Meta-analysis of the relationship between dietary tannin level and methane formation in ruminants from in vivo and in vitro experiments

Journal of Animal Physiology and Animal Nutrition

Volumn 96, Issue 3, 2012, Pages 365-375

  Jayanegara, A ^a   Leiber, F ^a   Kreuzer, M ^a  

^a ETH ZURICH   (Switzerland)

Author keywords

Meta analysis; Methane; Rumen; Ruminant; Tannin

Indexed keywords

METHANE; TANNIN DERIVATIVE;

ANIMAL; ANIMAL DISEASE; ANIMAL FOOD; BOVIDS; CHEMISTRY; DIET; META ANALYSIS; METABOLISM; REVIEW;

ANIMAL FEED; ANIMAL NUTRITIONAL PHYSIOLOGICAL PHENOMENA; ANIMALS; DIET; METHANE; RUMINANTS; TANNINS;

ANIMALIA; BACTERIA (MICROORGANISMS); BOVIDAE;

EID: 84857877446     PISSN: 09312439     EISSN: 14390396     Source Type: Journal    
DOI: 10.1111/j.1439-0396.2011.01172.x     Document Type: Review

References (57)

1. Animut, G.; Puchala, R.; Goetsch, A. L.; Patra, A. K.; Sahlu, T.; Varel, V. H.; Wells, J., 2008a: Methane emission by goats consuming different sources of condensed tannins. Animal Feed Science and Technology 144, 228-241.
2. Animut, G.; Puchala, R.; Goetsch, A. L.; Patra, A. K.; Sahlu, T.; Varel, V. H.; Wells, J., 2008b: Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza. Animal Feed Science and Technology 144, 212-227.
3. Beauchemin, K. A.; McGinn, S. M.; Martinez, T. F.; McAllister, T. A., 2007: Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle. Journal of Animal Science 85, 1990-1996.
4. Beauchemin, K. A.; Kreuzer, M.; O'Mara, F.; McAllister, T. A., 2008: Nutritional management for enteric methane abatement: a review. Australian Journal of Experimental Agriculture 48, 21-27.
5. Bekele, A. Z.; Clement, C.; Kreuzer, M.; Soliva, C. R., 2009: Efficiency of Sesbania sesban and Acacia angustissima in limiting methanogenesis and increasing ruminally available nitrogen in a tropical grass-based diet depends on accession. Animal Production Science 49, 145-153.
6. Benchaar, C.; Calsamiglia, S.; Chaves, A. V.; Fraser, G. R.; Colombatto, D.; McAllister, T. A.; Beauchemin, K. A., 2008: A review of plant-derived essential oils in ruminant nutrition and production. Animal Feed Science and Technology 145, 209-228.
7. Bhatta, R.; Tajima, K.; Takusari, N.; Higuchi, K.; Enishi, O.; Kurihara, M., 2007: Comparison of in vivo and in vitro techniques for methane production from ruminant diets. Asian-Australasian Journal of Animal Sciences 20, 1049-1056.
8. Bhatta, R.; Uyeno, Y.; Tajima, K.; Takenaka, A.; Yabumoto, Y.; Nonaka, I.; Enishi, O.; Kurihara, M., 2009: Difference in nature of tannins on in vitro ruminal methane and volatile fatty acid production and on methanogenic archaea and protozoal populations. Journal of Dairy Science 92, 5512-5522.
9. Blümmel, M.; Givens, D. I.; Moss, A. R., 2005: Comparison of methane produced by straw fed sheep in open-circuit respiration with methane predicted by fermentation characteristics measured by an in vitro gas procedure. Animal Feed Science and Technology 123-124, 379-390.
10. Carulla, J. E.; Kreuzer, M.; Machmüller, A.; Hess, H. D., 2005: Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Australian Journal of Agricultural Research 56, 961-970.
11. Czerkawski, J. W.; Breckenridge, G., 1977: Design and development of a long-term rumen simulation technique (Rusitec). British Journal of Nutrition 38, 371-384.
12. De Oliveira, S. G.; Berchielli, T. T.; Pedreira, M. S.; Primavesi, O.; Frighetto, R.; Lima, M. A., 2007: Effect of tannin levels in sorghum silage and concentrate supplementation on apparent digestibility and methane emission in beef cattle. Animal Feed Science and Technology 135, 236-248.
13. Flachowsky, G.; Lebzien, P., 2009: Comments on in vitro studies with methane inhibitors. Animal Feed Science and Technology 151, 337-339.
14. Goel, G.; Puniya, A. K.; Aguilar, C. N.; Singh, K., 2005: Interaction of gut microflora with tannins in feeds. Naturwissenschaften 92, 497-503.
15. Grainger, C.; Clarke, T.; Auldist, M. J.; Beauchemin, K. A.; McGinn, 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 Science 89, 241-251.
16. Hariadi, B. T.; Santoso, B., 2010: Evaluation of tropical plants containing tannin on in vitro methanogenesis and fermentation parameters using rumen fluid. Journal of the Science of Food and Agriculture 90, 456-461.
17. Hayler, R.; Steingass, H.; Drochner, W., 1998: Effect of various feedstuffs rich in tannin content on rumen methanogenesis in vitro using the Hohenheim Gas Test. Proceedings of the Society of Nutrition Physiology 7, 35.
18. Hess, H. D.; Kreuzer, M.; Diaz, T. E.; Lascano, C. E.; Carulla, J. E.; Soliva, C. R.; Machmüller, A., 2003: Saponin rich tropical fruits affect fermentation and methanogenesis in faunated and defaunated rumen fluid. Animal Feed Science and Technology 109, 79-94.
19. Hess, H. D.; Tiemann, T. T.; Noto, F.; Franzel, S.; Lascano, C. E.; Kreuzer, M., 2006: The effects of cultivation site on forage quality of Calliandra calothyrsus var. Patulul. Agroforestry Systems 68, 209-220.
20. Hess, H. D.; Mera, M. L.; Tiemann, T. T.; Lascano, C. E.; Kreuzer, M., 2008: In vitro assessment of the suitability of replacing the low-tannin legume Vigna unguiculata with the tanniniferous legumes Leucaena leucocephala or Calliandra calothyrsus in a tropical grass diet. Animal Feed Science and Technology 147, 105-115.
21. Jayanegara, A.; Togtokhbayar, N.; Makkar, H. P. S.; Becker, K., 2009: Tannins determined by various methods as predictors of methane production reduction potential of plants by an in vitro rumen fermentation system. Animal Feed Science and Technology 150, 230-237.
22. Jayanegara, A.; Wina, E.; Soliva, C. R.; Marquardt, S.; Kreuzer, M.; Leiber, F., 2011a: Dependence of forage quality and methanogenic potential of tropical plants on their phenolic fractions as determined by principal component analysis. Animal Feed Science and Technology 163, 231-243.
23. Jayanegara, A.; Marquardt, S.; Kreuzer, M.; Leiber, F., 2011b: Nutrient and energy content, in vitro ruminal fermentation characteristics and methanogenic potential of alpine forage plant species during early summer. Journal of the Science of Food and Agriculture, online first (doi: ).
24. Khiaosa-ard, R.; Bryner, S. F.; Scheeder, M. R. L.; Wettstein, H. R.; Leiber, F.; Kreuzer, M.; Soliva, C. R., 2009: Evidence for the inhibition of the terminal step of ruminal α-linolenic acid biohydrogenation by condensed tannins. Journal of Dairy Science 92, 177-188.
25. Krishnamoorthy, U.; Rymer, C.; Robinson, P. H., 2005: The in vitro gas production technique: limitations and opportunities. Animal Feed Science and Technology 123-124, 1-7.
26. Külling, D. R.; Menzi, H.; Kröber, T. F.; Neftel, A.; Sutter, F.; Lischer, P.; Kreuzer, M., 2001: Emissions of ammonia, nitrous oxide and methane from different types of dairy manure during storage as affected by dietary protein content. Journal of Agricultural Science, Cambridge 137, 235-250.
27. Machmüller, A.; Ossowski, D. A.; Kreuzer, M., 2000: Comparative evaluation of the effects of coconut oil, oilseeds and crystalline fat on methane release, digestion and energy balance in lambs. Animal Feed Science and Technology 85, 41-60.
28. Makkar, H. P. S., 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.
29. Makkar, H. P. S.; Becker, K.; Abel, H.; Szegletti, C., 1995: Degradation of condensed tannins by rumen microbes exposed to quebracho tannins (QT) in Rumen Simulation Technique (RUSITEC) and effects of QT on fermentative processes in the RUSITEC. Journal of the Science of Food and Agriculture 69, 495-500.
30. McSweeney, C. S.; Palmer, B.; McNeill, D. M.; Krause, D. O., 2001: Microbial interactions with tannins: nutritional consequences for ruminants. Animal Feed Science and Technology 91, 83-93.
31. Min, B. R.; Pinchak, W. E.; Fulford, J. D.; Puchala, R., 2005: Wheat pasture bloat dynamics, in vitro ruminal gas production, and potential bloat mitigation with condensed tannins. Journal of Animal Science 83, 1322-1331.
32. Moss, A. R.; Givens, D. I., 1997: Methane production from a range of feedstuffs as determined in vitro using the cumulative gas production technique and compared with that measured in vivo. Proceedings of the British Society of Animal Science, p. 194.
33. Moss, A. R.; Jouany, J. P.; Newbold, J., 2000: Methane production by ruminants: its contribution to global warming. Annales de Zootechnie 49, 231-253.
34. Mueller-Harvey, I., 2006: Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 86, 2010-2037.
35. Owens, F. N.; Bergen, W. G., 1983: Nitrogen metabolism of ruminant animals: historical perspective, current understanding and future implications. Journal of Animal Science 57, 498-518.
36. Patra, A. K., 2010: Effects of supplementing low-quality roughages with tree foliages on digestibility, nitrogen utilization and rumen characteristics in sheep: a meta-analysis. Journal of Animal Physiology and Animal Nutrition 94, 338-353.
37. Patra, A. K.; Saxena, J., 2009: Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek 96, 363-375.
38. Pinares-Patino, C. S.; Ulyatt, M. J.; Waghorn, G. C.; Lassey, K. R.; Barry, T. N.; Holmes, C. W.; Johnson, D. E., 2003: Methane emission by alpaca and sheep fed on lucerne hay or grazed on pastures of perennial ryegrass/white clover or birdsfoot trefoil. Journal of Agricultural Science 140, 215-226.
39. Poungchompu, O.; Wanapat, M.; Wachirapakorn, C.; Wanapat, S.; Cherdthong, A., 2009: Manipulation of ruminal fermentation and methane production by dietary saponins and tannins from mangosteen peel and soapberry fruit. Archives of Animal Nutrition 63, 389-400.
40. Puchala, R.; Min, B. R.; Goetsch, A. L.; Sahlu, T., 2005: The effect of a condensed tannin-containing forage on methane emission by goats. Journal of Animal Science 83, 182-186.
41. Ramirez-Restrepo, C. A.; Barry, T. N.; Marriner, A.; Lopez-Villalobos, N.; McWilliam, E. L.; Lassey, K. R.; Clark, H., 2010: Effects of grazing willow fodder blocks upon methane production and blood composition in young sheep. Animal Feed Science and Technology 155, 33-43.
42. Reed, J. D., 1995: Nutritional toxicology of tannins and related polyphenols in forage legumes. Journal of Animal Science 73, 1516-1528.
43. SAS Institute Inc., 2008: SAS/STAT Software, Version 9.2. SAS Institute Inc., Cary, NC, USA.
44. Sauvant, D.; Schmidely, P.; Daudin, J. J.; St-Pierre, N. R., 2008: Meta-analyses of experimental data in animal nutrition. Animal 2, 1203-1214.
45. Scalbert, A., 1991: Antimicrobial properties of tannins. Phytochemistry 30, 3875-3883.
46. Silanikove, N.; Perevolotsky, A.; Provenza, F. D., 2001: Use of tannin-binding chemicals to assay for tannins and their negative postingestive effects in ruminants. Animal Feed Science and Technology 91, 69-81.
47. Śliwiński, B. J.; Soliva, C. R.; Machmüller, A.; Kreuzer, M., 2002a: Efficacy of plant extracts rich in secondary constituents to modify rumen fermentation. Animal Feed Science and Technology 101, 101-114.
48. Śliwiński, B. J.; Kreuzer, M.; Wettstein, H. R.; Machmüller, A., 2002b: Rumen fermentation and nitrogen balance of lambs fed diets containing plant extracts rich in tannins and saponins, and associated emissions of nitrogen and methane. Archives of Animal Nutrition 56, 379-392.
49. St-Pierre, N. R., 2001: Integrating quantitative findings from multiple studies using mixed model methodology. Journal of Dairy Science 84, 741-755.
50. Tavendale, M. H.; Meagher, L. P.; Pacheco, D.; Walker, N.; Attwood, G. T.; Sivakumaran, S., 2005: Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Animal Feed Science and Technology 123-124, 403-419.
51. Tiemann, T. T.; Lascano, C. E.; Wettstein, H. R.; Mayer, A. C.; Kreuzer, M.; Hess, H. D., 2008a: Effect of the tropical tannin-rich shrub legumes Calliandra calothyrsus and Flemingia macrophylla on methane emission and nitrogen and energy balance in growing lambs. Animal 2, 790-799.
52. Tiemann, T. T.; Avila, P.; Ramirez, G.; Lascano, C. E.; Kreuzer, M.; Hess, H. D., 2008b: In vitro ruminal fermentation of tanniniferous tropical plants: plant-specific tannin effects and counteracting efficiency of PEG. Animal Feed Science and Technology 146, 222-241.
53. Tiemann, T. T.; Lascano, C. E.; Kreuzer, M.; Hess, H. D., 2008c: The ruminal degradability of fibre explains part of the low nutritional value and reduced methanogenesis in highly tanniniferous tropical legumes. Journal of the Science of Food and Agriculture 88, 1794-1803.
54. Vogels, G. D.; Hoppe, W. F.; Stumm, C. K., 1980: Association of methanogenic bacteria with rumen ciliates. Applied and Environmental Microbiology 40, 608-612.
55. Wang, Y.; Xu, Z.; Bach, S. J.; McAllister, T. A., 2008: Effects of phlorotannins from Ascophyllum nodosum (brown seaweed) on in vitro ruminal digestion of mixed forage or barley grain. Animal Feed Science and Technology 145, 375-395.
56. Woodward, S. L.; Waghorn, G. C.; Lassey, K. R.; Laboyrie, P. G., 2002: Does feeding sulla (Hedysarum coronarium) reduce methane emissions from dairy cows? Proceedings of the New Zealand Society of Animal Production 62, 227-230.
57. Woodward, S. L.; Waghorn, G. C.; Laboyrie, P. G., 2004: Condensed tannins in birdsfoot trefoil (Lotus corniculatus) reduce methane emissions from dairy cows. Proceedings of the New Zealand Society of Animal Production 64, 160-164.