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Invited Review: Methane sources, quantification, and mitigation in grazing beef systems

      ABSTRACT

      Purpose

      The purpose of the review was to examine enteric methane emissions, quantification methods, and mitigation strategies in grazing beef systems.

      Sources

      Peer-reviewed literature and conference abstracts were the main sources of information for this review.

      Synthesis

      Methane emissions (CH4) can be reduced by improving forage quality by including more cool-season forages and legumes and rotationally grazing animals. Including forages with beneficial secondary compounds such as condensed tannins and saponins also has CH4-mitigation potential. Providing nutritional supplements that improve the nutritional status of the animal and the efficiency of feed energy use has the potential to reduce CH4 emissions from grazing cattle. Genetic selection has shown some viability in reducing herd emissions, but heritability estimates are low for CH4 yield. More research is needed to understand the potential. Soil methanotrophy may partially offset CH4 emissions when animals are stocked moderately but soil CH4 uptake rates are relatively low in most grazing ecosystems. A new metric to quantify the global warming potential of CH4, GWP*, may allow future models to more appropriately consider the behavior and effects of CH4 in the atmosphere.

      Conclusions and Applications

      Methane mitigation strategies in grazing environments are limited, but producer decisions that improve the nutritional status of animals, the quality of the forage base, and supplementation of known CH4-mitigation compounds can reduce CH4 production. Now that less expensive, easier to use quantification tools exist, researchers need to conduct more long-term monitoring experiments and focus on reducing CH4 production of grazing animals where potential for reduction is largest.

      Key words

      INTRODUCTION

      The environmental impact of the beef industry has received increased public attention due to its perceived effects on climate change. A recent International Panel on Climate Change (IPCC;

      IPCC. 2019. Climate Change and Land 2019. An IPCC Special Report on Climate Change, Desertification, Land Degradation, Sustainable Land Management, Food Security, and Greenhouse Gas Fluxes in Terrestrial Ecosystems. Accepted Draft. Intergov. Panel Climate Change, Geneva, Switzerland.

      ) report estimated that 23% of global anthropogenic greenhouse gas (GHG) emissions were from agriculture, forestry, and other land uses. These sources contribute an estimated 44% of all methane (CH4) emissions (4.5 ± 1.4 Gt of CO2 equivalents∙y−1), with enteric CH4 from ruminants responsible for 46%, of the 4.5 ± 1.4 Gt of CO2 equivalents∙y−1 or 2.1 Gt of CO2 equivalents∙y−1 (

      IPCC. 2019. Climate Change and Land 2019. An IPCC Special Report on Climate Change, Desertification, Land Degradation, Sustainable Land Management, Food Security, and Greenhouse Gas Fluxes in Terrestrial Ecosystems. Accepted Draft. Intergov. Panel Climate Change, Geneva, Switzerland.

      ;

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). Anthropogenic GHG have been increasing since the start of the industrial revolution and will continue to grow with increased fossil fuel (e.g., coal, gas, and oil) combustion (
      • Place S.E.
      • Mitloehner F.M.
      Invited review: Contemporary environmental issues: A review of the dairy industry’s role in climate change and air quality and the potential of mitigation through improved production efficiency..
      ).
      In the United States, the agriculture sector contributes about 9% of total GHG emissions, whereas the transportation, industry, and electricity sectors produce the majority of emissions (about 79% of total;

      EPA. 2019. Inventory of U. S. Greenhouse Gas Emissions and Sinks: 1990–2014. EPA 430-R-19-001. Environ. Prot. Agency, Washington, DC.

      ). The Paris Climate Accord funded a special IPCC climate report in 2018 that recommended that developed countries should reach zero-emission targets in an “as soon as possible” window and reduce global emissions by 45% by 2030. Thus, although the United States agriculture emission footprint is considerably less compared with other US sectors and the world, the zero-emission target implies mitigation from all sectors barring marked improvement in carbon (C) sequestration technologies (

      Rogeli, J., D. Shindell, K. Jiang, S. Fifita, P. Forster, V. Ginzburg, C. Handa, H. Kheshgi, S. Kobayashi, E. Kriegler, L. Mundaca, R. Séférian, and M. V. Vilariño. 2018. Mitigation pathways compatible with 1.5°C in the context of sustainable development. In Global Warming of 1.5°C. An IPCC Special Report on the Impacts of Global Warming of 1.5°C Above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty. V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P. R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield, ed. World Meteorol. Org., Geneva, Switzerland.

      ). Of the 9.1% attributed to US agriculture production, about 60% is due to animal agriculture, and about 60% of that is attributed to biogenic enteric CH4 emissions from all domesticated ruminants (3.2% of total US emissions;

      EPA. 2019. Inventory of U. S. Greenhouse Gas Emissions and Sinks: 1990–2014. EPA 430-R-19-001. Environ. Prot. Agency, Washington, DC.

      ). Methane is a potent GHG with a global warming potential (GWP) 28 times that of CO2 (

      IPCC. 2014. Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. O. Edenhofer, R. Pichs-Madruga, Y. Sokona, E. Farahani, S. Kadner, K. Seyboth, A. Adler, I. Baum, S. Brunner, P. Eickemeier, B. Kriemann, J. Savolainen, S. Schlömer, C. von Stechow, T. Zwickel and J. C. Minx, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). Agriculture contributes about 37.8% of domestic CH4 emissions from the combined sources of enteric, manure management rice cultivation and field residue burning, with enteric CH4 emissions being the largest agricultural source at 27% of US CH4 emissions (

      EPA. 2019. Inventory of U. S. Greenhouse Gas Emissions and Sinks: 1990–2014. EPA 430-R-19-001. Environ. Prot. Agency, Washington, DC.

      ). Because of methane’s contribution to the overall agriculture emission footprint, addressing mitigation opportunities is essential to reach reduced emission targets.
      Recent life-cycle assessments have highlighted the need to focus on the grazing sectors of the US beef industry, with the cow-calf and stocker cattle components contributing approximately 70 to 80% of total GHG from the US beef sector (
      • Rotz C.A.
      • Asem-Hiablie S.
      • Dillon J.
      • Bonifacio H.
      Cradle-to-farm gate environmental footprints of beef cattle production in Kansas, Oklahoma, and Texas..
      ,
      • Rotz C.A.
      • Asem-Hiablie S.
      • Place S.E.
      • Thoma G.
      Environmental footprints of beef cattle production in the United States..
      ;
      • Alemu A.W.
      • Janzen H.
      • Little S.
      • Hao X.
      • Thompson D.J.
      • Baron V.
      • Iwaasa A.
      • Beauchemin K.A.
      • Kröbel R.
      Assessment of grazing management on farm greenhouse gas intensity of beef production systems in the Canadian Prairies using life cycle assessment..
      ). The reason for this is 2-fold. First, cattle consuming a high-forage diet have increased CH4 emissions, and second, breeding stock live on the land continuously and produce one calf per year (
      • Rotz C.A.
      • Asem-Hiablie S.
      • Dillon J.
      • Bonifacio H.
      Cradle-to-farm gate environmental footprints of beef cattle production in Kansas, Oklahoma, and Texas..
      ). To date there have been several reviews detailing the effects of nutrition on enteric CH4 production and mitigation options (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ;
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review..
      ;
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). Considering the contribution of the grazing sector to enteric CH4 emissions, the primary objectives of this review were to focus on mitigation strategies from a grazing perspective and to explore how soil–plant–animal interrelationships can be manipulated and enhanced to reduce CH4 emissions and improve ecosystem functioning and overall system sustainability.

      SOURCES OF METHANE EMISSIONS

      Enteric Methanogenesis

      Enteric CH4 is a natural by-product of the anaerobic fermentation process in the reticulo-rumen and hindgut in ruminants (
      • Patra A.K.
      Enteric methane mitigation technologies for ruminant livestock: A synthesis of current research and future directions..
      ; Figure 1). The rumen is an anaerobic environment where large numbers of symbiotic bacteria, protozoa, and fungi derive their energy from consumed feedstuffs. The digestion end products of their digestion are primarily microbial cell protein and VFA (primarily acetate, butyrate, and propionate) that the host animal uses to meet its own metabolic needs (
      • Krehbiel C.R.
      Invited Review: Applied nutrition of ruminants: Fermentation and digestive physiology..
      ). This symbiotic relationship allowed ruminants to evolve across a multitude of biomes to fill an ecological niche using complex carbohydrates, chiefly cellulose, that most mammalian species cannot digest (
      • Knapp J.R.
      • Laur G.L.
      • Vadas P.A.
      • Weiss W.P.
      • Tricarico J.M.
      Invited review: Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions..
      ). This evolution led to the rise of a complex microbial community that include methanogenic species that differ from methanogens in other populations because it lacks cytochrome proteins responsible for electron transfer (
      • Knapp J.R.
      • Laur G.L.
      • Vadas P.A.
      • Weiss W.P.
      • Tricarico J.M.
      Invited review: Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions..
      ;
      • Muñoz-Tamayo R.
      • Popova M.
      • Tillier M.
      • Morgavi D.P.
      • Morel J.P.
      • Fonty G.
      • Morel-Desrosiers N.
      Hydrogenotrophic methanogens of the mammalian gut: Functionally similar, thermodynamically different—A modelling approach..
      ). In most ecosystems this would be an energetic disadvantage, but instead, it allows the methanogens to survive in the reticulo-ruminal environment (
      • Muñoz-Tamayo R.
      • Popova M.
      • Tillier M.
      • Morgavi D.P.
      • Morel J.P.
      • Fonty G.
      • Morel-Desrosiers N.
      Hydrogenotrophic methanogens of the mammalian gut: Functionally similar, thermodynamically different—A modelling approach..
      ). In addition to the VFA and protein produced during the fermentation process, gaseous CO2 and H2 are produced. These serve as the primary substrates for methanogenic archaea to produce CH4, typically through the hydrogenotrophic pathway (
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming..
      ):
      CO2+4H2CH4+2H2O.
      [1]


      Figure 1
      Figure 1Methane in the carbon cycle. GWP = global warming potential; GHG = greenhouse gas.
      This process of cellular respiration by methanogens uses the H2 to produce CH4 and H2O, thereby preventing metabolic hydrogen from accumulating in the reticulo-rumen. Hydrogen removal is crucial for healthy ruminal fermentation as accumulation limits the ability of microbial populations to oxidize the cofactors responsible for electron transfer, thereby reducing carbohydrate degradation, microbial growth rate, and synthesis of microbial cell protein (
      • Wolin M.J.
      Metabolic interactions among intestinal microorganisms..
      ;
      • McAllister T.A.
      • Newbold C.J.
      Redirecting rumen fermentation to reduce methanogenesis..
      ;
      • Beauchemin K.A.
      • McAllister T.A.
      • McGinn S.M.
      Dietary mitigation of enteric methane from cattle..
      ).
      Enteric CH4 production is driven primarily by level of feed intake and dietary fiber concentrations (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). Methane production increases with greater intake due to effects on ruminal passage rate and carbohydrate fermentation (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ). The form of carbohydrate also influences CH4 production (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). Feeding cattle a high-concentrate diet compared with a diet high in cell wall fiber results in less dietary energy lost as CH4 through effects on ruminal pH, shifting microbial populations, and a decrease in the acetate:propionate ratio (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ). The production of acetate is greatest in cattle fed high-fiber diets, and its production increases CH4 production by increasing the amount of metabolic H2, whereas propionate acts as a hydrogen sink:
      C6H12O6+2H2O2C2H4O2+2CO2+8Hacetate,
      [2]


      C6H12O6+4H2C3H6O2+2H2Opropionate.
      [3]


      Numerous other factors including forage processing and quality, lipid content, forage secondary compounds, and dietary additives also alter CH4 production. Due to the myriad of factors influencing enteric CH4 production, energy losses in the form of CH4 can range from 2 to 12% of GE intake (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ). Therefore, when including its effects on global climate change, taking strides to mitigate CH4 production is both economically and environmentally beneficial. Figure 1 displays the role of enteric CH4 in the biogenic C cycle. Carbon dioxide is fixed in plants via photosynthesis, and this C is then converted into CH4 after consumption of plant material by ruminants and expelled out of the mouth of the animal. This CH4 has a residence time of about 9 to 12 yr in the atmosphere before being broken back down into CO2.

      Regional Emissions

      An inherent complexity when discussing global emission mitigation is the regional specificity of emissions and the societal cost–benefit relationship at the more localized level. Therefore, it is important to compare regional emission rates to determine where improvement is needed and why some regions favor lower CH4 intensity (CH4 per unit of product, typically kg of carcass weight in beef cattle) compared with others. Globally, 2.8 Gt of enteric CH4 GHG are annually produced, with cattle being responsible for 77% of the total (

      FAO. 2013. Tackling Climate Change Through Livestock: A Global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations, Rome, Italy.

      ). However, the emission rate is not equal across countries, with developing countries contributing as much as 75% of total global GHG emissions from ruminants (
      • Herrero M.
      • Havlik P.
      • Valin H.
      • Notenbaert A.
      • Rufino M.C.
      • Thornton P.K.
      • Blummel M.
      • Weiss F.
      • Grace D.
      • Obersteiner M.
      Biomass use, production, feed efficiencies, and greenhouse gas emissions from global livestock systems..
      ). In terms of CH4 emission intensity (kg of CO2 equivalents/kg of carcass weight), sub-Saharan Africa and southern Asia have the greatest with 41 and 50 kg of CO2 equivalents/kg of carcass weight (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ). The developed regions of western and eastern Europe range from 5 to 7 kg of CO2 equivalents/kg of carcass weight (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ). North America and Oceania are estimated to have an emission intensity of 11, whereas the emission intensity of Latin America is about 24 (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ). In developing countries, greater CH4 emission intensities are driven by poor feed digestibility, low slaughter weights, greater age at slaughter, and poor animal husbandry (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ;
      • Herrero M.
      • Havlik P.
      • Valin H.
      • Notenbaert A.
      • Rufino M.C.
      • Thornton P.K.
      • Blummel M.
      • Weiss F.
      • Grace D.
      • Obersteiner M.
      Biomass use, production, feed efficiencies, and greenhouse gas emissions from global livestock systems..
      ). In developed countries, emission rates are low due to improved grazing management leading to greater diet digestibility, more intensive feeding practices, and temperate conditions (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ;
      • Herrero M.
      • Havlik P.
      • Valin H.
      • Notenbaert A.
      • Rufino M.C.
      • Thornton P.K.
      • Blummel M.
      • Weiss F.
      • Grace D.
      • Obersteiner M.
      Biomass use, production, feed efficiencies, and greenhouse gas emissions from global livestock systems..
      ). All of these result in improved dietary quality throughout the life span of the animal, thereby reducing days on feed and emitting less enteric CH4 emission per unit of feed consumed (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ;
      • Herrero M.
      • Havlik P.
      • Valin H.
      • Notenbaert A.
      • Rufino M.C.
      • Thornton P.K.
      • Blummel M.
      • Weiss F.
      • Grace D.
      • Obersteiner M.
      Biomass use, production, feed efficiencies, and greenhouse gas emissions from global livestock systems..
      ). In addition, European countries mitigate the footprint of their beef sector by producing 80% of their beef from dairy animals (

      Gerber, P. J., H. Steinfeld, B. Henderson, A. Mottet, C. Opio, J. Dijkman, A. Falcucci, and G. Tempio. 2013. Tackling Climate Change Through Livestock—A global Assessment of Emissions and Mitigation Opportunities. Food Agric. Org. United Nations (FAO), Rome, Italy.

      ). Overcoming the economic, political, and educational complexities of developing countries is essential for these regions to reduce their enteric CH4 emissions and improve their C footprint. Beef production in these countries is not focused primarily on food production and nutrient security as in developed countries (
      • Tedeschi L.O.
      • Almeida A.K.D.
      • Atzori A.S.
      • Muir J.P.
      • Fonseca M.A.
      • Cannas A.
      Invited Review: A glimpse of the future in animal nutrition science. 1. Past and future challenges..
      ). In developing countries livestock provide wealth, draft power, fuel, and religious significance, which are not as important in developed countries (
      • Smith J.
      • Sones K.
      • Grace D.
      • MacMillan S.
      • Tarawali S.
      • Herrero M.
      Beyond, milk, meat, and eggs. Role of livestock in food and nutrition security..
      ). It is estimated that livestock production plays a major role in the livelihoods of more than 1 billion people in Africa and Asia and that two-thirds of the livestock managers are women (
      • Smith J.
      • Sones K.
      • Grace D.
      • MacMillan S.
      • Tarawali S.
      • Herrero M.
      Beyond, milk, meat, and eggs. Role of livestock in food and nutrition security..
      ). Mitigation strategies for these countries must balance the improvements in efficiency with the underlying complexities of the local populations and their cultures and not be detrimental to human health and environmental sustainability.

      QUANTIFICATION METHODS

      The gold standard for measuring enteric CH4 production is the respiration chamber and, similarly, the head-box method that quantifies enteric CH4 production by multiplying airflow through the chamber by the difference in CH4 concentration in and out measured by a gas analyzer (
      • Hill J.
      • McSweeney C.
      • Wright A.G.
      • Bishop-Hurley G.
      • Kalantar-zadeh K.
      Review: Measuring methane production from ruminants..
      ). These methods are based on indirect calorimetry and provide very precise and accurate estimates of gas production (
      • Hill J.
      • McSweeney C.
      • Wright A.G.
      • Bishop-Hurley G.
      • Kalantar-zadeh K.
      Review: Measuring methane production from ruminants..
      ). However, restricted movement of animals in the respiration chambers and head-boxes creates an artificial environment that does not reflect a normal production environment and could limit feed intake (
      • Storm I.M.L.D.
      • Hellwing A.L.F.
      • Nielsen N.I.
      • Madsen J.
      Methods for measuring and estimating methane emission from ruminants..
      ). Additionally, an issue in estimating farm-scale emissions is that grazing cattle are selective grazers, forming food preferences over time, which play a critical role in meeting their nutritional needs (
      • Provenza F.D.
      Postingestive feedback as an elementary determinant of food preference and intake in ruminants..
      ). This can result in animals selecting a higher quality diet than the average of the available forage base; this adds uncertainty to applying confinement emission quantification methods to grazing animals. Additionally, the artificial environment created within the chamber can result in lower DMI (
      • Huhtanen P.
      • Ramin M.
      • Hristov A.N.
      Enteric methane emission can be reliably measured by the GreenFeed monitoring unit..
      ). The respiration chamber or head-box was used in the vast majority of studies used to develop emission equations and C accounting. Therefore, there are potential flaws in that these methods may not adequately capture farm-scale emissions when comparing changes in management and environment. In an examination of chamber data,
      • Huhtanen P.
      • Ramin M.
      • Hristov A.N.
      Enteric methane emission can be reliably measured by the GreenFeed monitoring unit..
      found that using these methods underestimated DMI compared with that found in grazing studies and gave lower total enteric CH4 emission estimates. Current methods to quantify enteric CH4 production in grazing environments are the sulfur hexafluoride tracer technique (SF6), the GreenFeed gas quantification system (GEM; C-Lock Inc., Rapid City, SD), various field-level emission quantification methods, and animal models (
      • Hill J.
      • McSweeney C.
      • Wright A.G.
      • Bishop-Hurley G.
      • Kalantar-zadeh K.
      Review: Measuring methane production from ruminants..
      ;
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ).

      Sulfur Hexafluoride Tracer Technique

      The first method to demonstrate repeatable accuracy in quantifying emissions in an open-air environment, such as grazing, and allow for natural forage selection was the SF6 system (

      Zimmerman, P. R. 1993. System for measuring metabolic gas emissions from animals. Univ. Corp. Atmos. Res. US Pat. No. 5, 265,618.

      ;
      • Hill J.
      • McSweeney C.
      • Wright A.G.
      • Bishop-Hurley G.
      • Kalantar-zadeh K.
      Review: Measuring methane production from ruminants..
      ;
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ). This method uses SF6 as a tracer gas based on the assumption that the standard SF6 emission rate is equal to the CH4 emission rate (
      • Johnson K.
      • Huyler M.
      • Westberg H.
      • Lamb B.
      • Zimmerman P.
      Measurement of methane emissions from ruminant livestock using a sulfur hexafluoride tracer technique..
      ). Before the beginning of the experiment, the release rate of the SF6 bolus is estimated in vitro before the bolus is placed into the rumen (

      Zimmerman, P. R. 1993. System for measuring metabolic gas emissions from animals. Univ. Corp. Atmos. Res. US Pat. No. 5, 265,618.

      ). A halter with a stainless steel collection vessel and a capillary tube attached to a collection canister is then placed around the animal’s head to collect respired air from the animal (

      Zimmerman, P. R. 1993. System for measuring metabolic gas emissions from animals. Univ. Corp. Atmos. Res. US Pat. No. 5, 265,618.

      ;
      • Johnson K.
      • Huyler M.
      • Westberg H.
      • Lamb B.
      • Zimmerman P.
      Measurement of methane emissions from ruminant livestock using a sulfur hexafluoride tracer technique..
      ). The enteric CH4 emission rate can then be determined by gas chromatography using the ratio of CH4:SF6 multiplied by the standard SF6 release rate and corrected for background SF6 concentration (
      • Johnson K.
      • Huyler M.
      • Westberg H.
      • Lamb B.
      • Zimmerman P.
      Measurement of methane emissions from ruminant livestock using a sulfur hexafluoride tracer technique..
      ). This method initially was revolutionary because it allowed researchers to quantify emissions from free-grazing animals (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ). However, later research literature showed that the difference between SF6 and respiration chambers may be >10% at times (
      • Storm I.M.L.D.
      • Hellwing A.L.F.
      • Nielsen N.I.
      • Madsen J.
      Methods for measuring and estimating methane emission from ruminants..
      ). The limitations of the SF6 method may explain these, at times unacceptable, error rates including the curvilinear release rate of the standard SF6 gas from the intraruminal bolus over time, labor, and the inability to collect emissions from the hindgut (

      Vlaming, J. B. 2007. Quantifying variation in estimated methane emission from ruminants using the SF6 tracer technique. PhD Thesis. Animal Sci., Massey Univ., Palmerton North, New Zealand.

      ;
      • Storm I.M.L.D.
      • Hellwing A.L.F.
      • Nielsen N.I.
      • Madsen J.
      Methods for measuring and estimating methane emission from ruminants..
      ). The method relies on a presumably continuous and constant release rate of SF6 from the permeation tubes. Yet measured pre- and post-experiment release rates of SF6 from permeation tubes displayed a curvilinear release rate in the laboratory (

      Vlaming, J. B. 2007. Quantifying variation in estimated methane emission from ruminants using the SF6 tracer technique. PhD Thesis. Animal Sci., Massey Univ., Palmerton North, New Zealand.

      ;
      • Storm I.M.L.D.
      • Hellwing A.L.F.
      • Nielsen N.I.
      • Madsen J.
      Methods for measuring and estimating methane emission from ruminants..
      ). This could result in a decrease in release rate of 6 to 11% while in the rumen (

      Vlaming, J. B. 2007. Quantifying variation in estimated methane emission from ruminants using the SF6 tracer technique. PhD Thesis. Animal Sci., Massey Univ., Palmerton North, New Zealand.

      ). Therefore, studies that use permeation tubes of differing release rates within an experiment may have in inaccurate CH4 emission estimates (

      Vlaming, J. B. 2007. Quantifying variation in estimated methane emission from ruminants using the SF6 tracer technique. PhD Thesis. Animal Sci., Massey Univ., Palmerton North, New Zealand.

      ;
      • Pinares-Patiño C.S.
      • Machmuller A.
      • Molano G.
      • Smith A.
      • Vlaming J.B.
      • Clark H.
      The SF6tracer technique for measurements of methane emission from cattle—Effect of tracer permeation rate..
      ). Additionally, hindgut CH4 emissions that are not absorbed into the blood stream and respired out of the lungs may account for 1 to 11% of CH4 emissions (
      • McGinn S.M.
      • Beauchemin K.A.
      • Iwaasa A.D.
      • McAllister T.A.
      Assessment of the sulfur hexafluoride (SF6) tracer technique for measuring enteric methane emissions from cattle..
      ). Last, the use of SF6 is paradoxical as it is a potent GHG with a GWP of 22,800 (

      Vlaming, J. B. 2007. Quantifying variation in estimated methane emission from ruminants using the SF6 tracer technique. PhD Thesis. Animal Sci., Massey Univ., Palmerton North, New Zealand.

      ).

      GreenFeed Emission Measurement System

      Based on the previously outlined limitations of the SF6 system, the GEM system was developed by using spot measurements to estimate enteric CH4 production (
      • Hristov A.N.
      • Oh J.
      • Giallongo F.
      • Frederick T.
      • Weeks H.
      • Zimmerman P.R.
      • Harper M.T.
      • Hristova R.A.
      • Zimmerman R.S.
      • Branco A.F.
      The use of an automated system (GreenFeed) to monitor enteric methane and carbon dioxide emissions from ruminant animals..
      ;
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ). Similar to SF6, this method is able to estimate CH4 emissions from free-grazing animals but is less intrusive and relies on spot measurements to estimate daily production (
      • Hristov A.N.
      • Oh J.
      • Giallongo F.
      • Frederick T.
      • Weeks H.
      • Zimmerman P.R.
      • Harper M.T.
      • Hristova R.A.
      • Zimmerman R.S.
      • Branco A.F.
      The use of an automated system (GreenFeed) to monitor enteric methane and carbon dioxide emissions from ruminant animals..
      ). The GEM system uses a portable head-box either in a freestall or on a trailer that uses bait feed to entice animals to place their head in the head-box (
      • Hristov A.N.
      • Oh J.
      • Giallongo F.
      • Frederick T.
      • Weeks H.
      • Zimmerman P.R.
      • Harper M.T.
      • Hristova R.A.
      • Zimmerman R.S.
      • Branco A.F.
      The use of an automated system (GreenFeed) to monitor enteric methane and carbon dioxide emissions from ruminant animals..
      ). When an animal places its head in the hood, the volume of air that is drawn from around the animal’s head and shoulders is measured, and a subsample is analyzed by nondispersive near infrared gas analyzers for CO2 and CH4 concentrations (
      • Hristov A.N.
      • Oh J.
      • Giallongo F.
      • Frederick T.
      • Weeks H.
      • Zimmerman P.R.
      • Harper M.T.
      • Hristova R.A.
      • Zimmerman R.S.
      • Branco A.F.
      The use of an automated system (GreenFeed) to monitor enteric methane and carbon dioxide emissions from ruminant animals..
      ). These results are then compared with background gas concentrations from before the animal entered the hood to determine gas emission rates. Spot estimates are then averaged over the course of the sampling period to estimate each animal’s daily gas production (
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ). Previous research indicates the GEM can result in highly variable data sets due to greater within-day and within-animal variability that is more difficult to capture with a spot measurement system (
      • Hammond K.J.
      • Crompton L.A.
      • Bannink A.
      • Dijkstra J.
      • Yáñez-Ruiz D.R.
      • O’Kiely P.
      • Kebreab E.
      • Eugène M.A.
      • Yu Z.
      • Shingield K.J.
      • Schwarm A.
      • Hristov A.N.
      • Reynolds C.K.
      Review of current in vivo measurement techniques for quantifying enteric methane emissions from ruminants..
      ). However, the system proved to be sufficiently accurate with adequate number of visits over an extended period of time (
      • Cottle D.J.
      • Velazco J.
      • Hegarty R.S.
      • Mayer D.G.
      Estimating daily methane production in individual cattle with irregular feed intake patterns from short-term methane emission measurements..
      ). In a power analysis of cattle visiting a GEM,
      • Gunter S.A.
      • Bradford J.A.
      Technical Note: Effect of bait delivery interval in an automated head-chamber system on respiration gas estimates when cattle are grazing rangeland..
      found that accurate daily estimates can be obtained if animals visit the unit an average of 2.4 times per day for 4.8 to 6.3 d.
      • Hammond K.J.
      • Humphries D.J.
      • Crompton L.A.
      • Green C.
      • Reynolds C.K.
      Methane emissions from cattle: Estimates from short-term measurements using a GreenFeed system compared with measurements obtained using respiration chambers or sulphur hexafluoride tracer..
      reported that GEM in a grazing experiment was not able to capture treatment differences that were evident in respiration chambers using 4-d sampling periods with an average of 1.6 visits per day. However, recent studies on the duration of sampling and number of adequate visits may explain these differences as more visits may be required to detect treatment differences during short sampling periods (
      • Hammond K.J.
      • Humphries D.J.
      • Crompton L.A.
      • Green C.
      • Reynolds C.K.
      Methane emissions from cattle: Estimates from short-term measurements using a GreenFeed system compared with measurements obtained using respiration chambers or sulphur hexafluoride tracer..
      ;
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ). Additionally, these studies focused on meal-fed cattle, which have a larger diurnal variation than grazing animals, which emphasizes the importance of the timing of visits to the head-box (
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ). Last, because this system is less expensive than chamber methods and requires less labor than the SF6 method, larger samples sizes (more experimental replicates) are possible compared with other sampling techniques, which aids in efforts to minimize experimental and sampling errors (
      • Gunter S.A.
      • Bradford J.A.
      Influence of sampling time of carbon dioxide and methane emissions by grazing cattle..
      ).

      Portable Accumulation Chambers

      Another system that relies on spot sampling, the portable accumulation chamber (PAC), has been used to estimate CH4 production (
      • Goopy J.P.
      • Woodgate R.
      • Donaldson A.
      • Robinson D.L.
      • Hegarty R.S.
      Validation of a short-term methane measurement using portable static chambers to estimate daily methane production in sheep..
      ). This method has typically been used with grazing sheep and has shown moderately high correlations with the respiration chamber method (r = 0.71); it can also identify relative emission changes without scaling up to daily CH4 production (DMP) estimates (
      • Goopy J.P.
      • Woodgate R.
      • Donaldson A.
      • Robinson D.L.
      • Hegarty R.S.
      Validation of a short-term methane measurement using portable static chambers to estimate daily methane production in sheep..
      ;
      • Hegarty R.S.
      Applicability of short-term emission measurements for on-farm quantification of enteric methane..
      ). These chambers are boxes that are open at the bottom and clear sided, and they seal at the bottom with high-density foam rubber. The chambers have 3 sampling ports located on the superior, posterior, and lateral walls, and the chamber is placed on industrial-grade rubber (
      • Goopy J.P.
      • Woodgate R.
      • Donaldson A.
      • Robinson D.L.
      • Hegarty R.S.
      Validation of a short-term methane measurement using portable static chambers to estimate daily methane production in sheep..
      ,
      • Goopy J.P.
      • Robinson D.L.
      • Woodgate R.T.
      • Donaldson A.J.
      • Oddy V.H.
      • Vercoe P.E.
      • Hegarty R.S.
      Estimates of repeatability and heritability of methane production in sheep using portable accumulation chambers..
      ). Animals are positioned on top of the rubber bottom, and the box is lowered down and sealed. Sampling durations last from 1 to 2 h (
      • Hammond K.J.
      • Crompton L.A.
      • Bannink A.
      • Dijkstra J.
      • Yáñez-Ruiz D.R.
      • O’Kiely P.
      • Kebreab E.
      • Eugène M.A.
      • Yu Z.
      • Shingield K.J.
      • Schwarm A.
      • Hristov A.N.
      • Reynolds C.K.
      Review of current in vivo measurement techniques for quantifying enteric methane emissions from ruminants..
      ). Studies comparing PAC to respiration chambers have found moderate correlations at both 1- and 2-h sampling durations (
      • Goopy J.P.
      • Woodgate R.
      • Donaldson A.
      • Robinson D.L.
      • Hegarty R.S.
      Validation of a short-term methane measurement using portable static chambers to estimate daily methane production in sheep..
      ;
      • Robinson D.L.
      • Goopy J.P.
      • Hegarty R.S.
      • Oddy V.H.
      Comparison of repeated measurements of methane production in sheep over 5 years and a range of measurement protocols..
      ;
      • Goopy J.P.
      • Robinson D.L.
      • Woodgate R.T.
      • Donaldson A.J.
      • Oddy V.H.
      • Vercoe P.E.
      • Hegarty R.S.
      Estimates of repeatability and heritability of methane production in sheep using portable accumulation chambers..
      ;
      • Robinson D.L.
      • Cameron M.
      • Donaldson A.J.
      • Dominik S.
      • Oddy V.H.
      One-hour portable chamber methane measurements are repeatable and provide useful information on feed intake and efficiency..
      ).
      • Goopy J.P.
      • Woodgate R.
      • Donaldson A.
      • Robinson D.L.
      • Hegarty R.S.
      Validation of a short-term methane measurement using portable static chambers to estimate daily methane production in sheep..
      , in a study comparing respiration chambers with PAC using sheep, found R2 = 0.42 to 0.48 for 2-h sampling periods and 0.39 to 0.43 in 1-h sampling periods. Measuring ewes for 40 to 60 min,
      • Robinson D.L.
      • Cameron M.
      • Donaldson A.J.
      • Dominik S.
      • Oddy V.H.
      One-hour portable chamber methane measurements are repeatable and provide useful information on feed intake and efficiency..
      determined that these estimates had a repeatability of about 0.47 once adjusted for BW and ADG but did not alter the animal’s intake as respiration chambers do. Researchers using the PAC method have noted that repeatability can be affected by time of sampling and feeding schedules, which can cause issues with repeatability by altering the diurnal pattern of DMP (
      • Hammond K.J.
      • Crompton L.A.
      • Bannink A.
      • Dijkstra J.
      • Yáñez-Ruiz D.R.
      • O’Kiely P.
      • Kebreab E.
      • Eugène M.A.
      • Yu Z.
      • Shingield K.J.
      • Schwarm A.
      • Hristov A.N.
      • Reynolds C.K.
      Review of current in vivo measurement techniques for quantifying enteric methane emissions from ruminants..
      ). This causes issues when scaling up to estimate DMP, which is less of an issue when using the GEM because spot samples are obtained throughout the day if the animals use the head-box (
      • Hammond K.J.
      • Crompton L.A.
      • Bannink A.
      • Dijkstra J.
      • Yáñez-Ruiz D.R.
      • O’Kiely P.
      • Kebreab E.
      • Eugène M.A.
      • Yu Z.
      • Shingield K.J.
      • Schwarm A.
      • Hristov A.N.
      • Reynolds C.K.
      Review of current in vivo measurement techniques for quantifying enteric methane emissions from ruminants..
      ;
      • Gunter S.A.
      • Beck M.R.
      Measuring the respiratory gas exchange by grazing cattle using an automated, open-circuit gas quantification system..
      ).

      Micrometeorological Techniques

      On the field level, micrometeorological techniques including flux-gradient, eddy covariance, and inverse dispersion models are being developed to provide herd-scale emission estimates (
      • Harper L.A.
      • Denmead O.T.
      • Flesch T.K.
      Micrometeorological techniques for measurement of enteric greenhouse gas emissions..
      ;
      • Storm I.M.L.D.
      • Hellwing A.L.F.
      • Nielsen N.I.
      • Madsen J.
      Methods for measuring and estimating methane emission from ruminants..
      ;
      • McGinn S.M.
      Developments in micrometeorological methods for methane measurements..
      ;
      • Hill J.
      • McSweeney C.
      • Wright A.G.
      • Bishop-Hurley G.
      • Kalantar-zadeh K.
      Review: Measuring methane production from ruminants..
      ). These methods measure atmospheric CH4 concentrations and meteorological variables to estimate herd-level, animal-group, or farm-level emission rates. Measuring emissions on a farm scale allows researchers to have a better understanding of how mitigation strategies are affecting the operation and to test strategies on a large number of animals (
      • Harper L.A.
      • Denmead O.T.
      • Flesch T.K.
      Micrometeorological techniques for measurement of enteric greenhouse gas emissions..
      ;
      • McGinn S.M.
      • Flesch T.K.
      • Beauchemin K.A.
      • Shreck A.
      • Kindermann M.
      Micrometeorological methods for measuring methane emission reduction at beef cattle feedlots: Evaluation of 3-nitrooxypropanol feed additive..
      ). These methods have an advantage over individual animal sampling techniques because they do not require animal handling or bait feeding, which may alter animal behavior and diet selection, and allow for long-term comparison between management strategies (
      • Harper L.A.
      • Denmead O.T.
      • Flesch T.K.
      Micrometeorological techniques for measurement of enteric greenhouse gas emissions..
      ;
      • Coates T.W.
      • Benvenutti M.A.
      • Flesch T.K.
      • Charmley E.
      • McGinn S.M.
      • Chen D.
      Applicability of eddy covariance to estimate methane emissions from grazing cattle..
      ). However, spatial variability and low intensity of emissions from grazing animals have limited the adoption of these methods beyond feedlot and confinement operations and may require animals to be grazed at high densities to estimate emissions (
      • Dengel S.
      • Levy P.E.
      • Grace J.
      • Jones S.K.
      • Skiba U.M.
      Methane emissions from sheep pasture, measured with an open-path eddy covariance system..
      ;
      • Flesch T.K.
      • Basarab J.A.
      • Baron V.S.
      • Wilson J.D.
      • Hu N.
      • Tomkins N.W.
      • Ohama A.J.
      Methane emissions from cattle grazing under diverse conditions: An examination of field configurations appropriate for line-averaging sensors..
      ). There are numerous different micrometeorological methods each having its own set of advantages and disadvantages and proper field configurations, which are outside the scope of this review but have been reviewed in depth by
      • McGinn S.M.
      Developments in micrometeorological methods for methane measurements..
      ,
      • Flesch T.K.
      • Basarab J.A.
      • Baron V.S.
      • Wilson J.D.
      • Hu N.
      • Tomkins N.W.
      • Ohama A.J.
      Methane emissions from cattle grazing under diverse conditions: An examination of field configurations appropriate for line-averaging sensors..
      , and
      • Harper L.A.
      • Denmead O.T.
      • Flesch T.K.
      Micrometeorological techniques for measurement of enteric greenhouse gas emissions..
      .

      MITIGATION OF METHANE IN GRAZING ENVIRONMENTS

      Methane production in grazing environments is a combination of many different factors that interact to influence individual animal intake, performance, and emission rates. Dietary quality (e.g., digestibility) plays an important role in the production of CH4 (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ;
      • Knapp J.R.
      • Laur G.L.
      • Vadas P.A.
      • Weiss W.P.
      • Tricarico J.M.
      Invited review: Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions..
      ). Feeding highly fermentable carbohydrates, such as the starch in high-concentrate diets, results in lower enteric CH4 production per unit of feed DM consumed by ultimately shifting microbial populations to favor propionate production and increased ruminal rate of passage (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows..
      ;
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ). However, feeding all cattle only diets high in digestible carbohydrates would reduce the advantage of the ability to convert complex carbohydrates with high fiber content and untillable land into useable end products, chiefly milk or meat (
      • Carvalho P.C.
      • Peterson C.A.
      • Nunes P.A.A.
      • Martins A.P.
      • de Souza Filho W.S.
      • Bertolazi V.T.
      • Kunrath T.R.
      • Moraes A.
      • Anghinoni I.
      Animal production and soil characteristics from integrated crop-livestock systems: Toward sustainable intensification..
      ). Therefore, the question posed to scientists, and ultimately producers, should be how to leverage soil–plant–animal interrelationships to meet productivity goals of the present and future, without compromising social and ecologic outcomes (
      • Tilman D.
      • Balzer C.
      • Hill J.
      • Befort B.L.
      Global food demand and the sustainable intensification of agriculture..
      ).

      Managing the Forage Base

      Forage Quality.

      Proper management of the forage base, the type of forage being grazed, and the stage of forage maturity can affect CH4 emissions and productivity of cattle and can serve to improve or degrade the land base (
      • Teague W.R.
      • Dowhower S.L.
      • Waggoner J.A.
      Drought and grazing patch dynamics under different grazing management..
      ;
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review..
      ). Improving pasture quality can improve dietary digestibility and result in decreased enteric CH4 emissions (
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review..
      ;
      • Archimède H.
      • Eugene M.
      • Magdeleine C.M.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ).
      • Archimède H.
      • Eugene M.
      • Magdeleine C.M.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes..
      conducted a meta-analysis examining CH4 production of C3 and C4 grasses and cold- and warm-season legumes (all legumes use the C3 photosynthetic pathway). Grasses using the C3 photosynthetic pathway are typically considered cool or temperate grasses, and those using the C4 pathway are considered warm or tropical grasses (
      • Archimède H.
      • Eugene M.
      • Magdeleine C.M.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes..
      ). The authors indicated that cattle fed C4 grasses had greater CH4 production than cattle fed C3 grasses and both warm and cold legumes. Cattle fed warm-season legumes produced the least CH4 per kilogram of DMI and per kilogram of OM intake compared with the other diets (
      • Archimède H.
      • Eugene M.
      • Magdeleine C.M.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes..
      ). The results are similar to those of
      • Margan D.E.
      • Graham N.M.
      • Minson D.J.
      • Searle T.W.
      Energy and protein values of four forages including comparison between tropical temperate species..
      , who compared 2 C4 species and a C3 grass and found that C4 grasses produced 23% more CH4 than a C3 grass grown under the same subtropical conditions. These results also align with established literature about CH4 production from forages. Grasses that use the C3 photosynthetic pathway are normally considered higher quality than C4 grasses because they are typically lower in fiber, including decreased lignin production, and greater in protein contents (
      • Barbehenn R.V.
      • Chen Z.
      • Karowe D.N.
      • Spickard A.
      C3 grasses have higher nutritional quality than C4 grasses under ambient and elevated atmospheric CO2..
      ). This results in lower CH4 production values based on the correlation between fiber content of the diet and CH4 production (
      • Blaxter K.L.
      • Wainman F.W.
      The utilization of the energy of different rations by sheep and cattle for maintenance and for fattening..
      ;
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows..
      ). Similarly,
      • McCaughey W.P.
      • Wittenberg K.
      • Corrigan D.
      Impact of pasture type on methane production by lactating beef cows..
      found that first-calf heifers grazing a mixture of alfalfa–meadow bromegrass (Medicago sativa L. and Bromus biebersteinii) lost less energy as CH4 compared with heifers grazing a 100% meadow bromegrass pasture at 7.1 versus 9.5% of gross energy intake (GEI) lost as methane, respectively.
      • Waghorn G.G.
      • Tavendale M.H.
      • Woodfield D.R.
      Methanogenesis from forages fed to sheep..
      examined the CH4 production of young ram lambs fed different forage rations: a mixture of ryegrass–white clover pasture, lucerne, sulla, chicory, red clover, lotus, and mixtures of sulla and lucerne, sulla and chicory, and chicory with red clover. They found that lambs consuming the ryegrass–white clover pasture produced the most CH4 (g/kg of DMI) as compared with the other 10 treatments and reported a 10-fold range in overall CH4 emissions. These results clearly highlight the wide range of emissions that occur even in high-quality forages. However, these studies were all conducted with monoculture or a simple forage mixture. Studies using diverse forage bases resulted in reduced enteric CH4 production, as diverse forage bases allow animals to select plants and plant parts and build their own diet, when animals grazed at lower stocking densities (
      • Provenza F.D.
      Postingestive feedback as an elementary determinant of food preference and intake in ruminants..
      ;
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      ;

      Provenza, F. D., and J. J. Villalba. 2006. Foraging in domestic herbivores: linking the internal and external milieu. Pages 210–240 in Feeding in Domestic Vertebrates: From Structure to Function. V. L. Bels, ed. CABI Publ., Oxfordshire, UK.

      ;
      • Chiavegato M.B.
      • Rowntree J.E.
      • Carmichael D.
      • Powers W.J.
      Enteric methane from lactating beef cows managed with high- and low-input grazing systems..
      ;
      • MacAdam J.W.
      • Villalba J.J.
      Beneficial effects of temperate forage legumes that contain condensed tannins..
      ).
      The quality of a forage diet is not solely determined by the type of forage being offered. Forage maturity affects enteric CH4 production by altering the nutrient density and digestibility of the forage, thereby lowering its quality. As forages mature, fiber content increases and lignin deposition in the cell wall increases as the plants shift from primary cell wall growth to secondary cell wall thickening, resulting in decreased digestibility and intake (
      • Jung H.G.
      • Allen M.S.
      Characteristics of plant cell walls affecting intake and digestibility of forages by ruminants..
      ).
      • Boadi D.A.
      • Wittenberg K.M.
      Methane production from dairy and beef heifers fed forages differing in nutrient density using the sulphur hexafluoride (SF6) tracer gas technique..
      examined 3 different forage diets classified as high quality (legume–grass mixed hay, 61.5% in vitro OM disappearance), medium quality (grass hay, 50.7% in vitro OM disappearance), or low quality (grass hay, 38.5% in vitro OM disappearance) and found that DMI, digestible OM digestibility, and GEI decreased. However, CH4 emissions as a percent of GEI were not affected by stage of maturity, but the reductions in DMI and digestibility resulted in CH4 emissions per unit of digestible OM consumed being highest on the low-quality diet. Similarly,
      • Pinares-Patiño C.S.
      • Baumont R.
      • Martin C.
      Methane emission by Charolais cows grazing a monospecific pasture of timothy at four stages of maturity..
      measured CH4 production of Charolais cows grazing timothy grass monocultures at 4 differing stages of maturity: early vegetative, heading, flowering, and senescence. Organic matter intake was greatest at heading compared with other stages of maturity, but the GEI lost as CH4 was not affected by maturity. The production of CH4 did decrease, however, with increasing fiber digestibility.
      • Muñoz C.
      • Letelier P.A.
      • Ungerfeld E.M.
      • Morales J.M.
      • Hube S.
      • Pérez-Prieto L.A.
      Effects of pregrazing herbage mass in late spring on enteric methane emissions, dry matter intake, and milk production of dairy cows..
      reported that when emissions were reported per unit of milk yield in dairy cows grazing pastures of differing forage quality, the less-mature, higher-quality pasture resulted in a reduction in CH4 emissions. Similarly, in a study comparing low and high stocking rate systems in France with Holstein-Friesian heifers, CH4 emissions per unit of digestible feed intake were decreased with increasing digestibility, and heifers consuming the higher-quality forage in the high stocking rate treatment were heavier at the end of the grazing season (
      • Pinares-Patiño C.S.
      • D’Hour P.
      • Jouany J.P.
      • Martin C.
      Effects of stocking rate on methane and carbon dioxide emissions from grazing cattle..
      ). These studies highlight that when considering the effects of forage quality and maturity on enteric CH4 emissions, production may best be expressed on an intake or animal-production basis rather than GEI lost (
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review..
      ).

      Grazing Management.

      Along with improving pasture quality, grazing management strategies have the potential to decrease CH4 production (
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ;
      • Savian J.V.
      • Schons R.M.T.
      • Marchi D.E.
      • Freitas T.S.D.
      • da Silva Neto G.F.
      • Mezzalira J.C.
      • Berndt A.
      • Bayer C.
      Rotatinuous stocking: A grazing management innovation that has high potential to mitigate methane emissions by sheep..
      ). However, the literature is inconsistent on the short- and long-term effects of different grazing management strategies. Ruminants selectively graze and form food preferences over time, which play a critical role in meeting their nutritional needs (
      • Provenza F.D.
      Postingestive feedback as an elementary determinant of food preference and intake in ruminants..
      ).

      Matches, A. G., and J. C. Burns. 1995. Systems of grazing management. Pages 179–192 in The Science of Grassland Agriculture. R. F. Barnes, D. A. Miller, and C. J. Nelson, ed. Iowa State Univ. Press, Ames.

      and
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      agreed that continuous set stocking allows for maximum diet selection, which results in the capture of short-term gains in animal performance. However, long-term effects on enteric CH4 production between continuous and rotational systems is an area of recurrent inconsistency.
      • Savian J.V.
      • Neto A.B.
      • de David D.B.
      • Bremm C.
      • Schons R.M.T.
      • Genro T.C.M.
      • do Amaral G.A.
      • Gere J.
      • McManus C.M.
      • Bayer C.
      • de Faccio Carvalho P.C.
      Grazing intensity and stocking methods on animal production and methane emission by grazing sheep: Implications for integrated crop-livestock system..
      , in a comparison of continuous versus rotational stocking systems in Brazil, indicated that continuous stocking resulted in lower emission intensity (CH4/kg of ADG) compared with a rotational system. Yet, by refining the rotational system,
      • Savian J.V.
      • Schons R.M.T.
      • Marchi D.E.
      • Freitas T.S.D.
      • da Silva Neto G.F.
      • Mezzalira J.C.
      • Berndt A.
      • Bayer C.
      Rotatinuous stocking: A grazing management innovation that has high potential to mitigate methane emissions by sheep..
      later showed that rotating cattle among paddocks at a target residual forage height of 11 cm resulted in decreased CH4 production compared with that of a traditional rotational system, which had targeted pre- and postgrazing sward heights of 25 and 5 cm, respectively.
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      determined that when incorporating a rotational system consisting of best management practices, with periodical fertilization and animals being rotated frequently, annual enteric CH4 production was reduced by 22% compared with a continuous stocking system. Conversely,
      • McCaughey W.P.
      • Wittenberg K.
      • Corrigan D.
      Methane production by steers on pasture..
      compared enteric CH4 production and voluntary intake of steers grazing in 1 of 2 grazing systems: continuous or 10-paddock rotational stocking system with animals moved based on forage availability, at 2 stocking rates: 1.1 or 2.2 steer/ha. They found that neither voluntary intake nor CH4 production were affected by management system.
      Considering that sustainability is a multipronged goal, perhaps the benefits of a grazing management system occur beyond short-term animal performance. One hypothesis suggests that the variable results in enteric CH4 production in different systems are the result of animals in the studies being able to select high-quality diets within the treatments and perform well. However, some literature argues that the effects of management are more crucial to the long-term performance of the supporting environment. One suggestion is that the use of continuous stocking results in imbalanced patch grazing pressure, which can result in overgrazing of preferred forages and ecosystem process impairment (short- or long-term damage to normal ecosystem function). This leads to a reduction in plant diversity, increases the proportion of undesirable or low-quality forages, and ultimately leads to soil erosion (
      • Teague W.R.
      • Dowhower S.L.
      • Waggoner J.A.
      Drought and grazing patch dynamics under different grazing management..
      ;
      • Teague W.R.
      • Apfelbaum S.
      • Lal R.
      • Kreuter U.P.
      • Rowntree J.
      • Davies C.A.
      • Conser R.
      • Rasmussen M.
      • Hatfield J.
      • Wang T.
      • Wang F.
      • Byck P.
      The role of ruminants in reducing agriculture’s carbon footprint in North America..
      ). Additionally, the loss of high-quality forages from overgrazing will result in a lower amount of solar energy captured and, thus, reduce the amount of solar energy converted to forage and then to useable end products (e.g., meat and milk).

      Forage Secondary Compounds.

      Grazing ecosystems are complex and affect emissions through other mechanisms beyond intake and forage quality. In grazing lands containing a forage base of differing forages at different stages of growth, cattle may capture synergies due to primary and secondary compounds present in the plants resulting in improved performance (
      • Provenza F.D.
      • Villalba J.J.
      • Dziba L.E.
      • Atwood S.B.
      • Banner R.E.
      Linking herbivore experience, varied diets, and plant biochemical diversity..
      ;
      • Villalba J.J.
      • Provenza F.D.
      • Manteca X.
      Links between ruminants’ food preference and their welfare..
      ). Plant secondary compounds or metabolites consist of a broad spectrum of compounds including flavonoids, tannins, pectins, glycosides, terpenoids, and sesquiterpene lactones, just to name a few. With a wide range of compounds comes a wide range of ecological functions performed by the compounds, but the compounds of interest from a grazing perspective are those that act as a defense against herbivory (the consumption of plants by animals;
      • Iason G.
      The role of plant secondary metabolites in mammalian herbivory: Ecological perspectives..
      ). Some of these defense compounds can be toxic to the animal or act as a deterrent through taste, and animals learn either by experience or animal-to-animal learning which plants to consume and how to minimize the effects of toxic compounds (
      • Provenza F.D.
      Postingestive feedback as an elementary determinant of food preference and intake in ruminants..
      ). However, some of these compounds have shown promise to improve animal productivity and health and mitigate enteric CH4 production. Compounds of interest are saponins, condensed tannins, and essential oils (
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ).
      • Lagrange S.
      • Beauchemin K.A.
      • MacAdam J.W.
      • Villalba J.J.
      Effects of grazing diverse combinations of sainfoin, birdsfoot trefoil, and alfalfa on beef cow performance and environmental impacts..
      found that grazing cattle on diverse pastures containing different legumes has divergent effects on CH4 production, potentially due to differences in secondary compounds. They noted that cattle grazing a diverse pasture with saponin-containing alfalfa had greater CH4 emissions per unit of BW gain than cattle on pastures with tannin-containing sainfoin or tannin-containing birdsfoot trefoil, as well as improved animal performance. In a study feeding alfalfa hay or sainfoin hay, beef heifers produced less CH4 on an OM basis when fed the tannin-containing sainfoin hay (
      • Chung Y.H.
      • McGeough E.J.
      • Acharya S.
      • McAllister T.A.
      • McGinn S.M.
      • Harstad O.M.
      • Beauchemin K.A.
      Enteric methane emission, diet digestibility, and nitrogen excretion from beef heifers fed sainfoin or alfalfa..
      ). Similarly,
      • Grainger C.
      • Williams R.
      • Clarke T.
      • Wright A.D.G.
      • Eckard R.J.
      Supplementation with whole cotton seed causes long-term reduction of methane emissions from lactating dairy cows offered a forage and cereal grain diet..
      found that dairy cows grazing ryegrass supplemented with 163 or 326 g/d of condensed tannins had reduced enteric CH4 emissions, although the condensed tannins also caused a corresponding decrease in milk yield and intake. Tannins are able to reduce enteric CH4 because of its affinity to bind protein and carbohydrates in the rumen, which decreases ruminal fiber digestion. However, its inclusion at high dietary concentrations can decrease voluntary feed intake.
      • Min B.R.
      • Barry T.N.
      • Attwood G.T.
      • McNabb W.C.
      The effect of condensed tannins on the nutrition and health of ruminants fed fresh temperate forages: A review..
      suggested that tannins affect rumen protein degradation when consumed at 20 to 45 g of condensed tannins/kg of DM, and >55 g/kg of DM can inhibit voluntary feed intake and forage digestibility. Tannins also may serve to improve animal performance through bloat control and providing some antiparasitic properties (
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). However, tannin research is difficult and inconsistent due to difficulties in isolating tannins and because different forages may contain different structural forms of tannins.

      Mitigation Strategies Directed Toward Animals

      Mitigating enteric CH4 emissions by acting directly on the animal and not the forage base is problematic in grazing environments partially due to the difficulty in estimating DMI of grazing animals (level of intake is a major driver of enteric CH4 production), the infrequency of supplementation, and the variable level of individual animal supplement intake (
      • Buddle B.M.
      • Denis M.
      • Attwood G.T.
      • Altermann E.
      • Janssen P.H.
      • Ronimus R.S.
      • Pinares-Patiño C.S.
      • Muetzel S.
      • Wedlock D.N.
      Strategies to reduce methane emissions from farmed ruminants grazing on pasture..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). Common mitigation strategies are supplementation to increase animal performance (thereby decreasing emission intensity, although not always done specifically to decrease emissions, e.g., protein supplementation), supplements that directly alter ruminal fiber digestion or methanogens, breeding for more efficient animals, and vaccinating against methanogens (
      • Phetteplace H.W.
      • Johnson D.E.
      • Seidl A.F.
      Greenhouse gas emissions from simulated beef and dairy livestock systems in the United States..
      ;
      • Grainger C.
      • Beauchemin K.A.
      Can enteric methane emissions from ruminants be lowered without lowering their production?.
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). Other strategies such as nitrate supplementation do not seem practical because of issues in getting the inhibitor to the animal in useful quantities or risks of toxicity (
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ;
      • Llonch P.
      • Haskell M.J.
      • Dewhurst R.J.
      • Turner S.P.
      Review: current available strategies to mitigate greenhouse gas emissions in livestock systems: an animal welfare perspective..
      ).

      Supplementation.

      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      and
      • Shibata M.
      • Terada F.
      Factors affecting methane production and mitigation in ruminants..
      hypothesized that improving the efficiency of feed energy use has the greatest potential for mitigating enteric CH4 production. Outside of improving the forage base, providing supplementation to meet the nutritional needs of different classes of grazing animals is a mitigation option. Producers have long supplemented grazing ruminants to improve performance during times of nutritional deficiencies in the forage crop, such as the late summer slump or winter dormancy that affects many forage bases across the United States (
      • Caton J.S.
      • Dhuyvetter D.V.
      Influence of energy supplementation on grazing ruminants: Requirements and responses..
      ). Similar to estimating emissions of grazing animals, accurate and precise supplementation is difficult because energy requirements for grazing animals are not the same as for confinement-fed cattle (
      • Caton J.S.
      • Dhuyvetter D.V.
      Influence of energy supplementation on grazing ruminants: Requirements and responses..
      ). The most common forms of beef cow supplementation are energy supplementation, when intake of C skeletons are the limiting nutrient for ruminal microbial growth, and protein supplementation when low-quality forages (e.g., CP <7%) are the primary diet. Energy supplementation can come in many forms, such as corn grain or fat supplementation, depending on the goals of the producer. For example, when cattle are grazing wheat pasture that is high in water and protein contents, but low in fiber, corn supplementation can improve animal performance (

      Hogan, J. P. 1982. Digestion and utilization of proteins. Pages 245–257 in Nutritional Limits to Animal Production from Pastures. J. B. Hacker, ed. Commonwealth Agric. Bureaux, Slough, UK.

      ). Although not specifically done to alter CH4 emissions, by improving animal performance, this strategy indirectly improves emission intensity (
      • Thompson L.R.
      • Beck M.R.
      • Gunter S.A.
      • Williams G.D.
      • Place S.E.
      • Reuter R.R.
      An energy and monensin supplement reduces methane emission intensity of stocker cattle grazing winter wheat..
      ). Similarly, during times of forage dormancy, protein is supplemented to improve performance to meet microbial N requirements (
      • McCollum III, F.T.
      • Horn G.W.
      Protein supplementation of grazing livestock: A review..
      ;
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      ). Protein supplementation does not directly affect rumen methanogens, unlike energy supplementation strategies, and can come in a multitude of forms including pelleted feed, limit grazing of cool-season forage, and lick blocks, among others (
      • Leng R.A.
      Quantitative ruminant nutrition—A green science..
      ;
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      ).
      • McCollum F.T.
      • Galyean M.L.
      Influence of cottonseed meal supplementation on voluntary intake, rumen fermentation and rate of passage of prairie hay in beef steers..
      in a crossover design using ruminally cannulated steers reported that cottonseed meal (37.9% CP) fed at 800 g/head per day improved forage use by improving IVDMD and animal performance. Unfortunately, there is limited literature on the effects of supplemental protein on enteric CH4 emissions. Decades ago,
      • Leng R.A.
      Quantitative ruminant nutrition—A green science..
      and
      • Moss A.R.
      Methane production by ruminants—Literature review of I. Dietary manipulation to reduce methane production and II. Laboratory procedures for estimating methane potential of diets..
      suggested that this strategy could be particularly beneficial in developing countries where animal nutrition is potentially poor. They also suggested that using targeted supplementation in these countries could reduce enteric CH4 emissions by improving the nutritional balance in the rumen.
      • DeRamus H.A.
      • Clement T.C.
      • Giampola D.D.
      • Dickison P.C.
      Methane emissions of beef cattle on forages..
      , using the SF6 technique, reported that heifers grazing ryegrass ad libitum had one-tenth of the CH4 emission intensity compared with animals limit grazing ryegrass for 1 h during the spring but that limit grazing for 4 h resulted in similar enteric CH4 emissions.
      • Boadi D.A.
      • Wittenberg K.M.
      • McCaughey W.P.
      Effects of grain supplementation on methane production of grazing steers using the sulphur (SF6) tracer gas technique..
      compared grazing steers supplemented with rolled barley grain at 2, 4, and 4 kg/head per day during the early, mid, and late grazing season, respectively, with steers grazing alfalfa and meadow grass pastures without supplementation. They reported that supplementation reduced forage intake and increased total OM consumed but did not affect overall enteric CH4 emissions. It was hypothesized from the results that the greater forage quality and quantity were the major factors influencing animal responses. However, considering the high forage quality available to the steers, one should not apply these results to cattle grazing lower quality forage where supplementation might improve the nutritional status of the rumen. Considering the heavy reliance on forage quality by governing bodies when estimating CH4 emissions (

      IPCC. 2006. IPCC Guidelines for Greenhouse Gas Inventories. Intergov. Panel Climate Change, Geneva, Switzerland.

      ), it would be beneficial to do more long-term monitoring because of the variation among different production systems, changes in forage quality throughout the year, and supplementation strategies that exist to improve animal performance. Considering the advancements in modern emission quantification techniques, along with the lowering cost of monitoring, long-term studies should be conducted.
      Lipid supplementation is a plausible approach to directly reduce enteric CH4 emissions (
      • Beauchemin K.A.
      • McAllister T.A.
      • McGinn S.M.
      Dietary mitigation of enteric methane from cattle..
      ). Nutritionally, lipids are categorized by their effects on ruminal activity and fiber digestion (
      • Jenkins T.
      Success of fat in dairy rations depends on the amount..
      ). There is a wealth of literature exploring the effects of fats on ruminal CH4 production. Lipid supplementation apparently alters emissions through reductions in ruminal fiber digestion, although there is some evidence for a suppressive effect on bacteria and protozoa activity (
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). An additional mode of action is UFA acting as a H2 sink during the process of biohydrogenation in the rumen. This reduces the H2 pool available to methanogenic archaea; however, this process appears to have minimal effect and was suggested to only account for 1 to 2% of metabolic H2 (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle..
      ;
      • Jenkins T.C.
      • Wallace R.J.
      • Moate P.J.
      • Mosley E.E.
      Board-invited review: Recent advances in biohydrogenation of unsaturated fatty acids within the rumen microbial ecosystem..
      ). A group of lipids, including animal-based tallow and grease, oils from plants (e.g., soybean oil and cottonseeds), and high-fat by-products (such as distillers grains), can alter ruminal CH4 production (
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). The most likely mode of action for these supplements is coating fiber particles to protect them from ruminal microbes. When supplemented at appropriate dietary concentrations, these lipid sources can reduce CH4 production without altering DM digestibility or forage intake (
      • Grainger C.
      • Beauchemin K.A.
      Can enteric methane emissions from ruminants be lowered without lowering their production?.
      ;
      • Patra A.K.
      Enteric methane mitigation technologies for ruminant livestock: A synthesis of current research and future directions..
      ). There has been extensive research done with dietary lipids, but unfortunately, the majority were conducted with dairy or beef cattle fed TMR with significant proportions of concentrate feeds (
      • Beck M.R.
      • Thompson L.R.
      • Williams G.D.
      • Place S.E.
      • Gunter S.A.
      • Reuter R.R.
      Fat supplements differing in physical form improve performance but divergently influence methane emissions of grazing beef cattle..
      ). In 2 separate experiments using the GEM emission measurement system,
      • Beck M.R.
      • Thompson L.R.
      • White J.E.
      • Williams G.D.
      • Place S.E.
      • Moffet C.A.
      • Gunter S.A.
      • Reuter R.R.
      Whole cottonseed supplementation improves performance and reduces methane emission intensity of grazing beef steers..
      ,
      • Beck M.R.
      • Thompson L.R.
      • Williams G.D.
      • Place S.E.
      • Gunter S.A.
      • Reuter R.R.
      Fat supplements differing in physical form improve performance but divergently influence methane emissions of grazing beef cattle..
      examined the effects of whole cottonseed supplementation and rumen bypass fat or soybean oil on enteric CH4 emissions of steers grazing old world bluestem pastures. In both experiments CH4 production was reduced when steers were offered whole cottonseed or soybean oil. Rumen bypass fat did not alter CH4 production (g/d) but did when expressed as grams per kilogram of BW gain and lowered CH4 yield (9.7 vs. 8.0% for control vs. bypass fat-supplemented cattle).
      • Carvalho P.C.
      • Fiorentini G.
      • Berndt A.
      • Castagnino P.S.
      • Messana J.D.
      • Frighetto R.T.S.
      • Reis R.A.
      • Berchielli T.T.
      Performance and methane emissions of Nellore steers grazing tropical pasture supplemented with lipid sources..
      examined Nellore steers grazing C4 grasses offered no supplement, palm oil, linseed oil, rumen bypass fat, or whole soybeans supplemented at 1% of BW. They found that the linseed oil treatment reduced CH4 emissions per kilogram of BW, but none of the lipid supplements improved animal performance or DMI. The authors hypothesized that a reduction in ruminal fiber digestibility may have been responsible for the lack of improvement in performance. These studies show that different lipid sources can potentially be beneficial both environmentally and economically through effects on performance, but overfeeding lipids can be detrimental, although results are not consistent across different lipid sources as some studies have shown reductions in DMI and productivity (
      • Grainger C.
      • Beauchemin K.A.
      Can enteric methane emissions from ruminants be lowered without lowering their production?.
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ).
      • Grainger C.
      • Beauchemin K.A.
      Can enteric methane emissions from ruminants be lowered without lowering their production?.
      conducted a meta-analysis and showed that whereas some supplemental lipids do reduce CH4 production, there were significant linear and curvilinear responses in CH4 production from diets containing up to 13% lipids, and dietary fat content should not be greater than 6 to 7%, DM basis (
      • Patra A.K.
      Enteric methane mitigation technologies for ruminant livestock: A synthesis of current research and future directions..
      ). The persistence of CH4 reduction has been inconsistent in the literature (
      • Grainger C.
      • Beauchemin K.A.
      Can enteric methane emissions from ruminants be lowered without lowering their production?.
      ). Studies such as those conducted by
      • Martin C.
      • Pomiès D.
      • Ferlay A.
      • Rochette Y.
      • Martin B.
      • Chilliard Y.
      • Morgavi D.P.
      • Doreau M.
      Methane output and rumen microbiota in dairy cows in response to long-term supplementation with linseed or rapeseed of grass silage- or pasture-based diets..
      and
      • Grainger C.
      • Williams R.
      • Clarke T.
      • Wright A.D.G.
      • Eckard R.J.
      Supplementation with whole cotton seed causes long-term reduction of methane emissions from lactating dairy cows offered a forage and cereal grain diet..
      have resulted in long-term emission mitigation that may be due to animal type or diet variability. More long-term experiments should be conducted with grazing beef cows to determine how effective lipid supplementation could be at the herd emissions level, as well as to explore economic methods of supplementation.
      Ionophores are common feed additives provided to both grazing and confinement-fed cattle because of their effects on animal health and efficiency (
      • Byers F.M.
      • Schelling G.T.
      Ionophore effects on composition of growth and digestive tract fill in grazing cattle..
      ;
      • Callaway T.R.
      • Edrington T.S.
      • Rychlik J.L.
      • Genovese K.J.
      • Poole T.L.
      • Jung Y.S.
      • Bischoff K.M.
      • Anderson R.C.
      • Nisbet D.J.
      Ionophores: Their use as ruminant growth promotants and impact on food safety..
      ). The most frequently used ionophore, monensin, improves energy and N utilization by selective inhibition of gram-positive ruminal bacteria, which favors propionate production (
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ). Ionophores effectively inhibit gram-positive bacteria by facilitating the transport of ions across the cell membrane, which leads to the disruption of the chemi-osmotic gradient (
      • Bergen W.G.
      • Bates D.B.
      Ionophores: Their effect on production efficiency and mode of action..
      ). A greater proportion of gram-negative bacteria shifts the acetate:propionate ratio, favoring production of the more energetically efficient propionate, which acts as a H sink, thereby potentially reducing CH4 production (

      Place, S. E., K. R. Stackhouse, Q. Wang, and F. M. Mitloehner. 2011. Mitigation of greenhouse gas emissions from U. S. beef and dairy production systems. Pages 443–457 in Understanding Greenhouse Gas Emissions from Agricultural Management. L. Guo, A. Gunasekara, and L. McConnell, ed. ACS Symp. Series, Washington, DC.

      ;
      • Ranga Niroshan Appuhamy J.A.D.
      • Strathe A.B.
      • Jayasundara S.
      • Wagner-Riddle C.
      • Dijkstra J.
      • France J.
      • Kebreab E.
      Anti-methanogenic effects of monensin in dairy and beef cattle: A meta-analysis..
      ). However, the effect of ionophores on CH4 production has been inconsistent and sometimes not detected in studies in grazing systems (
      • Ranga Niroshan Appuhamy J.A.D.
      • Strathe A.B.
      • Jayasundara S.
      • Wagner-Riddle C.
      • Dijkstra J.
      • France J.
      • Kebreab E.
      Anti-methanogenic effects of monensin in dairy and beef cattle: A meta-analysis..
      ;
      • Thompson L.R.
      • Beck M.R.
      • Gunter S.A.
      • Williams G.D.
      • Place S.E.
      • Reuter R.R.
      An energy and monensin supplement reduces methane emission intensity of stocker cattle grazing winter wheat..
      ). In a meta-analysis of 22 studies,
      • Ranga Niroshan Appuhamy J.A.D.
      • Strathe A.B.
      • Jayasundara S.
      • Wagner-Riddle C.
      • Dijkstra J.
      • France J.
      • Kebreab E.
      Anti-methanogenic effects of monensin in dairy and beef cattle: A meta-analysis..
      reported that including monensin at 32 mg/kg of DM reduced CH4 yield (% GE lost as CH4) by 0.33 ± 0.16% for steers consuming TMR. In an experiment with dairy cows grazing a predominantly ryegrass sward with monensin supplemented at 471 mg/d, no differences were detected compared with cows not receiving monensin (
      • Grainger C.
      • Williams R.
      • Eckard R.J.
      • Hannah M.C.
      A high dose of monensin does not reduce methane emissions of dairy cows offered pasture supplemented with grain..
      ). A respiration chamber experiment was conducted concurrently with the grazing experiment. In cows receiving the same monensin dose and offered fresh-cut ryegrass no difference on CH4 production was detected from monensin supplementation. Similarly,
      • Grainger C.
      • Auldist M.J.
      • Clarke T.
      • Beauchemin K.A.
      • McGinn S.M.
      • Hannah M.C.
      • Eckard R.J.
      • Lowe L.B.
      Use of monensin controlled-release capsules to reduce methane emissions and improve milk production of dairy cows offered pasture supplemented with grain..
      dosed monensin using a controlled-release capsule and reported that enteric CH4 yield of dairy cows grazing ryegrass pasture was not affected by monensin supplementation. In a respiration chamber experiment with steers consuming fresh chopped winter wheat at increasing intake levels and offered monensin (158 g/head per d), CH4 production tended to be reduced for supplemented animals compared with nonsupplemented animals at 115 versus 130 L/d, respectively (P = 0.06;
      • Shreck A.L.
      • Ebert P.J.
      • Bailey E.A.
      • Jennings J.S.
      • Casey K.D.
      • Meyer B.E.
      • Cole N.A.
      Effects of energy supplementation on energy losses and nitrogen balance of steers fed green-chopped wheat pasture I: Calorimetry..
      ). There was no difference in GEI lost as CH4 when animals were fed at 1.5×maintenance. However, in an experiment with beef steers and heifers grazing winter wheat offered an energy supplement containing monensin (34 mg/kg of DM),
      • Thompson L.R.
      • Beck M.R.
      • Gunter S.A.
      • Williams G.D.
      • Place S.E.
      • Reuter R.R.
      An energy and monensin supplement reduces methane emission intensity of stocker cattle grazing winter wheat..
      found that increasing level of supplement intake reduced CH4 emission intensity (g of CH4/kg of BW gain). Whereas cattle fed TMR have displayed long-term reductions in CH4 production, potential explanations for the inconsistency in grazing trials could be variable dietary quality of different forage bases, the rate of intake, and the lack of studies conducted using beef cattle in grazing environments (
      • Odongo N.E.
      • Bagg R.
      • Vessie G.
      • Dick P.
      • Or-Rashid M.M.
      • Hook S.E.
      • Gray J.T.
      • Kebreab E.
      • France J.
      • McBride B.W.
      Long-term effects of feeding monensin on methane production in lactating dairy cows..
      ;
      • Grainger C.
      • Auldist M.J.
      • Clarke T.
      • Beauchemin K.A.
      • McGinn S.M.
      • Hannah M.C.
      • Eckard R.J.
      • Lowe L.B.
      Use of monensin controlled-release capsules to reduce methane emissions and improve milk production of dairy cows offered pasture supplemented with grain..
      ;
      • Hristov A.N.
      • Oh J.
      • Firkins J.L.
      • Dijkstra J.
      • Kebreab E.
      • Waghorn G.
      • Makkar H.P.S.
      • Adesogan A.T.
      • Yang W.
      • Lee C.
      • Gerber P.J.
      • Henderson B.
      • Tricarico J.M.
      Mitigation of methane and nitrous oxide emissions from animal operations: I. A review of enteric methane mitigation options..
      ;
      • Ranga Niroshan Appuhamy J.A.D.
      • Strathe A.B.
      • Jayasundara S.
      • Wagner-Riddle C.
      • Dijkstra J.
      • France J.
      • Kebreab E.
      Anti-methanogenic effects of monensin in dairy and beef cattle: A meta-analysis..
      ). Even though monensin may result in reductions of CH4 emissions and has proven to improve feed efficiency and reduce bloat, it has been banned in the European Union since 2006, and its classification as an antibiotic could result in increased scrutiny in future years in other regions.
      Although not a new feed additive, recent research showed the potential antimethanogenic properties of Asparagopsis species (seaweed) inclusion in the diet, both in vitro and in vivo (
      • Machado L.
      • Magnusson M.
      • Paul N.A.
      • Kinley R.
      • de Nys R.
      • Tomkins N.
      Dose-response effects of Asparagopsis taxiformis and Oedogoniumsp. on in vitro fermentation and methane production..
      ;
      • Li X.
      • Norman H.C.
      • Kinley R.D.
      • Laurence M.
      • Wilmot M.
      • Bender H.
      • de Nys R.
      • Tomkins N.
      Asparagopsis taxiformis decreases enteric methane production in sheep..
      ;
      • Roque B.M.
      • Brooke C.G.
      • Ladau J.
      • Polley T.
      • Marsh L.J.
      • Najafi N.
      • Pandey P.
      • Singh L.
      • Kinley R.
      • Salwen J.K.
      • Eloe-Fadrosh E.
      • Kebreab E.
      • Hess M.
      Effect of macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage..
      ,
      • Roque B.M.
      • Salwen J.K.
      • Kinley R.
      • Kebreab E.
      Inclusion of Asparagopsis armata in lactating dairy cows’ diet reduces enteric methane emission by over 50 percent..
      ). Asparagopsis microalgae produces bioactive compounds including bromoform and dibromochloromethane, giving it the same potential mode of action as the chemical additive bromochloromethane that decreased enteric CH4 emissions (
      • Tomkins N.W.
      • Colegate S.M.
      • Hunter R.A.
      A bromochloromethane formulation reduces enteric methanogenesis in cattle fed grain-based diets..
      ). In an in vitro dose-response experiment,
      • Machado L.
      • Magnusson M.
      • Paul N.A.
      • Kinley R.
      • de Nys R.
      • Tomkins N.
      Dose-response effects of Asparagopsis taxiformis and Oedogoniumsp. on in vitro fermentation and methane production..
      tested 10 doses of Asparagopsis inclusion from 0 to 16.7% OM incubated with a grass hay substrate. Methane production was reduced by 99% at 2% OM inclusion level. When included on a 0.5 or 1% OM basis in a TMR,
      • Roque B.M.
      • Salwen J.K.
      • Kinley R.
      • Kebreab E.
      Inclusion of Asparagopsis armata in lactating dairy cows’ diet reduces enteric methane emission by over 50 percent..
      reported that CH4 emissions from dairy cows sampled with a GEM were reduced by 43% at the 1% inclusion level after adjusting to account for differences in DMI. Methane reduction of this magnitude would make seaweed supplementation with Asparagopsis inclusion one of the most noteworthy mitigation strategies tested in vivo. Additionally,
      • Li X.
      • Norman H.C.
      • Kinley R.D.
      • Laurence M.
      • Wilmot M.
      • Bender H.
      • de Nys R.
      • Tomkins N.
      Asparagopsis taxiformis decreases enteric methane production in sheep..
      offered it to sheep fed a high-fiber pelleted diet and reported that ruminal propionate concentrations increased with Asparagopsis supplementation and CH4 production decreased over a 72-d period. Supplementation of Asparagopsis in grazing environments at different intakes and frequencies of supplementation is needed to establish its efficacy in high-forage systems, beyond high-concentrate confinement feeding.
      Another possible avenue for enteric CH4 mitigation was the discovery that CH4 emissions might be heritable, suggesting that genetic selection of animals might be a viable mitigation possibility (
      • Pinares-Patiño C.S.
      • Hickey S.M.
      • Young E.A.
      • Dodds K.G.
      • MacLean S.
      • Molano G.
      • Sandoval E.
      • Kjestrup H.
      • Harland R.
      • Hunt C.
      • Pickering N.K.
      • McEwan J.C.
      Heritability estimates of methane emissions from sheep..
      ;
      • Roehe R.
      • Dewhurst R.J.
      • Duthie C.
      • Rooke J.A.
      • McKain N.
      • Ross D.W.
      • Hyslop J.J.
      • Waterhouse A.
      • Freeman T.C.
      • Watson M.
      • Wallace R.J.
      Bovine host genetic variation influences rumen microbial methane production with best selection criterion for low methane emitting and efficiently feed converting hosts based on metagenomic gene abundance..
      ). It is hypothesized that this is possible because the host animal asserts some form of influence over its own microbiota (
      • Roehe R.
      • Dewhurst R.J.
      • Duthie C.
      • Rooke J.A.
      • McKain N.
      • Ross D.W.
      • Hyslop J.J.
      • Waterhouse A.
      • Freeman T.C.
      • Watson M.
      • Wallace R.J.
      Bovine host genetic variation influences rumen microbial methane production with best selection criterion for low methane emitting and efficiently feed converting hosts based on metagenomic gene abundance..
      ). Some researchers suggested that the mechanisms controlling the microbiome may be in the interactions with receptors in the rumen wall or salivary antibodies (
      • Tapio I.
      • Snelling T.J.
      • Strozzi F.
      • Wallace R.J.
      The ruminal microbiome associated with methane emissions form ruminant livestock..
      ).
      • Goopy J.P.
      • Robinson D.L.
      • Woodgate R.T.
      • Donaldson A.J.
      • Oddy V.H.
      • Vercoe P.E.
      • Hegarty R.S.
      Estimates of repeatability and heritability of methane production in sheep using portable accumulation chambers..
      hypothesized that the physical structure of the rumen could explain the differences between genetic lines, but their results were not consistent. Additionally, their results implied, although indirectly, sire x environmental interactions, indicating that selecting cattle for reduced CH4 emissions in one environment may not improve performance as the animal moves from a grazing system to the feedlot. In a study analyzing about 3,400 records, along with the records reported by
      • Pinares-Patiño C.S.
      • Hickey S.M.
      • Young E.A.
      • Dodds K.G.
      • MacLean S.
      • Molano G.
      • Sandoval E.
      • Kjestrup H.
      • Harland R.
      • Hunt C.
      • Pickering N.K.
      • McEwan J.C.
      Heritability estimates of methane emissions from sheep..
      ,
      • Jonker A.
      • Hickey S.M.
      • Rowe S.J.
      • Janssen P.H.
      • Shackell G.H.
      • Elmes S.
      • Bain W.E.
      • Wing J.
      • Greer G.J.
      • Bryson B.
      • MacLean S.
      • Dodds K.G.
      • Pinares-Patiño C.S.
      • Young E.A.
      • Knowler K.
      • Pickering N.K.
      • McEwan J.
      Genetic parameters of methane emissions determined using portable accumulation chambers in lambs and ewes grazing pasture and genetic correlations with emissions determined in respiration chambers..
      reported heritability estimates of 0.23 and 0.13 for CH4 g/d and CH4 yield, respectively, in New Zealand sheep. Estimates in Angus cattle were similar as reported by
      • Hayes B.J.
      • Donoghue K.A.
      • Reich C.M.
      • Mason B.A.
      • Bird-Gardiner T.
      • Herd R.M.
      • Arthur P.F.
      Genomic heritabilities and genomic estimated breeding values for methane traits in Angus cattle..
      . They reported heritability values of 0.27 and 0.29 for CH4 production and CH4 yield from 737 Angus cattle in Australia. Additionally, new research found significant differences between breeds. In a study of Nelore and Angus cattle grazing during the growing period and finishing in a feedlot,
      • Maciel I.C.F.
      • Barbosa F.A.
      • Tomich T.R.
      • Ribeiro L.G.P.
      • Alvarenga R.C.
      • Lopes L.S.
      • Malacco V.M.R.
      • Rowntree J.E.
      • Thompson L.R.
      • Lana A.M.Q.
      Could the breed composition improve performance and change the enteric methane emissions from beef cattle in a tropical intensive production system?.
      determined that the Nelore cattle produced significantly less CH4 (g/d) than Angus cattle regardless of diet. However, in the finishing period the Angus steers reached finishing weight faster and therefore produced the same amount of CH4 during the finishing phase as the Nelore steers (
      • Maciel I.C.F.
      • Barbosa F.A.
      • Tomich T.R.
      • Ribeiro L.G.P.
      • Alvarenga R.C.
      • Lopes L.S.
      • Malacco V.M.R.
      • Rowntree J.E.
      • Thompson L.R.
      • Lana A.M.Q.
      Could the breed composition improve performance and change the enteric methane emissions from beef cattle in a tropical intensive production system?.
      ). More work to refine the selection technique and characterization of beef herds in other countries could potentially allow for reductions in the carbon footprint of beef production.
      Methane production is partially dependent on the quantity of feed consumed, which led researchers to explore selecting animals based on their residual feed intake (RFI;
      • Hegarty R.S.
      • Goopy J.P.
      • Herd R.M.
      • McCorkell B.
      Cattle selected for lower residual feed intake have reduced daily methane production..
      ). Residual feed intake is defined as the difference between actual feed intake and the expected rate of intake needed for that animal to meet its maintenance requirements plus the desired production level (e.g., milk, meat, wool;
      • Arthur P.F.
      • Archer J.A.
      • Johnston D.J.
      • Herd R.M.
      • Richardson E.C.
      • Parnell P.F.
      Genetic and phenotypic variance and covariance components for feed intake, feed efficiency, and other postweaning traits in Angus cattle..
      ). Research on this strategy has been inconsistent and variable across environments (
      • Hegarty R.S.
      • Goopy J.P.
      • Herd R.M.
      • McCorkell B.
      Cattle selected for lower residual feed intake have reduced daily methane production..
      ;
      • McDonnell R.P.
      • Hart K.J.
      • Boland T.M.
      • Kelly A.K.
      • McGee M.
      • Kenny D.A.
      Effect of divergence in phenotypic residual feed intake on methane emissions, ruminal fermentation, and apparent whole-tract digestibility of beef heifers across three contrasting diets..
      ;
      • Velazco J.I.
      • Herd R.M.
      • Cottle D.J.
      • Hegarty R.S.
      Daily methane emissions and emission intensity of grazing beef cattle genetically divergent for residual feed intake..
      ). In a study with low- and high-RFI Limousin × Fresian heifers, enteric CH4 production, DMI, and performance were measured in both grazing and confinement systems (
      • McDonnell R.P.
      • Hart K.J.
      • Boland T.M.
      • Kelly A.K.
      • McGee M.
      • Kenny D.A.
      Effect of divergence in phenotypic residual feed intake on methane emissions, ruminal fermentation, and apparent whole-tract digestibility of beef heifers across three contrasting diets..
      ). The study indicated that animals with low RFI actually had greater CH4 emissions on the basis of DMI and GEI than high-RFI animals. These results were similar to those of
      • Velazco J.I.
      • Herd R.M.
      • Cottle D.J.
      • Hegarty R.S.
      Daily methane emissions and emission intensity of grazing beef cattle genetically divergent for residual feed intake..
      and
      • Flay H.E.
      • Kuhn-Sherlock B.
      • MacDonald K.A.
      • Camara M.
      • Lopez-Villalobos N.
      • Donaghy D.J.
      • Roche J.R.
      Hot topic: Selecting cattle for low residual feed intake did not affect daily methane production but increased methane yield..
      , who found that cattle with heavier BW and low RFI had greater DMP compared with high-RFI cattle. Other studies, such as those conducted by
      • Hegarty R.S.
      • Goopy J.P.
      • Herd R.M.
      • McCorkell B.
      Cattle selected for lower residual feed intake have reduced daily methane production..
      and
      • Lawrence P.
      • Kenny D.A.
      • Earley B.
      • Crews Jr., D.H.
      • McGee M.
      Grass silage intake, rumen and blood variables, ultrasonic and body measurements, feeding behavior and activity in pregnant beef heifers differing in phenotypic residual feed intake..
      , reported low-RFI cattle had lower enteric CH4 emissions. These inconsistent results demonstrate that RFI classifications are not consistent across diets or animals, particularly growing animals, currently limiting the application of RFI as a mitigation tool.

      Vaccination Against Methanogens.

      Vaccination against ruminal methanogens is another potential strategy, which thus far has produced inconsistent results. This approach is based on the generation of an antibody response that is delivered to the rumen through salivary secretions to neutralize methanogens (
      • Buddle B.M.
      • Denis M.
      • Attwood G.T.
      • Altermann E.
      • Janssen P.H.
      • Ronimus R.S.
      • Pinares-Patiño C.S.
      • Muetzel S.
      • Wedlock D.N.
      Strategies to reduce methane emissions from farmed ruminants grazing on pasture..
      ). Such a vaccination potentially would be easy for many producers to implement because they already use some type of annual vaccination protocol; thus, vaccination might be cost effective (
      • Buddle B.M.
      • Denis M.
      • Attwood G.T.
      • Altermann E.
      • Janssen P.H.
      • Ronimus R.S.
      • Pinares-Patiño C.S.
      • Muetzel S.
      • Wedlock D.N.
      Strategies to reduce methane emissions from farmed ruminants grazing on pasture..
      ).
      • Cook S.R.
      • Maiti P.K.
      • Chaves A.V.
      • Benchaar C.
      • Beauchemin K.A.
      • McAllister T.A.
      Avian (IgY) anti-methanogen antibodies for reducing ruminal methane production: in vitro assessment of their effects..
      demonstrated that concentrations of avian antimethanogen antibodies can reduce CH4 production in vitro. In a study with mature wether sheep,
      • Wright A.D.G.
      • Kennedy P.
      • O’Neill C.J.
      • Toovey A.F.
      • Popovski S.
      • Rea S.M.
      • Pimm C.L.
      • Klein L.
      Reducing methane emissions in sheep by immunization against rumen methanogens..
      isolated methanogens and provided sheep with a 3-methanogen mixture, a 7-methanogen mixture followed by the 3-methanogen mixture, or adjuvant only. Primary and secondary immunizations were given subcutaneously 153 d apart. Testing CH4 emissions with both respiration chambers and the SF6 technique, they found a significant 7.7% reduction in enteric CH4 production 4 wk after secondary immunization in sheep provided the 3-methanogen mixture.
      • Wedlock D.N.
      • Pedersen G.
      • Denis M.
      • Dey D.
      • Janssen P.H.
      • Buddle B.M.
      Development of a vaccine to mitigate greenhouse gas emissions in agriculture: Vaccination of sheep with methanogen fractions induces antibodies that block methane production in vitro..
      , although not measuring enteric CH4 emission, did find that antisera selected from methanogen fractions produced a strong antibody response in sheep, with both IgG and IgA responses detected in the saliva. However, in a study using a vaccine attempting to account for 52% of the methanogens present in the rumen,
      • Williams Y.J.
      • Popovski S.
      • Rea S.M.
      • Skillman L.C.
      • Toovey A.F.
      • Northwood K.S.
      • Wright A.D.G.
      A vaccine against rumen methanogens can alter the composition of archaeal populations..
      found that CH4 production actually increased by 18% in sheep after 3 vaccinations, opposite of the effect expected. Minimal research has examined the efficacy of methanogen vaccination in cattle.
      • Subharat S.
      • Shu D.
      • Zheng T.
      • Buddle B.M.
      • Janssen P.H.
      • Luo D.
      • Wedlock D.N.
      Vaccination of cattle with a methanogen protein produces specific antibodies in the saliva which are stable in the rumen..
      , using 5-mo-old male Holstein-Friesian calves, provided s.c. antimethanogen vaccinations isolated from Methanobrevibacter ruminantium M1. They detected a strong IgG response and a moderate IgA response in the serum and saliva of inoculated animals. The authors also took rumen fluid samples and found an antibody presence in the rumen (
      • Subharat S.
      • Shu D.
      • Zheng T.
      • Buddle B.M.
      • Janssen P.H.
      • Luo D.
      • Wedlock D.N.
      Vaccination of cattle with a methanogen protein produces specific antibodies in the saliva which are stable in the rumen..
      ).
      In vivo vaccination trials showed promise but may be limited by current knowledge of the rumen methanogen population (
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review..
      ). In the study by
      • Williams Y.J.
      • Popovski S.
      • Rea S.M.
      • Skillman L.C.
      • Toovey A.F.
      • Northwood K.S.
      • Wright A.D.G.
      A vaccine against rumen methanogens can alter the composition of archaeal populations..
      , the 5-methanogen species vaccination resulted in increased CH4 production, even with the desired immune response being observed. The authors hypothesized that this was because the vaccine was not targeting the species responsible for most of the CH4 production or that some unknown conditions are necessary to see an abatement response recorded in previous studies (
      • Williams Y.J.
      • Popovski S.
      • Rea S.M.
      • Skillman L.C.
      • Toovey A.F.
      • Northwood K.S.
      • Wright A.D.G.
      A vaccine against rumen methanogens can alter the composition of archaeal populations..
      ). It also was noted by authors that any vaccine formulation is diet and environment specific, with a broad spectrum currently out of the reach of current research (
      • Williams Y.J.
      • Popovski S.
      • Rea S.M.
      • Skillman L.C.
      • Toovey A.F.
      • Northwood K.S.
      • Wright A.D.G.
      A vaccine against rumen methanogens can alter the composition of archaeal populations..
      ;
      • Hook S.E.
      • Wright A.D.G.
      • McBride B.W.
      Methanogens: Methane producers of the rumen and mitigation strategies..
      ).
      • Whitford M.F.
      • Teather R.M.
      • Forster R.J.
      Phylogenetic analysis of methanogens from the bovine rumen..
      found that most rumen methanogens are difficult to culture and that the majority of species, at that time, had yet to be isolated. For the vaccination approach to show promise in the future, it will be critical to successfully culture highly productive methanogen species and to do so across production systems as methanogen populations can vary widely by region and diet (
      • Hook S.E.
      • Wright A.D.G.
      • McBride B.W.
      Methanogens: Methane producers of the rumen and mitigation strategies..
      ).

      Soil Methanotrophy

      Outside of CH4 oxidation by OH radicals in the atmosphere, the only major sink of atmospheric CH4 is oxidation by soil microbes (
      • Saggar S.
      • Tate K.R.
      • Giltrap D.L.
      • Singh J.
      Soil-atmosphere exchange of nitrous oxide and methane in New Zealand terrestrial ecosystems and their mitigation options: A review..
      ;
      • Hartmann A.A.
      • Buchmann N.
      • Niklaus P.A.
      A study of soil methane sink regulation in two grasslands exposed to drought and N fertilization..
      ). Soils can be either a source or sink of CH4, with mostly obligate aerobic methanotrophs located in the upper levels of upland soils responsible for oxidizing atmospheric CH4 to CO2, but the ecological controls involved are still poorly understood, creating large uncertainties (
      • Saggar S.
      • Tate K.R.
      • Giltrap D.L.
      • Singh J.
      Soil-atmosphere exchange of nitrous oxide and methane in New Zealand terrestrial ecosystems and their mitigation options: A review..
      ;

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). It is estimated that methanotrophic activity in soil may remove about 9 to 47 Tg of CH4/yr, and this mostly occurs in aerobic soils (

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). Activity of soil methanotrophs is dependent on the diffusion rate of CH4 and biological activity of soil (
      • Mosier A.R.
      • Duxbury J.M.
      • Freney J.R.
      • Heinemeyer O.
      • Minami K.
      • Johnson D.E.
      Mitigating agricultural emissions of methane..
      ). After a rainfall, CH4 is immediately emitted from the soil, with this emission rate gradually decreasing as soil dries, and more CH4 is oxidized as the diffusion becomes less suppressed as less water fills the pore networks (
      • Mosier A.R.
      • Duxbury J.M.
      • Freney J.R.
      • Heinemeyer O.
      • Minami K.
      • Johnson D.E.
      Mitigating agricultural emissions of methane..
      ;
      • Hartmann A.A.
      • Buchmann N.
      • Niklaus P.A.
      A study of soil methane sink regulation in two grasslands exposed to drought and N fertilization..
      ). Forest soils with well-developed soil structure typically display the greatest CH4 oxidation rate, followed by immature forests and then native range land, and last, intensively managed agriculture lands have the lowest CH4 sink potential due to increased and frequent disturbance and fertilizer application (
      • Mosier A.R.
      • Duxbury J.M.
      • Freney J.R.
      • Heinemeyer O.
      • Minami K.
      • Johnson D.E.
      Mitigating agricultural emissions of methane..
      ). Temperate forest soils have CH4 uptake rates ranging from 12.8 to 25.6 kg of CH4/ha per year, compared with agriculture soils, having maximum oxidation rates of 1.6 to 3.2 kg of CH4/ha per year (
      • Smith K.A.
      • Dobbie K.E.
      • Ball B.C.
      • Bakken L.R.
      • Sitaula B.K.
      • Hansen S.
      • Brumme R.
      • Borken W.
      • Christensen S.
      • Prieme A.
      • Fowler D.
      • Macdonald J.A.
      • Skiba U.
      • Klemedtsson L.
      • Kasimir-Klemedtsson A.
      • Degorska A.
      • Orlanski P.
      Oxidation of atmospheric methane in northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink..
      ). Only soils with high water tables were reported to be sources of CH4 (
      • Smith K.A.
      • Dobbie K.E.
      • Ball B.C.
      • Bakken L.R.
      • Sitaula B.K.
      • Hansen S.
      • Brumme R.
      • Borken W.
      • Christensen S.
      • Prieme A.
      • Fowler D.
      • Macdonald J.A.
      • Skiba U.
      • Klemedtsson L.
      • Kasimir-Klemedtsson A.
      • Degorska A.
      • Orlanski P.
      Oxidation of atmospheric methane in northern European soils, comparison with other ecosystems, and uncertainties in the global terrestrial sink..
      ) Nitrogen fertilizer application has a negative relationship with methanotroph activity because ammonium may have an inhibitory effect on the enzyme system responsible for CH4 oxidation (
      • Dunfield P.
      • Knowles R.
      Kinetics of inhibition of methane oxidation by nitrate, nitrite, and ammonium in a humisol..
      ). However, these results are inconsistent in the literature. It was hypothesized by
      • Hütsch B.W.
      • Webster C.P.
      • Powlson D.S.
      Long-term effects of nitrogen-fertilization on methane oxidation in soil of the Broadbalk Wheat Experiment..
      that it may take at least 7 yr of fertilizer application before inhibitory effects are seen. Uptake rates also display significant temporal variation between seasons (
      • Mosier A.R.
      • Duxbury J.M.
      • Freney J.R.
      • Heinemeyer O.
      • Minami K.
      • Johnson D.E.
      Mitigating agricultural emissions of methane..
      ). Methane uptake rates are greatest in summer months when drier soil conditions are present and less in cold, wetter months when methanotroph activity is suppressed and methanogen activity is greater (
      • Mosier A.R.
      • Duxbury J.M.
      • Freney J.R.
      • Heinemeyer O.
      • Minami K.
      • Johnson D.E.
      Mitigating agricultural emissions of methane..
      ). Even with considerably lower oxidation rates, some agricultural soils may still be able to offset CH4 emissions from animal excreta and part of enteric CH4 emissions, but few studies have been conducted in this area and results have been inconsistent (

      Saggar, S., K. Tate, C. B. Hedley, and A. Carran. 2004. Methane emissions from cattle dung and methane consumption in New Zealand grazed pastures. Pages 102–106 in Proceedings of the Workshop on the Science of Atmospheric Trace Gases. NIWA Technical Report 125. T. S. Clackson, ed. Natl. Inst. Water Atmos. Res., Wellington, New Zealand.

      ,
      • Saggar S.
      • Hedley C.B.
      • Giltrap D.L.
      • Lambie S.M.
      Measured and modelled estimates of nitrous oxide emission and methane consumption from a sheep-grazed pasture..
      ).
      • Mosier A.R.
      • Schimel D.S.
      • Valentine D.
      • Bronson K.F.
      • Parton W.J.
      Methane and nitrous oxide fluxes in native, fertilized, and cultivated grassland..
      compared CH4 uptake rates in a native pasture, an annually fertilized pasture, and a nonirrigated wheat field and found that N fertilization of the native grassland reduced the CH4 uptake rate by 35% compared with the native pasture. The nonirrigated wheat field resulted in a further decrease of 15% from the fertilized native pasture (
      • Mosier A.R.
      • Schimel D.S.
      • Valentine D.
      • Bronson K.F.
      • Parton W.J.
      Methane and nitrous oxide fluxes in native, fertilized, and cultivated grassland..
      ). These results are similar to those of
      • Willison T.W.
      • Webster C.P.
      • Goulding K.W.T.
      • Powlson D.S.
      Methane oxidation in temperate soils: Effects of land use and the chemical form of nitrogen fertilizer..
      , who reported that long-term application of ammonium-N fertilizer resulted in reduced CH4 uptake by soils. However, in a study on the effects of plant diversity and fertilizer application on CH4 and N2O fluxes in Germany, it was found that CH4 uptake decreased with increasing plant diversity regardless of fertilization (
      • Niklaus P.A.
      • Le Roux X.
      • Poly F.
      • Buchmann N.
      • Scherer-Lorenzen M.
      • Weigelt A.
      • Barnard R.L.
      Plant species diversity affects soil-atmosphere fluxes of methane and nitrous oxide..
      ). It was hypothesized that this was due to increased soil moisture, which lowered the diffusion rate of CH4. However, other potential explanations for the inconsistency are that N concentrations were not high enough to be inhibitory, fertilizer may not have been applied to fields before experiment onset, or water content of the soils was the limiting factor before enzyme inhibition. In a grazing study on 3 different types of steppe in Inner Mongolia, China (meadow steppe, typical steppe, and desert steppe) and 3 different grazing rates (light, moderate, and heavy grazing), it was reported that light grazing did not change CH4 uptake rates, but moderate and heavy grazing reduced uptake by 6.8 to 37.9% (
      • Tang S.
      • Wang C.
      • Wilkes A.
      • Zhou P.
      • Jiang Y.
      • Han G.
      • Zhao M.
      • Huang D.
      • Schönbach P.
      Contribution of grazing to soil atmosphere CH4 exchange during the growing season in a continental steppe..
      ). However, in a synthesis of 43 studies conducted in China, including the previous study, only heavy grazing rates consistently decreased CH4 uptake (
      • Tang S.
      • Ma L.
      • Wei X.
      • Tian D.
      • Wang B.
      • Li Z.
      • Zhang Y.
      • Shao X.
      Methane emissions in grazing systems in grassland regions of China: A synthesis..
      ). Although the synthesis by
      • Tang S.
      • Ma L.
      • Wei X.
      • Tian D.
      • Wang B.
      • Li Z.
      • Zhang Y.
      • Shao X.
      Methane emissions in grazing systems in grassland regions of China: A synthesis..
      reviews a depth of literature on uptake rate in grazing ecosystems, there is a lack of research incorporating enteric CH4 production rates and the potential of different systems to offset parts of the enteric CH4 budget.

      Carbon Accounting

      The Paris Climate Accord set an aggressive goal of keeping global temperature rise below 1.5°C compared with preindustrial levels by the year 2100 (

      Rogeli, J., D. Shindell, K. Jiang, S. Fifita, P. Forster, V. Ginzburg, C. Handa, H. Kheshgi, S. Kobayashi, E. Kriegler, L. Mundaca, R. Séférian, and M. V. Vilariño. 2018. Mitigation pathways compatible with 1.5°C in the context of sustainable development. In Global Warming of 1.5°C. An IPCC Special Report on the Impacts of Global Warming of 1.5°C Above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty. V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P. R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield, ed. World Meteorol. Org., Geneva, Switzerland.

      ). To reach this goal all industries must reach net-zero emissions, particularly in developed countries, as soon as possible (

      Rogeli, J., D. Shindell, K. Jiang, S. Fifita, P. Forster, V. Ginzburg, C. Handa, H. Kheshgi, S. Kobayashi, E. Kriegler, L. Mundaca, R. Séférian, and M. V. Vilariño. 2018. Mitigation pathways compatible with 1.5°C in the context of sustainable development. In Global Warming of 1.5°C. An IPCC Special Report on the Impacts of Global Warming of 1.5°C Above Pre-Industrial Levels and Related Global Greenhouse Gas Emission Pathways, in the Context of Strengthening the Global Response to the Threat of Climate Change, Sustainable Development, and Efforts to Eradicate Poverty. V. Masson-Delmotte, P. Zhai, H.-O. Pörtner, D. Roberts, J. Skea, P. R. Shukla, A. Pirani, W. Moufouma-Okia, C. Péan, R. Pidcock, S. Connors, J. B. R. Matthews, Y. Chen, X. Zhou, M. I. Gomis, E. Lonnoy, T. Maycock, M. Tignor, and T. Waterfield, ed. World Meteorol. Org., Geneva, Switzerland.

      ). Methane production is a large component of the beef industry’s C footprint because it is a potent GHG with a GWP over a 100-yr time frame (GWP100) 28 times that of CO2 according to IPCC AR5 (

      IPCC. 2014. Climate Change 2014: Mitigation of Climate Change. Contribution of Working Group III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. O. Edenhofer, R. Pichs-Madruga, Y. Sokona, E. Farahani, S. Kadner, K. Seyboth, A. Adler, I. Baum, S. Brunner, P. Eickemeier, B. Kriemann, J. Savolainen, S. Schlömer, C. von Stechow, T. Zwickel and J. C. Minx, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). With a supporting population of approximately 32 million head of beef cows in the United States, and greater CH4 emission rates with high-forage diets compared with high-concentrate diets, this results in a C footprint that heavily favors intensive production systems, whereas cow-calf systems contribute 70 to 80% of total of the CO2 equivalents budget (
      • Alemu A.W.
      • Janzen H.
      • Little S.
      • Hao X.
      • Thompson D.J.
      • Baron V.
      • Iwaasa A.
      • Beauchemin K.A.
      • Kröbel R.
      Assessment of grazing management on farm greenhouse gas intensity of beef production systems in the Canadian Prairies using life cycle assessment..
      ;
      • Heflin K.R.
      • Parker D.B.
      • Marek G.W.
      • Auvermann B.W.
      • Marek T.H.
      Greenhouse-gas emissions of beef finishing systems in the southern High Plains..
      ;
      • Rotz C.A.
      • Asem-Hiablie S.
      • Place S.E.
      • Thoma G.
      Environmental footprints of beef cattle production in the United States..
      ). Therefore, the greatest emission reduction potential lies in reducing enteric CH4 emissions, especially from the cow herd (
      • Rotz C.A.
      • Asem-Hiablie S.
      • Place S.E.
      • Thoma G.
      Environmental footprints of beef cattle production in the United States..
      ). The importance of enteric CH4 from grazing ruminants in the biogenic C cycle, however, provides an additional layer of complexity in the discussion of enteric CH4 mitigation. In the United States, CH4 from ruminants has always been a large component of the C cycle during the transition from wild to farmed ruminants (
      • Kelliher F.M.
      • Clark H.
      Methane emissions from bison—An historic herd estimate for the North American Great Plains..
      ). Two studies examining pre-European enteric CH4 emissions from the large bison herds and other wild ruminants compared with modern-day farmed ruminants found that emission rates pre-European settlement were similar to modern emission rates (
      • Kelliher F.M.
      • Clark H.
      Methane emissions from bison—An historic herd estimate for the North American Great Plains..
      ;
      • Hristov A.N.
      Historic, pre-European settlement, and present-day contribution of wild ruminants to enteric methane emissions in the United States..
      ).
      The metrics being used when conducting current life cycle assessments and monitoring progress of mitigation are in continual discussion, and the benefits of reductions of short-lived pollutants, such as CH4, may be overstated because of this (
      • Pierrehumbert R.T.
      Short-lived climate pollution..
      ;
      • Allen M.R.
      • Shine K.P.
      • Fuglestvedt J.S.
      • Millar R.J.
      • Cain M.
      • Frame D.J.
      • Macey A.H.
      A solution to the misrepresentations of CO2-equivalent emissions of short-lived climate pollutants under ambitious mitigation..
      ). A carbon footprint represents the totality of emissions from a system, with different GHG contributions converted to a CO2-equivalents basis; this may be misrepresenting the burden of enteric CH4 (
      • Allen M.R.
      • Shine K.P.
      • Fuglestvedt J.S.
      • Millar R.J.
      • Cain M.
      • Frame D.J.
      • Macey A.H.
      A solution to the misrepresentations of CO2-equivalent emissions of short-lived climate pollutants under ambitious mitigation..
      ). Greenhouse gases are typically converted into CO2 equivalents using a GWP metric over varying time scales, and the time scale that is selected to calculate the equivalent metrics can have significant effect on the final computed C footprint (

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). For example, if GWP20 (meaning over a 20-yr time frame) is used, CH4 is considered 84 times more potent than CO2, but when this is expressed over 100-yr time frame, then the GWP falls to 28 (

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). The high heat-trapping potential increases with shorter time frames because CH4 is a short-lived pollutant with an atmospheric half-life of about 9 to 12 yr before being oxidized by hydroxy radicals, compared with CO2, which can remain in the atmosphere for thousands of years (

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ; Figure 1). This has led some to question the use of GWP100 and to suggest other metrics including global temperature potential and GWP*, although both are relatively new and lack policy influence (
      • Shine K.P.
      • Fuglestvedt J.S.
      • Hailemariam K.
      • Stuber N.
      Alternatives to the global warming potential for comparing climate impacts of emissions of greenhouse gases..
      ;
      • Allen M.R.
      • Shine K.P.
      • Fuglestvedt J.S.
      • Millar R.J.
      • Cain M.
      • Frame D.J.
      • Macey A.H.
      A solution to the misrepresentations of CO2-equivalent emissions of short-lived climate pollutants under ambitious mitigation..
      ). Using the GTP100 metric, CH4 is equal to just 4 times CO2, down from 28 using GWP100, but N2O only changes from 265 to 234 using GTP100 (

      IPCC. 2013. Climate Change 2013: The Physical Science Basis. Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. T. F. Stocker, D. Qin, G.-K. Plattner, M. Tignor, S. K. Allen, J. Boschung, A. Nauels, Y. Xia, V. Bex, and P. M. Midgley, ed. Cambridge Univ. Press, Cambridge, United Kingdom.

      ). The metric GWP* takes a slightly different approach to determine the effect of short-lived pollutants by equating a yearly 1-t increase in the rate of CH4 emission with a one-off pulse release of 100 × GWP100 tonne of CO2 (pulse release to calculate temperature effect of methane over 100 yr;
      • Allen M.R.
      • Shine K.P.
      • Fuglestvedt J.S.
      • Millar R.J.
      • Cain M.
      • Frame D.J.
      • Macey A.H.
      A solution to the misrepresentations of CO2-equivalent emissions of short-lived climate pollutants under ambitious mitigation..
      ). This allows CH4 to be considered on a decadal time scale, one that is more appropriate given its atmospheric lifetime. This may allow future models to more appropriately consider the behavior of CH4 in the atmosphere by allowing its warming potential to reach zero, which is not possible with CO2 due to its long atmospheric lifespan, unless sequestration is considered (
      • Allen M.R.
      • Shine K.P.
      • Fuglestvedt J.S.
      • Millar R.J.
      • Cain M.
      • Frame D.J.
      • Macey A.H.
      A solution to the misrepresentations of CO2-equivalent emissions of short-lived climate pollutants under ambitious mitigation..
      ). The implication, therefore, is that if cattle numbers remain static, there should be no increase in radiative forcing, and likewise, any decrease in cattle numbers or emission rate should actually have a cooling effect on a 100-yr time frame versus consistent radiative forcing during the same time.
      Livestock Environmental Assessment and Performance Partnership (

      FAO. 2016. Environmental Performance of Large Ruminant Supply Chains: Guidelines for Assessment Livestock Environmental Assessment and Performance Partnership. Food Agric. Org. United Nations, Rome, Italy.

      ), which standardizes life-cycle assessment modeling, requires IPCC Tier II or III calculations to compute enteric CH4 production (

      FAO. 2016. Environmental Performance of Large Ruminant Supply Chains: Guidelines for Assessment Livestock Environmental Assessment and Performance Partnership. Food Agric. Org. United Nations, Rome, Italy.

      ). Studies that use Tier II methods use a standard conversion factor for enteric CH4 production, 6.5% of GEI is lost as CH4 for grazing cattle and 3.5% of GEI for cattle on feedlot diets, which arise from studies that are not associated with normal grazing patterns and with nonrepresentative DMI based on the CH4 measurement techniques that were used traditionally. Research using new technologies, including the SF6 tracer technique and GEM, indicates that the conversion factor for grazing cattle may overestimate emissions in some systems (
      • Stackhouse-Lawson K.R.
      • Rotz C.A.
      • Oltjen J.W.
      • Mitloehner F.M.
      Carbon footprint and ammonia emissions of California beef production systems..
      ;
      • Chiavegato M.B.
      • Rowntree J.E.
      • Carmichael D.
      • Powers W.J.
      Enteric methane from lactating beef cows managed with high- and low-input grazing systems..
      ;
      • Stanley P.L.
      • Rowntree J.E.
      • Beede D.K.
      • DeLonge M.S.
      • Hamm M.W.
      Impacts of soil carbon sequestration on life cycle greenhouse gas emissions in midwestern USA beef finishing systems..
      ). Life cycle assessments conducted by
      • Stackhouse-Lawson K.R.
      • Rotz C.A.
      • Oltjen J.W.
      • Mitloehner F.M.
      Carbon footprint and ammonia emissions of California beef production systems..
      and
      • Stanley P.L.
      • Rowntree J.E.
      • Beede D.K.
      • DeLonge M.S.
      • Hamm M.W.
      Impacts of soil carbon sequestration on life cycle greenhouse gas emissions in midwestern USA beef finishing systems..
      using data collected for production systems in California and the upper Midwest, respectively, both indicated that the IPCC Tier II methods were overestimating emissions by up to 15%. With GHG monitoring technologies evolving rapidly to better sample the complex grazing environment where respiration chamber methods have limitations, more long-term monitoring studies and updated life-cycle assessment calculations are needed to improve the accuracy of the industry’s C footprint in grazing cattle systems.

      APPLICATIONS: CURRENT AND FUTURE

      Producer decisions affecting the soil–plant–animal interrelationships show promise in reducing the CH4 emission rates from cattle. Improving the quality of the forage base by incorporating high-quality, readily digestible forages and grazing strategies that improve the quality of the forage base, while potentially sacrificing short-term gains in animal performance, can result in the reduction of CH4 production. Additionally, mitigation tools such as lipid supplementation, supplementing Asparagopsis (seaweed), incorporating forages with beneficial secondary compounds, and genetic selection for reduced enteric CH4 production may be viable tools for beef producers to lower their C footprint. Improvements in grazing emission estimates and micrometeorological techniques also will give researchers better insights in future years on how animal management and grazing strategies affect whole-herd emissions and landscapes. In particular, as financial markets for C and ecosystem services develop over the coming decades, these landscape monitoring systems may serve an important role in the future of agriculture and allow producers to benefit from other ecosystem services they provide rather than just provisioning services. However, these systems must be cost effective, accurate, and precise for these services to be fairly compensated. Lastly, changing from the GWP100 system to GWP* may allow researchers to better understand the effects of short-lived pollutants on climate change and be an improved representation of how enteric CH4 production operates as part of the natural C cycle.

      ACKNOWLEDGMENTS

      The authors acknowledge that this work was partially funded by the Michigan Alliance for Animal Agriculture (East Lansing, MI; grant #AA18-027).

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