GoogleScholarGoogle Scholar |
Makkar HPS,
Becker K,
Abel HJ, Szegletti C
(1995a) Degradation of condensed tannins by rumen microbes exposed to Quebracho tannins (QT) in rumen simulation technique (RUSITECH) and effects of QT on fermentative processes in the RUSITEC. Journal of the Science of Food and Agriculture 69, 495–500.
Makkar HPS,
Blümmel M, Becker K
(1995b)
In vitro effects of and interactions between tannins and saponins and fate of tannins in the rumen. Journal of the Science of Food and Agriculture 69, 481–493.
Makkar HPS,
Borowy NK,
Becker K, Degen A
(1995c) Some problems in fiber determination of a tannin-rich forage (Acacia saligna leaves) and their implications in in vivo studies. Animal Feed Science and Technology 55, 67–76.
| Crossref | GoogleScholarGoogle Scholar |
Makkar, HPS ,
and
Chen, XB (2004).
Mbanzamihigo L,
Fievez V,
da Costa Gomez C,
Piattoni F,
Carlier L, Demeyer D
(2002) Methane emission from the rumen of sheep fed a mixed grass–clover pasture at two fertilisation rates in early and late season. Canadian Journal of Animal Science 82, 69–77.
McCaughey WP,
Wittenberg K, Corrigan D
(1999) Impact of pasture type on methane production by lactating beef cows. Canadian Journal of Animal Science 79, 221–226.
McNeill DM, Komolong MK, Gobius N, Barber D
(2000) Influence of dietary condensed tannin on microbial crude protein supply in sheep. ‘Tannins in livestock and human nutrition. Proceedings of an International Workshop’. Adelaide, Australia, 31 May–2 June 1999. (Ed. JD Brooker )
pp. 57–61. (Australian Centre for International Agricultural Research: Canberra, ACT)
McSweeney CS,
Palmer B,
Bunch R, Krause DO
(2001) Effect of the tropical forage calliandra on microbial protein synthesis and ecology in the rumen. Journal of Applied Microbiology 90, 78–88.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Min BR,
Barry TN,
Attwood GT, McNabb WC
(2003) The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: a review. Animal Feed Science and Technology 106, 3–19.
| Crossref | GoogleScholarGoogle Scholar |
Mueller-Harvey I, McAllan AB
(1992) Tannins. Their biochemistry and nutritional properties. Advances in Plant Cell Biochemistry and Biotechnology 1, 151–217.
Murray PJ,
Gill E,
Balsdon SL, Jarvis SC
(2001) A comparison of methane emission from sheep grazing pastures with differing management intensities. Nutrient Cycling in Agroecosystems 60, 93–97.
| Crossref | GoogleScholarGoogle Scholar |
Norton BW
(2000) The significance of tannins in tropical animal production. ‘Tannins in livestock and human nutrition. Proceedings of an International Workshop’. Adelaide, Australia, 31 May–2 June 1999. (Ed. JD Brooker )
pp. 14–23. (Australian Centre for International Agricultural Research: Canberra, ACT)
Pelchen A, Peters KJ
(1998) Methane emissions from sheep. Small Ruminant Research 27, 137–150.
| Crossref | GoogleScholarGoogle Scholar |
Reed JD
(1995) Nutritional toxicology of tannins and related polyphenols in forage legumes. Journal of Animal Science 73, 1516–1528.
| PubMed |
Robertson JB, Van Soest PJ
(1981) The detergent system of analysis. ‘The analysis of dietary fibre in food’. (Eds WPT James, O Theander)
pp. 123–158. (Marcel Dekker: New York)
Rosskopf R,
Rainer H, Giesecke D
(1991) Purin- und Pyrimidinmetaboliten zur Beruteilung des Pansenstoffwechsels: HPLC-Analysen in Milch und Blutplasma Archives of Animal Nutrition [Purine and pyrimidine metabolites to assess rumen metabolism: HPLC analyses of milk and blood] 41, 411–426.
| PubMed |
SAS (1996).
Schwarting G, Kaufmann W
(1978) Die Verdaulichkeit des Proteins beim Wiederkäuer. Zeitschrift fur Tierphysiologie, Tierernahrung und Futtermittelkunde [The digestibility of protein in ruminants] 40, 6–18.
| PubMed |
Śliwiński BJ,
Kreuzer M,
Sutter F,
Machmüller A, Wettstein H-R
(2004) Performance, body nitrogen conversion and nitrogen emission from manure of dairy cows fed diets supplemented with different plant extracts. Journal of Animal and Feed Sciences 13, 73–91.
Tangerman A, Nagengast FM
(1996) A gas chromatographic analysis of fecal short-chain fatty acids, using the direct injection method. Analytical Biochemistry 236, 1–8.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Terrill TH,
Rowan AM,
Douglas GB, Barry TN
(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 Agriculture 58, 321–329.
Terrill TH,
Waghorn GC,
Woolley DJ,
McNabb WC, Barry TN
(1994) Assay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheep. The British Journal of Nutrition 72, 467–477.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Ulyatt MJ,
Lassey KR,
Martin RJ,
Walker CF, Shelton ID
(1997) Methane emission from grazing sheep and cattle. Proceedings of the New Zealand Society of Animal Production 57, 130–133.
Van Soest PJ,
Robertson JB, Lewis BA
(1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. Journal of Dairy Science 74, 3583–3597.
| PubMed |
Varga GA, Tyrrell HF, Waldo DR, Huntington GB, Glenn BP
(1985) Effect of alfalfa or orchardgrass silage on energy and nitrogen utilization for growth by Holstein steers. ‘Energy metabolism of farm animals’. EAAP Publication No. 32.,(Eds PW Moe, HF Tyrrell, PJ Reynolds)
pp. 86–89. (Rowman and Littlefield: Totowa, NJ)
Waghorn GC,
Tavendale MH, Woodfield DR
(2002) Methanogenesis from forages fed to sheep. Proceedings of the New Zealand Grassland Association 64, 167–171.
Woodward SL,
Waghorn GC,
Ulyatt MJ, Lassey KR
(2001) Early indications that feeding Lotus will reduce methane emissions from ruminants. Proceedings of the New Zealand Society of Animal Production 61, 23–26.
Yáñez Ruiz DR,
Moumen A,
Martín García AI, Molina Alcaide E
(2004) Ruminal fermentation and degradation patterns, protozoa population, and urinary purine derivatives excretion in goats and wethers fed diets based on two-stage olive cake: effect of PEG supply. Journal of Animal Science 82, 2023–2032.
| PubMed |