Effects of condensed tannins from Leucaena on methane production, rumen fermentation and populations of methanogens and protozoa in vitro

Animal Feed Science and Technology

Volumn 169, Issue 3-4, 2011, Pages 185-193

  Tan, H Y ^a   Sieo, C C ^a   Abdullah, N ^a   Liang, J B ^a   Huang, X D ^a   Ho, Y W ^a  

^a UNIVERSITY PUTRA MALAYSIA   (Malaysia)

Author keywords

Condensed tannins; Leucaena leucocephala hybrid Rendang; Methane; Methanogen; Protozoa

Indexed keywords

ARCHAEA; LEUCAENA; LEUCAENA LEUCOCEPHALA; METHANOBACTERIALES; PANICUM MAXIMUM; PROTOZOA;

EID: 80053053708     PISSN: 03778401     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.anifeedsci.2011.07.004     Document Type: Article

References (69)

1. Aerts R.J., Barry T.N., McNabb W.C. Polyphenols and agriculture: beneficial effects of proanthocyanidins in forages. Agric. Ecosyst. Environ. 1999, 75:1-12.
2. Altschul S.F., Madden T.L., Schaffer A.A., Zhang J., Zhang Z., Miller W., Lipman D.J. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 1997, 25:3389.
3. Animut G., Puchala R., Goetsch A.L., Patra A.K., Sahlu T., Varel V.H., Wells J. Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza. Anim. Feed Sci. Technol. 2008, 144:212-227.
4. Ashelford K.E., Chuzhanova N.A., Fry J.C., Jones A.J., Weightman A.J. At least 1 in 20 16S rRNA sequence records currently held in public repositories is estimated to contain substantial anomalies. Appl. Environ. Microbiol. 2005, 71:7724.
5. Beauchemin K.A., McGinn S.M., Martinez T.F., McAllister T.A. Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle. J. Anim Sci. 2007, 85:1990-1996.
6. Benson D.A., Karsch-Mizrachi I., Lipman D.J., Ostell J., Wheeler D.L. GenBank. Nucleic Acids Res. 2008, 36:D25-D30.
7. Brewbaker J.L. Leucaena: a multipurpose tree genus for tropical agroforestry. Agroforestry: A Decade of Development 1987, International Council for Research in Agroforestry, Nairobi, Kenya, 289-323. H.A. Steppler, P.K. Ramachandran Nair (Eds.).
8. Carulla J.E., Kreuzer M., Machmüller A., Hess H.D. Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep. Aust. J. Agric. Res. 2005, 56:961-970.
9. Chaucheyras F., Fonty G., Bertin G., Gouet P. In vitro H2 utilization by a ruminal acetogenic bacterium cultivated alone or in association with an archaea methanogen is stimulated by a probiotic strain of Saccharomyces cerevisiae. Appl. Environ. Microbiol. 1995, 61:3466.
10. De Man J.C. The probability of most probable numbers. Appl. Microbiol. Biotechnol. 1975, 1:67-78.
11. FAOSTAT, 2006. Animal production online database. Food and Agriculture Organization of the 432 United Nations, Rome, Italy. http://faostat.fao.org/default.aspx.
12. García-Martínez R., Ranilla M.J., Tejido M.L., Carro M.D. Effects of disodium fumarate on in vitro rumen microbial growth, methane production and fermentation of diets differing in their forage: concentrate ratio. Br. J. Nutr. 2005, 94:71-77.
13. Getachew G., Blümmel M., Makkar H.P.S., Becker K. In vitro gas measuring techniques for assessment of nutritional quality of feeds: a review. Anim. Feed Sci. Technol. 1998, 72:261-281.
14. Hall, 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41, 95-98.
15. Hess H.D., Monsalve L.M., Lascano C.E., Carulla J.E., Díaz T.E., Kreuzer M. Supplementation of a tropical grass diet with forage legumes and Sapindus saponaria fruits: effects on in vitro ruminal nitrogen turnover and methanogenesis. Aust. J. Agric. Res. 2003, 54:703-713.
16. Huang X.D., Liang J.B., Tan H.Y., Yahya R., Khamseekhiew B., Ho Y.W. Molecular weight and protein binding affinity of Leucaena condensed tannins and their effects on in vitro fermentation parameters. Anim. Feed Sci. Technol. 2010, 159:81-87.
17. IPCC, 2001. Climate Change 2001. The Scientific Basis. Cambridge University Press, Cambridge, UK.
18. IPCC, 2007. Summary for policymakers. In: Metz, B., Davidson, O.R., Bosch, P. R., Dave, R., Meyer, L. A. (Eds.), Climate Change 2007: Mitigation of Climate Change, Contribution of Working Group III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, Cambridge University Press, Cambridge, UK and New York, NY, USA.
19. Irbis C., Ushida K. Detection of methanogens and proteobacteria from a single cell of rumen ciliate protozoa. J. Gen. Appl. Microbiol. 2004, 50:203-212.
20. Joblin, K.N., 2005. Methanogenic archaea. In: Makkar, H.P.S., McSweeney, C.S. (Eds.), Methods in Gut Microbial Ecology for Ruminants, Springer, Dordrecht, The Netherlands, pp. 47-53.
21. Johnson K.A., Johnson D.E. Methane emissions from cattle. J. Anim. Sci. 1995, 73:2483.
22. Jones R.J., Meyer J.H.F., Bechaz M., Stoltz M.A. An approach to screening potential pasture species for condensed tannin activity. Anim. Feed Sci. Technol. 2000, 85:269-277.
23. Kamra D.N., Sawal R.K., Pathak N.N., Kewalramani N., Agarwal N. Diurnal variation in ciliate protozoa in the rumen of black buck (Antilope cervicapra) fed green forage. Lett. Appl. Microbiol. 1991, 13:165-167.
24. Kariuki I.W., Norton B.W. The digestion of dietary protein bound by condensed tannins in the gastro-intestinal tract of sheep. Anim. Feed Sci. Technol. 2008, 142:197-209.
25. Klein D., Janda P., Steinborn R., Müller M., Salmons B., Günzburg W.H. Proviral load determination of different feline immunodeficiency virus isolates using real-time polymerase chain reaction: influence of mismatches on quantification. Electrophoresis 1999, 20:291-299.
26. Leinmüller E., Steingass H., Menke K.H. Tannins in ruminant feedstuffs. Anim. Res. Dev. 1991, 33:9-62.
27. Liang, J.B., Khamseekhiew, B., 2006. Binding affinity of condensed tannins for protein complexes of selected Leucaena species. Proceedings of the XIIth AAAP Animal Science Congress - Abstract, BEXCO, Busan, Korea, September 18-22, p. 269.
28. Lin C., Raskin L., Stahl D.A. Microbial community structure in gastrointestinal tracts of domestic animals: comparative analyses using rRNA-targeted oligonucleotide probes. FEMS Microbiol. Ecol. 1997, 22:281-294.
29. Lopez S., Valdés C., Newbold C.J., Wallace R.J. Influence of sodium fumarate addition on rumen fermentation in vitro. Br. J. Nutr. 1999, 81:59-64.
30. Mackie R.I., Bryant M.P. Acetogenesis and the rumen: syntrophic relationships. Acetogenesis 1994, Chapman and Hall, New York, NY, USA, pp. 331-364. H.L. Drake (Ed.).
31. Makkar, H., Blümmel, M., Becker, K., 1995a. Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins, and their implication in gas production and true digestibility in in vitro techniques. Br. J. Nutr. 73, 897-913.
32. Makkar H.P.S., Blümmel M., Becker K. In vitro effects of and interactions between tannins and saponins and fate of tannins in the rumen. J. Sci. Food Agric. 1995, 69:481-493.
33. McAllister T.A., Newbold C.J. Redirecting rumen fermentation to reduce methanogenesis. Aust. J. Exp. Agric. 2008, 48:7-13.
34. Menke K.H., Raab L., Salewski A., Steingass H., Fritz D., Schneider W. The estimation of the digestibility and metabolizable energy content of ruminant feeding stuffs from the gas production when they are incubated with rumen liquor in vitro. J. Agric. Sci. 1979, 93:217-222.
35. Menke K.H., Steingass H. Estimation of the energetic feed value obtained from chemical analysis and in vitro gas production using rumen fluid. Anim. Res. Dev. 1988, 28:7-55.
36. Newbold C.J., López S., Nelson N., Ouda J.O., Wallace R.J., Moss A.R. Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. Br. J. Nutr. 2005, 94:27-35.
37. Orskov E.R., McDonald I. The estimation of protein degradability in the rumen from incubation measurements weighted according to the rate of passage. J. Agric. Sci. 1979, 92:499-503.
38. Osborne N.J.T., McNeill D.M. Characterisation of Leucaena condensed tannins by size and protein precipitation capacity. J. Sci. Food Agric. 2001, 81:1113-1119.
39. Patra A.K., Saxena J. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie van Leeuwenhoek 2009, 96:363-375.
40. Pei C.X., Mao S.Y., Cheng Y.F., Zhu W.Y. Diversity, abundance and novel 16S rRNA gene sequences of methanogens in rumen liquid, solid and epithelium fractions of Jinnan cattle. Animal 2010, 4:20-29.
41. Pinares-Patino C.S., Ulyatt M.J., Waghorn G.C., Lassey K.R., Barry T.N., Holmes C.W., Johnson D.E. Methane emission by alpaca and sheep fed on lucerne hay or grazed on pastures of perennial ryegrass/white clover or birdsfoot trefoil. J. Agric. Sci. 2003, 140:215-226.
42. Puchala R., Min B.R., Goetsch A.L., Sahlu T. The effect of a condensed tannin-containing forage on methane emission by goats. J. Anim Sci. 2005, 83:182.
43. Regensbogenova, M., Pristas, P., Javorsky, P., Moon-Van Der Staay, S.Y., Van Der Staay, G.W.M., Hackstein, J.H.P., Newbold, C.J., McEwan, N.R., 2004. Assessment of ciliates in the sheep rumen by DGGE. Lett. Appl. Microbiol. 39, 144-147.
44. Sallam S.M.A., da Silve Bueno I.C., Godoy P.B., Nozella E.F., Vitti D.M.S.S., Abdalla A.L. Ruminal fermentation and tannins bioactivity of some browses using a semi-automated gas production technique. Trop. Subtrop. Agroecosys. 2010, 12:1.
45. SAS Institute, 2008. SAS Version 9.0. SAS Inst. Inc., Cary, NC, USA.
46. Sharp R., Ziemer C.J., Stern M.D., Stahl D.A. Taxon-specific associations between protozoal and methanogen populations in the rumen and a model rumen system. FEMS Microbiol. Ecol. 1998, 26:71-78.
47. Shibata M., Terada F. Factors affecting methane production and mitigation in ruminants. Anim. Sci. J. 2010, 81:2-10.
48. Skillman L.C., Evans P.N., Naylor G.E., Morvan B., Jarvis G.N., Joblin K.N. 16S ribosomal DNA-directed PCR primers for ruminal methanogens and identification of methanogens colonising young lambs. Anaerobe 2004, 10:277-285.
49. Sylvester J.T., Karnati S.K.R., Yu Z., Morrison M., Firkins J.L. Development of an assay to quantify rumen ciliate protozoal biomass in cows using real-time PCR. J. Nutr. 2004, 134:3378-3380.
50. Tavendale M.H., Meagher L.P., Pacheco D., Walker N., Attwood G.T., Sivakumaran S. Methane production from in vitro rumen incubations with Lotus pedunculatus and Medicago sativa, and effects of extractable condensed tannin fractions on methanogenesis. Anim. Feed Sci. Technol. 2005, 123:403-419.
51. Terrill T.H., Windham W.R., Evans J.J., Hoveland C.S. Condensed tannin concentration in Sericea lespedeza as influenced by preservation method. Crop Sci. 1990, 30:219-224.
52. Terrill T.H., Rowan A.M., Douglas G.B., Barry T.N. Determination of extractable and bound condensed tannin concentrations in forage plants, protein concentrate meals and cereal grains. J. Sci. Food Agric. 1992, 58:321-329.
53. Tiemann T.T., Avila P., Ramírez G., Lascano C.E., Kreuzer M., Hess H.D. In vitro ruminal fermentation of tanniniferous tropical plants: Plant-specific tannin effects and counteracting efficiency of PEG. Anim. Feed Sci. Technol. 2008, 146:222-241.
54. Tilley J.M.A., Terry R.A. A two-stage technique for the in vitro digestion of forage crops. Grass Forage Sci. 1963, 18:104-111.
55. Ungerfeld E.M., Rust S.R., Burnett R. Use of some novel alternative electron sinks to inhibit ruminal methanogenesis. Reprod. Nutr. Dev. 2003, 43:189-202.
56. Universiti Putra Malaysia Animal Care and Use Committee, 2008. Reference No. UPM/FPV/PS/3.2.1.551/AUP-R32, Serdang, Selangor, Malaysia.
57. Vogels G.D., Hoppe W.F., Stumm C.K. Association of methanogenic bacteria with rumen ciliates. Appl. Environ. Microbiol. 1980, 40:608.
58. Waghorn G.C., Tavendale M.H., Woodfield D.R. Methanogenesis in forages fed to sheep. Proc. NZ Grassland Assoc. 2002, 64:167-171.
59. Whitford M.F., Teather R.M., Forster R.J. Phylogenetic analysis of methanogens from the bovine rumen. BMC Microbiol. 2001, 1:1-5.
60. Wong C.C., Chen C.P., Hutton E.M. Development of acid/psyllid tolerant Leucaena hybrids for ruminant production. Leucaena-Adaptation, Quality and Farming System 1998, 132-135. ACIAR Proceedings, 86, Canberra, Australia. H.M. Shelton, R.C. Gutteridge, B.F. Muellen, R.A. Bray (Eds.).
61. Woodward S.L., Waghorn G.C., Ulyatt M.J., Lassey K.R. Early indications that feeding Lotus will reduce methane emissions from ruminants. Proc. N. Z. Soc. Anim. Prod. 2001, 61:23-26.
62. Woodward S.L., Waghorn G.C., Lassey K.R., Laboyrie P.G. Does feeding sulla (Hedysarum coronarium) reduce methane emissions from dairy cows. Proc. N. Z. Soc. Anim. Prod. 2002, 62:227-230.
63. Woodward S.L., Waghorn G.C., Laboyrie P.G. Condensed tannins in birdsfoot trefoil (Lotus corniculatus) reduce methane emissions from dairy cows. Proc. N. Z. Soc. Anim. Prod. 2004, 64:160-164.
64. Wright A.D.G., Pimm C. Improved strategy for presumptive identification of methanogens using 16S riboprinting. J. Microbiol. Methods 2003, 55:337-349.
65. Wright A.D.G., Williams A.J., Winder B., Christophersen C.T., Rodgers S.L., Smith K.D. Molecular diversity of rumen methanogens from sheep in Western Australia. Appl. Environ. Microbiol. 2004, 70:1263-1270.
66. Wright A.D.G., Ma X., Obispo N.E. Methanobrevibacter phylotypes are the dominant methanogens in sheep from Venezuela. Microb. Ecol. 2008, 56:390-394.
67. Yanagita K., Kamagata Y., Kawaharasaki M., Suzuki T., Nakamura Y., Minato H. Phylogenetic analysis of methanogens in sheep rumen ecosystem and detection of Methanomicrobium mobile by fluorescence in situ hybridization. Biosci. Biotechnol. Biochem. 2000, 64:1737-1742.
68. Yu Y., Lee C., Kim J., Hwang S. Group-specific primer and probe sets to detect methanogenic communities using quantitative real-time polymerase chain reaction. Biotechnol. Bioeng. 2005, 89:670-679.
69. Zhang C.M., Guo Y.Q., Yuan Z.P., Wu Y.M., Wang J.K., Liu J.X., Zhu W.Y. Effect of octadeca carbon fatty acids on microbial fermentation, methanogenesis and microbial flora in vitro. Anim. Feed Sci. Technol. 2008, 146:259-269.