Control of Rumen Microbial Fermentation for Mitigating Methane Emissions from the Rumen

  • Mitsumori, Makoto (National Institute of Livestock and Grassland Science) ;
  • Sun, Weibin (College of Animal Science and Technology, Northwest Agriculture and Forestry University)
  • Published : 2008.01.01


The rumen microbial ecosystem produces methane as a result of anaerobic fermentation. Methanogenesis in the rumen is thought to represent a 2-12% loss of energy intake and is estimated to be about 15% of total atmospheric methane emissions. While methanogenesis in the rumen is conducted by methanogens, PCR-based techniques have recently detected many uncultured methanogens which have a broader phylogenetic range than cultured strains isolated from the rumen. Strategies for reduction of methane emissions from the rumen have been proposed. These include 1) control of components in feed, 2) application of feed additives and 3) biological control of rumen fermentation. In any case, although it could be possible that repression of hydrogen-producing reactions leads to abatement of methane production, repression of hydrogen-producing reactions means repression of the activity of rumen fermentation and leads to restrained digestibility of carbohydrates and suppression of microbial growth. Thus, in order to reduce the flow of hydrogen into methane production, hydrogen should be diverted into propionate production via lactate or fumarate.


  1. Asanuma, N., M. Iwamoto and T. Hino. 1999a. Effect of the addition of fumarate on methane production by ruminal microorganisms in vitro. J. Dairy Sci. 82:780-787.
  2. Asanuma, N., M. Iwamoto and T. Hino. 1999b. The production of formate, a substrate for methanogenesis, from compounds related with the glyoxylate cycle by mixed ruminal microbes. Anim. Sci. J. 70:67-73.
  3. Asanuma, N. and T. Hino. 2000a. Effects of pH and energy supply on activity and amount of pyruvate formate-lyase in Streptococcus bovis. Appl. Environ. Microbiol. 66:3773-3777.
  4. Asanuma, N. and T. Hino. 2000b. Activity and properties of fumarate reductase in ruminal bacteria. J. Gen. Appl. Microbiol. 46:119-125.
  5. Blaxter, K. L. and J. L. Clapperton. 1965. Prediction of the amount of methane produced by ruminants. Br. J. Nutr. 19:511-522.
  6. Busquet, M., S. Calsamiglia, A. Ferret, P. W. Cardozo and C. Kamel. 2005. Effects of cinnamaldehyde and garlic oil on rumen microbial fermentation in a dual flow continuous culture. J. Dairy Sci. 88:2508-2516.
  7. Busquet, M., S. Calsamiglia, A. Ferret and C. Kamel. 2006. Plant extracts affect in vitro rumen microbial fermentation. J. Dairy Sci. 89:761-771.
  8. Carro, M. D. and M. J. Ranilla. 2003a. Effect of the addition of malate on in vitro rumen fermentation of cereal grains. Br. J. Nutr. 89:181-188.
  9. Carro, M. D. and M. J. Ranilla. 2003b. Influence of different concentrations of disodium fumarate on methane production and fermentation of concentrate feeds by rumen microorganisms in vitro. Br. J. Nutr. 90:617-623.
  10. Chalupa, W. 1977. Manipulating rumen fermentation. J. Anim. Sci. 46:585-599.
  11. Counotte, G. H. M., R. A. Prins, R. H. A. M. Janssen and M. J. A. deBie. 1981. Role of Megasphaera elsdenii in the Fermentation of dl-[2-13C]lactate in the Rumen of Dairy Cattle. Appl. Environ. Microbiol. 42:649-655.
  12. Czerkawski, J. W. 1969. Methane production in ruminants and its significance. World Review of Ruminants and Dietetics 11:240-282.
  13. Dawson, K. A., M. A. Rasmussen and M. J. Allison. 1997. Digestive disorders and nutritional toxicity. In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 633-660.
  14. Denman, S. E., N. Tomkins and C. S. McSweeney. 2006. Monitoring the effect of bromochloromethane on methanogen populations within the rumen using qPCR. The 2nd International Conference on Greenhouse Gases and Animal Agriculture GGAA2005-Working papers. pp. 112-114.
  15. Dennis, S. M., T. G. Nagaraja and A. D. Dayton. 1986. Effect of lasalocid, monensin and thiopeptin on rumen protozoa. Res. Vet. Sci. 41:251-256.
  16. Dohme, F., A. Machmüller, A. Wasserfallen and M. Kreuzer. 2000. Comparative efficiency of various fats rich in medium-chain fatty acids to suppress ruminal methanogenesis as measured with RUSITEC. Can. J. Anim. Sci. 80:473-484.
  17. Dohme, F., A. Machmüller, A. Wasserfallen and M. Kreuzer. 2001. Ruminal methanogenesis as influenced by individual fatty acids supplemented to complete ruminant diets. Lett. Appl. Microbiol. 32:47-51.
  18. Dong Y., H. D. Bae, T. A. McAllister, G. W. Mathison and K.-J. Cheng. 1997. Lipid-induced depression of methane production and digestibility in the artificial rumen system (RUSITEC). Can. J. Anim. Sci. 77:269-278.
  19. Ermler, U., W. Grabarse, S. Shima, M. Goubeaud and R. K. Thauer. 1997. Crystal structure of methyl coenzyme M reductase: the key enzyme of biological methane formation. Sci. 278:1457-1462.
  20. Fahey, G. C. Jr., L. D. Bourquin, E. C. Titgemeyer and D. G. Atwell. 1993. Postharvest treatment of fibrous feedstuffs to improve their nutritive value. In: Forage Cell Wall Structure and Digestibility (Ed. H. G. Jung, D. R. Buxton, R. D. Hatfield and J. Ralph), American Society of Agronomy, Madison, Wisconsin, USA. pp. 715-766.
  21. Finlay, B. J., G. Esteban, K. J. Clarke, A. G. Williams, T. M. Embley and R. P. Hirt. 1994. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiol. Lett. 117:157- 161.
  22. Friedrich, M. W. 2005. Methyl-coenzyme M reductase genes: unique functional markers for methanogenic and anaerobic methane-oxidizing Archaea. Methods Enzymol. 397:428-442.
  23. Garcia-Martinez, R., M. J. Ranilla, M. L. Tejido and M. D. Carro. 2005. 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. 94:71-77.
  24. Gill, H. S., Q. Shu and R. A. Leng. 2000. Immunization with Streptococcus bovis protects against lactic acidosis in sheep. Vaccine. 18:2541-2548.
  25. Gomez, J. A., M. L. Tejido and M. D. Carro. 2005. Influence of disodium malate on microbial growth and fermentation in rumen-simulation technique fermenters receiving medium- and high-concentrate diets. Br. J. Nutr. 93:479-484.
  26. Hegarty, R. S. 2002. Strategies for mitigating methane emissions from livestock-Australian options and opportunities. In: Greenhouse Gases and Animal Agriculture (Ed. J. Takahashi and B. A. Young). Elsevier, Amsterdam. pp. 61-65.
  27. Hino, T., K. Takeshi, M. Kanda and S. Kumazawa. 1993. Effects of aibellin, a novel peptide antibiotic, on rumen fermentation in vitro. J. Dairy Sci. 76:2213-2221.
  28. Hino, T., H. Saitoh, T. Miwa, M. Kanda and S. Kumazawa. 1994. Effect of aibellin, a peptide antibiotic, on propionate production in the rumen of goats. J. Dairy Sci. 77:3426-3431.
  29. Hoogenraad, N. J., F. J. Hirk, I. Holmes and N. F. Millis. 1967. Bacteriophages in rumen contents of sheep. J. Gen. Virol. 1:575-576.
  30. Hu, W. L., Y. M. Wu, J. X. Liu, Y. Q. Guo and J. A. Ye. 2005. Tea saponins affect in vitro fermentation and methanogenesis in faunated and defaunated rumen fluid. J. Zhejiang Univ. Sci. 6B:787-792.
  31. Hungate, R. E. 1966. The rumen and its microbes. Acad. Press, New York, USA.
  32. Hungate, R. E., W. Smith, T. Bauchop, Ida Yu and J. C. Rabinowitz. 1970. Formate as an Intermediate in the Bovine Rumen Fermentation. J. Bacteriol. 102:389-397
  33. Irbis, C. and K. Ushida. 2004. Detection of methanogens and proteobacteria from a single cell of rumen ciliate protozoa. J. Gen. Appl. Microbiol. 50:203-212.
  34. Iwamoto, M., N. Asanuma and T. Hino. 1999. Effects of nitrate combined with fumarate on methanogenesis, fermentation, and cellulose digestion by mixed ruminal microbes in vitro. Anim. Sci. J. 70:471-478.
  35. Jarvis, G. N., C. Strompl, D. M. Burgess, L. C. Skillman, E. R. B. Moore and K. N. Joblin. 2000. Isolation and identification of ruminal methanogens from grazing cattle. Curr. Microbiol. 40:327-332.
  36. Kajikawa, H., C. Valdes, K. Hillman, R. J. Wallace and C. J. Newbold. 2003. Methane oxidation and its coupled electronsink reactions in ruminal fluid. Lett. Appl. Microbiol. 36:354- 357.
  37. Klieve, A. V. and R. S. Hegarty. 1999. Opportunities for biological control of ruminal methanogenesis. Aust. J. Agric. Res. 50: 1315-1320.
  38. Klieve, A. V., P. A. Bain, M. T. Yokoyama, D. Ouwerkerk, R. J. Forster and A. F. Turner. 2004. Bacteriophages that infect the cellulolytic ruminal bacterium Ruminococcus albus AR67. Lett. Appl. Microbiol. 38:333-338.
  39. Kume, S. 2002. Establishment of profitable dairy farming system on control of methane production in Hokkaido region. In: Greenhouse Gases and Animal Agriculture. (Ed. J. Takahashi and B. A. Young), Elsevier, Amsterdam. pp. 87-94.
  40. Kurihara, M., M. Shibata, T. Nishida, A. Purnomoadi and F. Terada. 1997. Methane production and its dietary manipulation in ruminants. In: Ruminal Microbes and Digestive Physiology in Ruminants (Ed. R. Onodera et al.) Japan Scientific Societies Press, Tokyo, Japan. pp 199-208.
  41. Kurihara, M., T. Nishida, A. Purnomoadi, M. Shibata and F. Terada. 2002. The prediction of methane conversion rate from dietary factors. In: Greenhouse Gases and Animal Agriculture. (Ed. J. Takahashi and B. A. Young), Elsevier, Amsterdam. pp. 171-174.
  42. Lee, S. S., J. T. Hsu, H. C. Mantovani and J. B. Russell. 2002. The effect of bovicin HC5, a bacteriocin from Streptococcus bovis HC5, on ruminal methane production in vitro. FEMS Microbiol. Lett. 217:51-55.
  43. Leng, R. A. 1993. Quantitative ruminant nutrition-A green science. Aust. J. Agric. Res. 44:363-380.
  44. Lila, Z. A., N. Mohammed, S. Kanda, T. Kamada and H. Itabashi. 2003. Effect of sarsaponin on ruminal fermentation with particular reference to methane production in vitro. J. Dairy Sci. 86:3330-3336.
  45. Lila, Z. A., N. Mohammed, T. Yasui, Y. Kurokawa, S. Kanda and H. Itabashi. 2004. Effects of a twin strain of saccharomyces cerevisiae live cells on mixed ruminal microorganism fermentation in vitro. J. Anim. Sci. 82:1847-1854.
  46. Lovett, D. K., D. McGilloway, A. Bortolozzo, M. Hawkins, J. Callan, B. Flynn and F. P. O'Mara. 2006. In vitro fermentation patterns and methane production as influenced by cultivar and season of harvest of Lolium perenne L. Grass and Forage Sci. 61:9-21.
  47. Luton, P. E., J. M. Wayne, R. J. Sharp and P. W. Riley. 2002. The mcrA gene as an alternative to 16S rRNA in the phylogenetic analysis of methanogen populations in landfill. Microbiol. 148:3521-3530.
  48. Martin, S. A., D. J. Nisbet and R. G. Dean. 1989. Influence of a commercial yeast supplement on the in-vitro ruminal fermentation. Nutr. Rep. Int. 40:395-403.
  49. McCaughey, W. P., K. Wittenberg and D. Corrigan. 1997. Methane production by steers on pasture. Can. J. Anim. Sci. 77:519-524.
  50. Machmuller, A., C. R. Soliva and M. Kreuzer. 2003. Effect of coconut oil and defaunation treatment on methanogenesis in sheep. Reprod. Nutr. Dev. 43:41-55.
  51. Mackie, R. I. and F. M. Gilchrist. 1979. Changes in lactateproducing and lactate-utilizing bacteria in relation to pH in the rumen of sheep during stepwise adaptation to a highconcentrate diet. Appl. Environ. Microbiol. 38:422-430.
  52. McCrabb, G. J., K. T. Berger, T. Magner, C. May and R. A. Hunter. 1997. Inhibiting methane production in Brahman cattle by dietary supplementation with a novel compound and the effects on growth. Aust. J. Agric. Res. 48:323-329.
  53. Miller, T. L. and M. J. Wolin. 2001. Inhibition of growth of methane-producing bacteria of the ruminant forestomach by hydroxymethylglutaryl-SCoA reductase inhibitors. J. Dairy Sci. 84:1445-1448.
  54. Mitsumori, M., N. Ajisaka, K. Tajima, H. Kajikawa and M. Kurihara. 2002a. Detection of Proteobacteria from the rumen by PCR using methanotroph-specific primers. Lett. Appl. Microbiol. 35:251-255.
  55. Mitsumori, M., K. Tajima and H. Itabashi. 2002b. Detection of methanogens from the rumen by PCR-based techniques In: Greenhouse Gases and Animal Agriculture (Ed. J. Takahashi and B. A. Young), Elsevier, Amsterdam. pp. 125-128.
  56. Mohammed, N., N. Ajisaka, Z. A. Lila, K. Hara, K. Mikuni, K. Hara, S. Kanda and H. Itabashi. 2004. Effect of Japanese horseradish oil on methane production and ruminal fermentation in vitro and in steers. J. Anim. Sci. 82:1839-1846.
  57. Nagaraja, T. G., C. J. Newbold, C. J. Van Nevel and D. I. Demeyer. 1997. Manipulation of ruminal fermentation. In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 523-632.
  58. Newbold, C. J., R. J. Wallace and N. D. Walker. 1993. The effect of tetronasin and monensin on fermentation, microbial numbers and the development of ionophore-resistant bacteria in the rumen. J. Appl. Bacteriol. 75:129-134.
  59. Newbold, C. J., B. Lassalas and J. P. Jouany. 1995. The importance of methanogens associated with ciliate protozoa in ruminal methane production in vitro. Lett. Appl. Microbiol. 21:230-234.
  60. Newbold, C. J., K. Ushida, B. Morvan, G. Fonty and J. P. Jouany. 1996a. The role of ciliate protozoa in the lysis of methanogenic archaea in rumen fluid. Lett. Appl. Microbiol. 23:421-425.
  61. Newbold, C. J., R. J. Wallace and F. M. McIntosh. 1996b. Mode of action of the yeast Saccharomyces cerevisiae as a feed additive for ruminants. Br. J. Nutr. 76:249-261.
  62. Newbold, C. J., S. Lopez, N. Nelson, J. O. Ouda, R. J. Wallace and A. R. Moss. 2005. Propionate precursors and other metabolic intermediates as possible alternative electron acceptors to methanogenesis in ruminal fermentation in vitro. Br. J. Nutr. 94:27-35.
  63. Newbold, C. J. and L. M. Rode. 2006. Dietary additives to control methanogenesis in the rumen. The 2nd International Conference on Greenhouse Gases and Animal Agriculture GGAA2005-Working papers. pp. 60-70.
  64. Orpin, C. G. and K. N. Joblin. 1997. The rumen anaerobic fungi. In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 140-195.
  65. Regensbogenova, M., N. R. McEwan, P. Javorsky, S. Kisidayova, T. Michalowski, C. J. Newbold, J. H. Hackstein and P. Pristas. 2004. A re-appraisal of the diversity of the methanogens associated with the rumen ciliates. FEMS Microbiol. Lett. 238:307-313.
  66. Russell, J. B. and D. B. Dombrowski. 1980. Effect of pH on the efficiency of growth by pure cultures of rumen bacteria in continuous culture. Appl. Environ. Microbiol. 39:604-610.
  67. Russell, J. B. and R. J. Wallace. 1997. Energy-yielding and energy-consuming reactions. In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 246-282.
  68. Russell, J. B. 1998. The importance of pH in the regulation of ruminal acetate to propionate ratio and methane production in vitro. J. Dairy Sci. 81:3222-3230.
  69. Russell, J. B. and J. L. Rychlik. 2001. Factors that alter rumen microbial ecology. Sci. 292:1119-1122.
  70. Russell, J. B. and A. J. Houlihan. 2003. Ionophore resistance of ruminal bacteria and its potential impact on human health. FEMS Microbiol. Rev. 27:65-74.
  71. Satter, L. D., J. W. Suttie and B. R. Baumgardt. 1964. Dietary induced changes in volatile fatty acid formation from cellulose-C14 and hemicellulose-C14. J. Dairy Sci. 47:1365- 1370.
  72. Shibata, M., F. Terada, K. Iwasaki, M. Kurihara and T. Nishida. 1992. Methane Production in heifers, sheep and goats consuming diets of various hay-concentrations, Anim. Sci. Technol. 63:1221-1227.
  73. Shibata, M., F. Terada, M. Kurihara, T. Nishida and K. Iwasaki. 1993. Estimation of methane production in ruminants. Anim. Sci. Technol. 64:790-796.
  74. Shima, S., E. Warkentin, R. K. Thauer and U. Ermler. 2002. Structure and function of enzymes involved in the methanogenic pathway utilizing carbon dioxide and molecular hydrogen. J. Biosci. Bioeng. 93:519-530.
  75. Shu, Q., M. A. Hillard, B. M. Bindon, E. Duan, Y. Xu, S. H. Bird, J. B. Rowe, V. H. Oddy and H. S. Gill. 2000. Effects of various adjuvants on efficacy of a vaccine against Streptococcus bovis and Lactobacillus spp. in cattle. Am. J. Vet. Res. 61:839-843.
  76. Skillman, L. C., P. N. Evans, C. Strompl and K. N. Joblin. 2006. 16S rDNA directed PCR primers and detection of methanogens in the bovine rumen. Lett. Appl. Microbiol. 42:222-228.
  77. Slyter, L. L. 1986. Ability of pH-Selected Mixed Ruminal Microbial Populations to Digest Fiber at Various pHs. Appl. Environ. Microbiol. 52:390-391.
  78. Stewart, C. S. 1977. Factors Affecting the Cellulolytic Activity of Rumen Contents. Appl. Environ. Microbiol. 33:497-502.
  79. Stewart, C. S., H. J. Flint and M. P. Bryant. 1997. The rumen bacteria. In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 10-72.
  80. Swain, R. A., J. V. Nolan and A. V. Klieve AV. 1996. Natural variability and diurnal fluctuations within the bacteriophage population of the rumen. Appl. Environ. Microbiol. 62:994- 997.
  81. Tajima, K., R. I. Aminov, T. Nagamine, H. Matsui, M. Nakamura and Y. Benno. 2001. Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR. Appl. Environ. Microbiol. 67:2766-2774.
  82. Takahashi, J., B. Mwenya, B. Santoso, C. Sar, K. Umetsu, T. Kishimoto, K. Nishizaki, K. Kimura and O. Hamamoto. 2005. Mitigation of methane emission and energy recycling in animal agricultural systems. Asian-Aust. J. Anim. Sci. 18:1199-1208.
  83. Tedeschi, L. O., D. G. Fox and T. P. Tylutki. 2003. Potential environmental benefits of ionophores in ruminant diets. J. Environ. Qual. 32:1591-1602.
  84. Tokura, M., I. Chagan, K. Ushida and Y. Kojima. 1999. Phylogenetic study of methanogens associated with rumen ciliates. Curr. Microbiol. 39:123-128.
  85. Tatsuoka, N., N. Mohammed, M. Mitsumori, K. Hara, M. Kurihara and H. Itabashi. 2004. Phylogenetic analysis of methyl coenzyme-M reductase detected from the bovine rumen. Lett. Appl. Microbiol. 39:257-260.
  86. Ueno, Y., K. Yamada, N. Yoshida, S. Maruyama and Y. Isozaki. 2006. Evidence from fluid inclusions for microbial methanogenesis in the early Archaean era. Nature. 440:516- 519.
  87. Ulyatt, M. J., K. R. Lassey, I. D. Shelton and C. F. Walker. 2002. Seasonal variation in methane emission from dairy cows and breeding ewes grazing ryegrass/white clover pasture in New Zealand. New Zealand J. Agri. Res. 45:217-226.
  88. Ungerfeld, E. M., S. R. Rust and R. Burnett. 2003. Use of some novel alternative electron sinks to inhibit ruminal methanogenesis. Reprod. Nutr. Dev. 43:189-202.
  89. Ungerfeld, E. M., S. R. Rust, D. R. Boone and Y. Liu. 2004. Effects of several inhibitors on pure cultures of ruminal methanogens. J. Appl. Microbiol. 97:520-526.
  90. Ushida, K. and J. P. Jouany. 1996. Methane production associated with rumen-ciliated protozoa and its effect on protozoan activity. Lett. Appl. Microbiol. 23:129-132.
  91. Vogels, G. D., W. F. Hoppe and C. K. Stumm. 1980. Association of methanogenic bacteria with rumen ciliates. Appl. Environ. Microbiol. 40:608-612.
  92. Wallace, R. J. 2004. Antimicrobial properties of plant secondary metabolites. Proc. Nutr. Soc. 63:621-629.
  93. Weimer, P. J. 1998. Manipulating ruminal fermentation: a microbial ecological perspective. J. Anim. Sci. 76:3114-3122.
  94. Whitelaw, F. G., J. M. Eadie, L. A. Bruce and W. J. Shand. 1984. Methane formation in faunated and ciliate-free cattle and its relationship with rumen volatile fatty acid proportions. Br. J. Nutr. 52:261-275.
  95. Williams, A. G. and G. S. Coleman. 1997. The rumen protozoa, In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 73-139.
  96. Wolin, M. J. 1979. The rumen fermentation: a model for microbial interactions in anaerobic ecosystems. Adv. Microbial. Ecol. 3:49-77.
  97. Wolin, M. J., T. L. Miller and C. S. Stewart. 1997. Microbemicrobe interactions In: The Rumen Microbial Ecosystem. 2nd ed. (Ed. P. J. Hobson and C. S. Stewart), Blackie Acad. Profess. London. pp. 467-491.
  98. Wright, A. D., P. Kennedy, C. J. O'Neill, A. F. Toovey, S. Popovski, S. M. Rea, C. L. Pimm and L. Klein. 2004a. Reducing methane emissions in sheep by immunization against rumen methanogens. Vaccine. 22:3976-3985.
  99. Wright, A. D., A. J. Williams, B. Winder, C. T. Christophersen, S. L. Rodgers and K. D. Smith. 2004b. Molecular diversity of rumen methanogens from sheep in Western Australia. Appl. Environ. Microbiol. 70:1263-1270.
  100. Yan, T., R. E. Agnew, F. J. Gordon and M. G. Porter. 2000. Prediction of methane energy output in dairy and beef cattle offered grass silage-based diets. Livest. Prod. Sci. 64:253-263.
  101. Yoshii T., N. Asanuma and T. Hino. 2005. Effect of ethanol on nitrate and nitrite reduction and methanogenesis in the ruminal microbiota. Anim. Sci. J. 76:37-42.

Cited by

  1. Combination Effects of Nitrocompounds, Pyromellitic Diimide, and 2-Bromoethanesulfonate on in Vitro Ruminal Methane Production and Fermentation of a Grain-Rich Feed vol.60, pp.1, 2012,
  2. Effect of bromochloromethane and fumarate on phylogenetic diversity of the formyltetrahydrofolate synthetase gene in bovine rumen vol.85, pp.1, 2013,
  3. Effect of cashew nut shell liquid on metabolic hydrogen flow on bovine rumen fermentation vol.85, pp.3, 2013,
  4. Effects of Coconut Materials on In vitro Ruminal Methanogenesis and Fermentation Characteristics vol.27, pp.12, 2014,
  5. Effects of Dietary Linseed Oil and Propionate Precursors on Ruminal Microbial Community, Composition, and Diversity in Yanbian Yellow Cattle vol.10, pp.5, 2015,
  6. 外源添加产乙酸菌和酿酒酵母发酵物对瘤ƒƒ发酵特性及产乙酸菌菌群结构的影响 vol.16, pp.8, 2015,
  7. rumen fermentation, methanogenesis and methanogens vol.87, pp.3, 2015,
  8. The effect of a high-roughage diet on the metabolism of aromatic compounds by rumen microbes: a metagenomic study using Mehsani buffalo (Bubalus bubalis) vol.100, pp.3, 2016,
  9. Effects of Medicinal Herb Extracts on In vitro Ruminal Methanogenesis, Microbe Diversity and Fermentation System vol.29, pp.9, 2016,
  10. Degradabilidade de gramíneas, fermentação e protozoários no rúmen de bovinos em dietas com diferentes aditivos vol.18, pp.2, 2017,
  11. The ruminal microbiome associated with methane emissions from ruminant livestock vol.8, pp.1, 2017,
  12. In vitro rumen fermentation of soluble and non-soluble polymeric carbohydrates in relation to ruminal acidosis pp.1869-2044, 2017,
  13. Sustained reduction in methane production from long-term addition of 3-nitrooxypropanol to a beef cattle diet1 vol.93, pp.4, 2015,
  14. Effect of Rhodophyta extracts on in vitro ruminal fermentation characteristics, methanogenesis and microbial populations vol.31, pp.1, 2018,
  15. Effects of Gelidium amansii extracts on in vitro ruminal fermentation characteristics, methanogenesis, and microbial populations vol.31, pp.1, 2018,
  16. Candidate metabolites for methane mitigation in the forage legume biserrula vol.38, pp.3, 2018,
  17. Effect of feeding of blend of essential oils on methane production, growth, and nutrient utilization in growing buffaloes vol.31, pp.5, 2018,