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Dietary manipulation: a sustainable way to mitigate methane emissions from ruminants

  • Haque, Md Najmul (Bangabandhu Sheikh Mujibur Rahman Science and Technology University)
  • Received : 2017.11.28
  • Accepted : 2018.06.04
  • Published : 2018.06.30

Abstract

Methane emission from the enteric fermentation of ruminant livestock is a main source of greenhouse gas (GHG) emission and a major concern for global warming. Methane emission is also associated with dietary energy lose; hence, reduce feed efficiency. Due to the negative environmental impacts, methane mitigation has come forward in last few decades. To date numerous efforts were made in order to reduce methane emission from ruminants. No table mitigation approaches are rumen manipulation, alteration of rumen fermentation, modification of rumen microbial biodiversity by different means and rarely by animal manipulations. However, a comprehensive exploration for a sustainable methane mitigation approach is still lacking. Dietary modification is directly linked to changes in the rumen fermentation pattern and types of end products. Studies showed that changing fermentation pattern is one of the most effective ways of methane abatement. Desirable dietary changes provide two fold benefits i.e. improve production and reduce GHG emissions. Therefore, the aim of this review is to discuss biology of methane emission from ruminants and its mitigation through dietary manipulation.

Keywords

References

  1. Solomon S, Qin D, Manning M. Technical summary. In: Solomon S, Qin D, Manning M, Marquis M, Averyt K, Tignor MMB, Miller HL, Chen ZL, editors. Climate change 2007. The physical science basis. Contribution of working group i to the fourth assessment report of the intergovernmental panel on climate change. United Kingdom and New York, NY, USA: Cambridge University Press, Cambridge; 2007. p. 19-91.
  2. Steinfeld H, Gerber P, Wassenaar T, Castel V, Rosales M, Haan CD. Livestock's long shadow: Environmental issues and options. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO); 2006.
  3. IPCC, Climate change 2007. In: Mertz B, Davidson OR, Bosch PR, et al., editors. Mitigation. Contribution of working group iii to the fourth assessment report of the intergovernmental panel on climate change. United Kingdom and New York, NY, USA: Cambridge University Press, Cambridge; 2007.
  4. Opio C, Gerber P, Mottet A, Falcucci A, Tempio G, MacLeod M, Vellinga T, Henderson B, Steinfeld H. Greenhouse gas emissions from ruminant supply chains - a global life cycle assessment. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO); 2013.
  5. Gerber PJ, Steinfeld H, Henderson B, Mottet A, Opio C, Dijkman J, Falcucci A, Tempio G. Tackling climate change through livestock - a global assessment of emissions and mitigation opportunities. Rome, Italy: Food and Agriculture Organization of the United Nations (FAO); 2013.
  6. EPA. Inventory of u.S. Greenhouse gas emissions and sinks. Washington, DC, USA: Environmental Protection Agency (EPA); 2011.
  7. EPA. Global mitigation of non-co2 gases. Washington, DC, USA: Environmental Protection Agency (EPA); 2006.
  8. Stams AJ, Plugge CM. Electron transfer in syntrophic communities of anaerobic bacteria and archaea. Nat Rev Microbiol. 2009;7:568-77. https://doi.org/10.1038/nrmicro2166
  9. Ellis JL, Dijkstra J, Kebreab E, Bannink A, Odongo NE, McBride BW, France J. Aspects of rumen microbiology central to mechanistic modelling of methane production in cattle. J Agric Sci. 2008;146:213-33.
  10. Wolin MJ. In: Mcdonald IW, Warner ACI, editors. Interactions between the bacterial species of the rumen. : Digestion and metabolism in the ruminants. Armidale, Australia: The University of new England; 1975.
  11. Carroll EJ, Hungate RE. Formate dissimilation and methane production in bovine rumen contents. Arch Biochem Biophys. 1955;56:525-36. https://doi.org/10.1016/0003-9861(55)90272-1
  12. Hungate RE. Formate as an intermediate in bovine rumen fermentation. J Bacteriol. 1970;102:389-97.
  13. Liu YC, Whitman WB. In: Wiegel J, Maier RJ, Adams MWW, editors. Metabolic, phylogenetic, and ecological diversity of the methanogenic archaea, in Incredible anaerobes: From physiology to genomics to fuels; 2008. p. 171-89.
  14. Thauer RK, Kaster AK, Seedorf H, Buckel W, Hedderich R. Methanogenic archaea: ecologically relevant differences in energy conservation. Nat Rev Microbiol. 2008;6:579-91. https://doi.org/10.1038/nrmicro1931
  15. Morgavi DP, Forano E, Martin C, Newbold CJ. Microbial ecosystem and methanogenesis in ruminants. Animal. 2010;4:1024-36. https://doi.org/10.1017/S1751731110000546
  16. Neill AR, Grime DW, Dawson RM. Conversion of choline methyl groups through trimethylamine into methane in the rumen. Biochem J. 1978;170:529-35. https://doi.org/10.1042/bj1700529
  17. Janssen PH, Kirs M. Structure of the archaeal community of the rumen. Appl Environ Microbiol. 2008;74:3619-25. https://doi.org/10.1128/AEM.02812-07
  18. Milich L. The role of methane in global warming: where might mitigation strategies be focused? Glob Environ Chang. 1999;9:179-201. https://doi.org/10.1016/S0959-3780(98)00037-5
  19. Beauchemin KA, Kreuzer M, O'Mara F, McAllister TA. Nutritional management for enteric methane abatement: a review. Aust J Exp Agric. 2008;48:21-7. https://doi.org/10.1071/EA07199
  20. Eckard RJ, Grainger C, de Klein CAM. Options for the abatement of methane and nitrous oxide from ruminant production: a review. Livest Sci. 2010;130:47-56. https://doi.org/10.1016/j.livsci.2010.02.010
  21. Martin C, Morgavi DP, Doreau M. Methane mitigation in ruminants: from microbe to the farm scale. Animal. 2010;4:351-65. https://doi.org/10.1017/S1751731109990620
  22. Benchaar C, Pomar C, Chiquette J. Evaluation of dietary strategies to reduce methane production in ruminants: a modelling approach. Can J Anim Sci. 2001;81:563-74. https://doi.org/10.4141/A00-119
  23. Mosier AR, Duxbury JM, Freney JR, Heinemeyer O, Minami K, Johnson DE. Mitigating agricultural emissions of methane. Clim Chang. 1998;40:39-80. https://doi.org/10.1023/A:1005338731269
  24. Boadi DA, Wittenberg KM. Methane production from dairy and beef heifers fed forages differing in nutrient density using the Sulphur hexafluoride (sf6) tracer gas technique. Can J Anim Sci. 2002;82:201-6. https://doi.org/10.4141/A01-017
  25. Beever DE, Dhanoa MS, Losada HR, Evans RT, Cammell SB, France J. The effect of forage species and stage of harvest on the processes of digestion occurring in the rumen of cattle. Br J Nutr. 1986;56:439-54. https://doi.org/10.1079/BJN19860124
  26. Hammond KJ, Burke JL, Koolaard JP, Muetzel S, Pinares-Patino CS, Waghorn GC. Effects of feed intake on enteric methane emissions from sheep fed fresh white clover (trifolium repens) and perennial ryegrass (lolium perenne) forages. Anim Feed Sci Technol. 2013;179:121-32. https://doi.org/10.1016/j.anifeedsci.2012.11.004
  27. Archimede H, Eugene M, Marie Magdeleine C, Boval M, Martin C, Morgavi DP, Lecomte P, Doreau M. Comparison of methane production between c3 and c4 grasses and legumes. Anim Feed Sci Technol. 2011;166-167:59-64. https://doi.org/10.1016/j.anifeedsci.2011.04.003
  28. Boadi DA, Wittenberg KM, Scott SL, Burton D, Buckley K, Small JA, Ominski KH. Effect of low and high forage diet on enteric and manure pack greenhouse gas emissions from a feedlot. Can J Anim Sci. 2004;84:445-53. https://doi.org/10.4141/A03-079
  29. Tamminga S, Bannink A, Dijkstra J, Zom R. Feeding strategies to reduce methane loss in cattle. Lelystad: The Netherlands: Animal Nutrition and Animal Sciences Group, Wageningen UR; 2007, Report.
  30. O'Mara FP, Fitzgerald JJ, Murphy JJ, Rath M. The effect on milk production of replacing grass silage with maize silage in the diet of dairy cows. Livest Prod Sci. 1998;55:79-87. https://doi.org/10.1016/S0301-6226(98)00115-8
  31. Hassanat F, Gervais R, Julien C, Masse DI. Replacing alfalfa silage with corn silage in dairy cow diets: effects on enteric methane production, ruminal fermentation, digestion, n balance, and milk production. J Dairy Sci. 2013;96:4553-67. https://doi.org/10.3168/jds.2012-6480
  32. Ferris CP, Gordon FJ, Patterson DC, Porter MG, Yan T. The effect of genetic merit and concentrate proportion in the diet on nutrient utilization by lactating dairy cows. J Agric Sci. 1999;132:483-90. https://doi.org/10.1017/S0021859699006553
  33. Lovett D, Lovell S, Stack L, Callan J, Finlay M, Conolly J, O'Mara FP. Effect of forage/concentrate ratio and dietary coconut oil level on methane output and performance of finishing beef heifers. Livest Prod Sci. 2003;84:135-46. https://doi.org/10.1016/j.livprodsci.2003.09.010
  34. Johnson KA, Johnson DE. Methane emissions from cattle. J Anim Sci. 1995; 73:2483-92. https://doi.org/10.2527/1995.7382483x
  35. Beauchemin KA, McAllister TA, McGinn SM. Dietary mitigation of enteric methane from cattle. CAB Reviews, vol. 4: Perspectives in Agriculture, Veterinary Science, Nutrition and Natural Resources; 2009. p. 1-18.
  36. Murphy MR, Baldwin RL, Koong LJ. Estimation of stoichiometric parameters for rumen fermentation of roughage and concentrate diets. J Anim Sci. 1982;55:411-21. https://doi.org/10.2527/jas1982.552411x
  37. Kessel JAS, Russell JB. The effect of ph on ruminal methanogenesis. FEMS Microbiol Ecol. 1996;20:205-10. https://doi.org/10.1111/j.1574-6941.1996.tb00319.x
  38. Finlay BJ, Esteban G, Clarke KJ, Williams AG, Embley TM, Hirt RP. Some rumen ciliates have endosymbiotic methanogens. FEMS Microbiol Lett. 1994;117:157-61. https://doi.org/10.1111/j.1574-6968.1994.tb06758.x
  39. Orskov ER. Starch digestion and utilization in ruminants. J Anim Sci. 1986;63: 1624-33. https://doi.org/10.2527/jas1986.6351624x
  40. Harmon DL, Yamka RM, Elam NA. Factors affecting intestinal starch digestion in ruminants: a review. Can J Anim Sci. 2004;84:309-18. https://doi.org/10.4141/A03-077
  41. Hindrichsen IK, Wettstein HR, Machmuller A, Jorg B, Kreuzer M. Effect of the carbohydrate composition of feed concentratates on methane emission from dairy cows and their slurry. Environ Monit Assess. 2005;107:329-50. https://doi.org/10.1007/s10661-005-3008-3
  42. Hindrichsen IK, Kreuzer M. High methanogenic potential of sucrose compared with starch at high ruminal ph. J Anim Physiol Anim Nutr. 2009;93:61-5. https://doi.org/10.1111/j.1439-0396.2007.00779.x
  43. Boadi D, Benchaar C, Chiquette J, Masse D. Mitigation strategies to reduce enteric methane emissions from dairy cows: update review. Can J Anim Sci. 2004;84:319-35. https://doi.org/10.4141/A03-109
  44. Giger-Reverdin S, Morand-Fehr P, Tran G. Literature survey of the influence of dietary fat composition on methane production in dairy cattle. Livest Prod Sci. 2003;82:73-9. https://doi.org/10.1016/S0301-6226(03)00002-2
  45. Jenkins TC. Lipid-metabolism in the rumen. J Dairy Sci. 1993;76:3851-63. https://doi.org/10.3168/jds.S0022-0302(93)77727-9
  46. Grainger C, Beauchemin KA. Can enteric methane emissions from ruminants be lowered without lowering their production? Anim Feed Sci Technol. 2011;166-67:308-20.
  47. Doreau M, Chilliard Y. Digestion and metabolism of dietary fat in farm animals. Br J Nutr. 1997;78(Suppl 1):S15-35. https://doi.org/10.1079/BJN19970132
  48. Castillo C, Benedito JL, Mendez J, Pereira V, Lopez-Alonso M, Miranda M, Hernandez J. Organic acids as a substitute for monensin in diets for beef cattle. Anim Feed Sci Technol. 2004;115:101-16. https://doi.org/10.1016/j.anifeedsci.2004.02.001
  49. Newbold CJ, Lopez S, Nelson N, Ouda JO, Wallace RJ, Moss AR. 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. https://doi.org/10.1079/BJN20051445
  50. McAllister TA, Newbold CJ. Redirecting rumen fermentation to reduce methanogenesis. Aust J Exp Agric. 2008;48:7-13. https://doi.org/10.1071/EA07218
  51. Kolver ES. Fumarate reduces methane production from pasture fermented in continuous culture: proceedings of the New Zealand society of animal production: New Zealand Society of Animal Production; 2004.
  52. Ungerfeld EM, Kohn RA, Wallace RJ, Newbold CJ. A meta-analysis of fumarate effects on methane production in ruminal batch cultures. J Anim Sci. 2007;85:2556-63. https://doi.org/10.2527/jas.2006-674
  53. Beauchemin K, McGinn S. Methane emission from beef cattle: effects of fumaric acid, essential oil and canola oil. J Anim Sci. 2006;84:1489-96. https://doi.org/10.2527/2006.8461489x
  54. Greathead H. Plants and plant extracts for improving animal productivity. Proc Nutr Soc. 2003;62:279-90. https://doi.org/10.1079/PNS2002197
  55. Burt S. Essential oils: their antibacterial properties and potential applications in foods - a review. Int J Food Microbiol. 2004;94:223-53. https://doi.org/10.1016/j.ijfoodmicro.2004.03.022
  56. Benchaar C, Calsamiglia S, Chaves AV, Fraser GR, Colombatto D, McAllister TA, Beauchemin KA. A review of plant-derived essential oils in ruminant nutrition and production. Anim Feed Sci Technol. 2008;145:209-28. https://doi.org/10.1016/j.anifeedsci.2007.04.014
  57. Benchaar C, Greathead H. Essential oils and opportunities to mitigate enteric methane emissions from ruminants. Anim Feed Sci Technol. 2011; 166-67:338-55.
  58. Jouany JP, Morgavi DR. Use of 'natural' products as alternatives to antibiotic feed additives in ruminant production. Animal. 2007;1:1443-66.
  59. Newbold CJ, McIntosh FM, Williams P, Losa R, Wallace RJ. Effects of a specific blend of essential oil compounds on rumen fermentation. Anim Feed Sci Technol. 2004;114:105-12. https://doi.org/10.1016/j.anifeedsci.2003.12.006
  60. McGuffey RK, Richardson LF, Wilkinson JID. Ionophores for dairy cattle: current status and future outlook. J Dairy Sci. 2001;84:E194-203. https://doi.org/10.3168/jds.S0022-0302(01)70218-4
  61. Hook SE, Northwood KS, Wright ADG, McBride BW. Long-term monensin supplementation does not significantly affect the quantity or diversity of methanogens in the rumen of the lactating dairy cow. Appl Environ Microbiol. 2009;75:374-80. https://doi.org/10.1128/AEM.01672-08
  62. Patra AK. Enteric methane mitigation technologies for ruminant livestock: a synthesis of current research and future directions. Environ Monit Assess. 2012;184:1929-52. https://doi.org/10.1007/s10661-011-2090-y
  63. McGinn SM, Beauchemin KA, Coates T, Colombatto D. Methane emissions from beef cattle: effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid. J Anim Sci. 2004;82:3346-56. https://doi.org/10.2527/2004.82113346x
  64. Odongo NE, Bagg R, Vessie G, Dick P, Or-Rashid MM, Hook SE, Gray JT, Kebreab E, France J, McBride BW. Long-term effects of feeding monensin on methane production in lactating dairy cows. J Dairy Sci. 2007;90:1781-8. https://doi.org/10.3168/jds.2006-708
  65. Guan H, Wittenberg KM, Ominski KH, Krause DO. Efficacy of ionophores in cattle diets for mitigation of enteric methane. J Anim Sci. 2006;84:1896-906. https://doi.org/10.2527/jas.2005-652
  66. Moss AR, Jouany JP, Newbold J. Methane production by ruminants: its contribution to global warming. Ann Zootech. 2000;49:231-53. https://doi.org/10.1051/animres:2000119
  67. Lopez S, McIntosh E, Wallace RJ, Newbold CJ. Effect of adding acetogenic bacteria on methane production by mixed rumen microorganisms. Anim Feed Sci Technol. 1999;78:1-9. https://doi.org/10.1016/S0377-8401(98)00273-9
  68. McAllister TA, Beauchemin KA, Alazzeh AY, Baah J, Teather RM, Stanford K. Review: the use of direct fed microbials to mitigate pathogens and enhance production in cattle. Can J Anim Sci. 2011;91:193-211. https://doi.org/10.4141/cjas10047
  69. Newbold CJ, Rode LM. Dietary additives to control methanogenesis in the rumen. Int Congr Ser. 2006;1293:138-47. https://doi.org/10.1016/j.ics.2006.03.047
  70. Beauchemin KA, Colombatto D, Morgavi DP, Yang WZ. Use of exogenous fibrolytic enzymes to improve feed utilization by ruminants. J Anim Sci. 2003;81:E37-47.
  71. Eun JS, Beauchemin KA. Assessment of the efficacy of varying experimental exogenous fibrolytic enzymes using in vitro fermentation characteristics. Anim Feed Sci Technol. 2007;132:298-315. https://doi.org/10.1016/j.anifeedsci.2006.02.014
  72. Kristjansson J, Schönheit P, Thauer R. Different ks values for hydrogen of methanogenic bacteria and sulfate reducing bacteria: an explanation for the apparent inhibition of methanogenesis by sulfate. Arch Microbiol. 1982;131: 278-82. https://doi.org/10.1007/BF00405893
  73. Leng RA. The potential of feeding nitrate to reduce enteric methane production in ruminants, in Report. Canberra ACT Australia: The Department of Climate Change, commonwealth government of Australia; 2008. Available on http://www.penambulbooks.com/Downloads/Leng- Final%20Modified%20%2017-9-2008.pdf
  74. van Zijderveld SM, Gerrits WJJ, Apajalahti JA, Newbold JR, Dijkstra J, Leng RA, Perdok HB. Nitrate and sulfate: effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep. J Dairy Sci. 2010;93: 5856-66. https://doi.org/10.3168/jds.2010-3281
  75. van Zijderveld SM, Gerrits WJJ, Dijkstra J, Newbold JR, Hulshof RBA, Perdok HB. Persistency of methane mitigation by dietary nitrate supplementation in dairy cows. J Dairy Sci. 2011;94:4028-38. https://doi.org/10.3168/jds.2011-4236
  76. Bruning-Fann CS, Kaneene JB. The effects of nitrate, nitrite, and n-nitroso compounds on animal health. Vet Hum Toxicol. 1993;35:237-53.
  77. Bodas R, Prieto N, Garcia-Gonzalez R, Andres S, Giraldez FJ, Lopez S. Manipulation of rumen fermentation and methane production with plant secondary metabolites. Anim Feed Sci Technol. 2012;176:78-93. https://doi.org/10.1016/j.anifeedsci.2012.07.010
  78. Hristov AN, Ivan M, Neill L, McAllister TA. Evaluation of several potential bioactive agents for reducing protozoal activity in vitro. Anim Feed Sci Technol. 2003;105: 163-84. https://doi.org/10.1016/S0377-8401(03)00060-9
  79. Patra AK, Saxena J. Dietary phytochemicals as rumen modifiers: a review of the effects on microbial populations. Antonie Van Leeuwenhoek. 2009;96: 363-75. https://doi.org/10.1007/s10482-009-9364-1
  80. Dorman HJD, Deans SG. Antimicrobial agents from plants: antibacterial activity of plant volatile oils. J Appl Microbiol. 2000;88:308-16. https://doi.org/10.1046/j.1365-2672.2000.00969.x
  81. Ramirez-Restrepo CA, Barry TN. Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Anim Feed Sci Technol. 2005;120:179-201. https://doi.org/10.1016/j.anifeedsci.2005.01.015
  82. Wallace RJ. Antimicrobial properties of plant secondary metabolites. Proc Nutr Soc. 2004;63:621-9. https://doi.org/10.1079/PNS2004393
  83. Goel G, Makkar HP. Methane mitigation from ruminants using tannins and saponins. Trop Anim Health Prod. 2012;44:729-39. https://doi.org/10.1007/s11250-011-9966-2
  84. Liu H, Vaddella V, Zhou D. Effects of chestnut tannins and coconut oil on growth performance, methane emission, ruminal fermentation, and microbial populations in sheep. J Dairy Sci. 2011;94:6069-77. https://doi.org/10.3168/jds.2011-4508
  85. Newbold CJ, el Hassan SM, Wang J, Ortega ME, Wallace RJ. Influence of foliage from african multipurpose trees on activity of rumen protozoa and bacteria. Br J Nutr. 1997;78:237-49. https://doi.org/10.1079/BJN19970143
  86. Patra AK, Saxena J. The effect and mode of action of saponins on the microbial populations and fermentation in the rumen and ruminant production. Nutr Res Rev. 2009;22:204-19. https://doi.org/10.1017/S0954422409990163
  87. Wright ADG, Kennedy P, O'Neill CJ, Toovey AF, Popovski S, Rea SM, Pimm CL, Klein L. Reducing methane emissions in sheep by immunization against rumen methanogens. Vaccine. 2004;22:3976-85. https://doi.org/10.1016/j.vaccine.2004.03.053
  88. Williams YJ, Popovski S, Rea SM, Skillman LC, Toovey AF, Northwood KS, Wright ADG. A vaccine against rumen methanogens can alter the composition of archaeal populations. Appl Environ Microbiol. 2009;75:1860-6. https://doi.org/10.1128/AEM.02453-08
  89. Goel G, Makkar HP, Becker K. Inhibition of methanogens by bromochloromethane: effects on microbial communities and rumen fermentation using batch and continuous fermentations. Br J Nutr. 2009; 101:1484-92. https://doi.org/10.1017/S0007114508076198
  90. Joblin KN. Ruminal acetogens and their potential to lower ruminant methane emissions. Aust J Agric Res. 1999;50:1307-13. https://doi.org/10.1071/AR99004
  91. Weisbjerg MR, Terkelsen M, Hvelplund T, Madsen J. Increased productivity in tanzanian cattle production is the main approach to reduce methane emission per unit of product. in Book of Abstracts, 35th Annual scientific conference. Olasiti Garden, Arusha, Tanzania; 2012.
  92. Clark H, Pinares-Patino C, de Klein C. Methane and nitrous oxide emissions from grazed grasslands, in 20th International Grassland Congress. In: McGilloway DA, editor. Grassland: A Global Resource. The Netherlands: Wageningen Academic Publishers; 2005. p. 279-93.
  93. Madsen J, Lassen J, Hvelplund T, Weisbjerg MR. A fast, easy, reliable and cheap method to measure the methane production from ruminants, in Eaap publication no. 127. Wageningen: Wageningen Academic Publishers; 2010. p. 121-2.
  94. Pinares-Patio CS, Ulyatt MJ, Lassey KR, Barry TN, Holmes CW. Persistence of differences between sheep in methane emission under generous grazing conditions. J Agric Sci. 2003;140:227-33. https://doi.org/10.1017/S0021859603003071
  95. Kohn RA, Boston RC. In: McNamara JP, France J, Beever DE, editors. The role of thermodynamics in controlling rumen metabolism: Modelling nutrient utilization in farm animals. Wallingford, Oxon, GBR: CABI Publishing; 2000.
  96. Ungerfeld EM. A theoretical comparison between two ruminal electron sinks. Frontiers in Microbiol. 2013;4:319.

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  20. Are dairy cows with a more reactive temperament less efficient in energetic metabolism and do they produce more enteric methane? vol.15, pp.6, 2018, https://doi.org/10.1016/j.animal.2021.100224
  21. Towards Sustainable Livestock Production: Estimation of Methane Emissions and Dietary Interventions for Mitigation vol.13, pp.11, 2021, https://doi.org/10.3390/su13116081
  22. Catfish oil supplementation in Bali cattle diet: Effects on rumen fermentation parameters, carboxymethylcellulase and protease activity in vitro vol.782, pp.2, 2021, https://doi.org/10.1088/1755-1315/782/2/022082
  23. Effects of probiotics and encapsulated probiotics on enteric methane emission and nutrient digestibility in vitro vol.788, pp.1, 2018, https://doi.org/10.1088/1755-1315/788/1/012050
  24. Dose response of biochar and wood vinegar on in vitro batch culture ruminal fermentation using contrasting feed substrates vol.5, pp.3, 2021, https://doi.org/10.1093/tas/txab107
  25. Insects as Novel Ruminant Feed and a Potential Mitigation Strategy for Methane Emissions vol.11, pp.9, 2018, https://doi.org/10.3390/ani11092648
  26. Effects of Replacing Cottonseed Meal with Corn Dried Distillers’ Grain on Ruminal Parameters, Performance, and Enteric Methane Emissions in Young Nellore Bulls Reared in Tropical Pastures vol.11, pp.10, 2021, https://doi.org/10.3390/ani11102959
  27. Mitigating rumen methane and enhancing fermentation using rambutan fruit peel powder and urea in lactating dairy cows vol.105, pp.6, 2021, https://doi.org/10.1111/jpn.13526
  28. The Use of Temperate Tannin Containing Forage Legumes to Improve Sustainability in Forage-Livestock Production vol.11, pp.11, 2018, https://doi.org/10.3390/agronomy11112264
  29. Lovastatin as a supplement to mitigate rumen methanogenesis: an overview vol.12, pp.1, 2018, https://doi.org/10.1186/s40104-021-00641-8
  30. Changed Rumen Fermentation, Blood Parameters, and Microbial Population in Fattening Steers Receiving a High Concentrate Diet with Saccharomyces cerevisiae Improve Growth Performance vol.8, pp.12, 2018, https://doi.org/10.3390/vetsci8120294