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Invited review: Enteric methane in dairy cattle production: Quantifying the opportunities and impact of reducing emissions

Open AccessPublished:April 18, 2014DOI:https://doi.org/10.3168/jds.2013-7234

      Abstract

      Many opportunities exist to reduce enteric methane (CH4) and other greenhouse gas (GHG) emissions per unit of product from ruminant livestock. Research over the past century in genetics, animal health, microbiology, nutrition, and physiology has led to improvements in dairy production where intensively managed farms have GHG emissions as low as 1 kg of CO2 equivalents (CO2e)/kg of energy-corrected milk (ECM), compared with >7 kg of CO2e/kg of ECM in extensive systems. The objectives of this review are to evaluate options that have been demonstrated to mitigate enteric CH4 emissions per unit of ECM (CH4/ECM) from dairy cattle on a quantitative basis and in a sustained manner and to integrate approaches in genetics, feeding and nutrition, physiology, and health to emphasize why herd productivity, not individual animal productivity, is important to environmental sustainability. A nutrition model based on carbohydrate digestion was used to evaluate the effect of feeding and nutrition strategies on CH4/ECM, and a meta-analysis was conducted to quantify the effects of lipid supplementation on CH4/ECM. A second model combining herd structure dynamics and production level was used to estimate the effect of genetic and management strategies that increase milk yield and reduce culling on CH4/ECM. Some of these approaches discussed require further research, but many could be implemented now. Past efforts in CH4 mitigation have largely focused on identifying and evaluating CH4 mitigation approaches based on nutrition, feeding, and modifications of rumen function. Nutrition and feeding approaches may be able to reduce CH4/ECM by 2.5 to 15%, whereas rumen modifiers have had very little success in terms of sustained CH4 reductions without compromising milk production. More significant reductions of 15 to 30% CH4/ECM can be achieved by combinations of genetic and management approaches, including improvements in heat abatement, disease and fertility management, performance-enhancing technologies, and facility design to increase feed efficiency and life-time productivity of individual animals and herds. Many of the approaches discussed are only partially additive, and all approaches to reducing enteric CH4 emissions should consider the economic impacts on farm profitability and the relationships between enteric CH4 and other GHG.

      Key words

      Introduction

      Methane and Greenhouse Gas Emissions

      Methane (CH4), carbon dioxide (CO2), nitrous oxide (N2O), and halocarbons are greenhouse gases (GHG) that enhance the effects of solar and thermal radiation on surface and atmospheric temperatures and are often expressed on a CO2-equivalent (CO2e) basis. Often, different and confusing bases are used in expressing the proportions of GHG and CH4 emissions from livestock agriculture (
      • Lassey K.R.
      Livestock methane emission and its perspective in the global methane cycle.
      ). Although enteric CH4 generated in the gastrointestinal tract of livestock is the single largest source of anthropogenic CH4 (Figure 1a), it is a lesser proportion of anthropogenic GHG emissions (Figure 1b). Methane has several natural sources (termites, wetlands, peat bogs, ocean sediments, and wildlife) and man-made sources (natural gas production, coal mining, wastewater treatment, landfills, and agriculture; Figure 1a;
      • Lassey K.R.
      Livestock methane emission and its perspective in the global methane cycle.
      ). Anthropogenic sources account for approximately 58% of total global CH4 emissions (Figure 1a;

      EPA (Environmental Protection Agency). 2010. Methane and Nitrous Oxide Emissions from Natural Sources. Publication 430-R-10-001. EPA, Washington, DC.

      ,

      EPA (Environmental Protection Agency). 2011a. DRAFT: Global Anthropogenic Non-CO2 Greenhouse Gas Emissions: 1990–2030. Publication 430-D-11-003. EPA, Washington, DC.

      ).
      Figure thumbnail gr1
      Figure 1(a) Estimated proportion of global CH4 emissions from natural and anthropogenic sources. Sources comprising 1% or less are not shown and include wild animals, wildfires, permafrost, and anthropogenic stationary and mobile sources. More uncertainty exists in estimates of CH4 emissions from natural than from anthropogenic sources [data from

      EPA (Environmental Protection Agency). 2010. Methane and Nitrous Oxide Emissions from Natural Sources. Publication 430-R-10-001. EPA, Washington, DC.

      ) and

      EPA (Environmental Protection Agency). 2011a. DRAFT: Global Anthropogenic Non-CO2 Greenhouse Gas Emissions: 1990–2030. Publication 430-D-11-003. EPA, Washington, DC.

      )]. (b) Global greenhouse gas (GHG) anthropogenic emissions by sector, with CH4 and N2O on a CO2-equivalent (CO2e) basis. Agriculture combined with land use change accounts for 22% of global greenhouse gas emissions. Deforestation accounts for 10.3% and fossil fuel utilization accounts for 1.4% of CO2 released; biogenic CO2 is not included [data from analysis by )]. (c) The 5 countries and regions with the largest livestock-associated enteric CH4 emissions on a million-metric-tonne (Mt)-of-CO2e basis. In the United States, 95% of enteric CH4 arises from ruminant livestock (

      EPA (Environmental Protection Agency). 2011b. Inventory of U. S. Greenhouse Gas Emissions and Sinks: 1990–2009. Publication 430-R-11–005. EPA, Washington, DC.

      ); this proportion can be assumed for other countries, although the contributions from beef versus dairy operations will vary. Manure CH4 is emitted by storage systems where anaerobic fermentation occurs. Manure CH4 and N2O can be from either ruminant or nonruminant livestock operations [data source:

      EPA (Environmental Protection Agency). 2011a. DRAFT: Global Anthropogenic Non-CO2 Greenhouse Gas Emissions: 1990–2030. Publication 430-D-11-003. EPA, Washington, DC.

      )]. EU 27 = European Union countries.
      In “Livestock’s Long Shadow,” the Food and Agriculture Organization of the United Nations (

      Steinfeld, H., P. Gerber, T. Wassenaar, V. Castel, M. Rosales, and C. de Haan. 2006. Livestock’s Long Shadow. Food and Agriculture Organization of the United Nations. Accessed Mar. 8, 2012. http://www.fao.org/docrep/010/a0701e/a0701e00.htm

      ) stated that global livestock agriculture was responsible for 18% of the anthropogenic GHG emissions annually. Since then, several groups have rebutted that report and provided reduced estimates of the impact of livestock agriculture on GHG emissions (
      • Pitesky M.E.
      • Stackhouse K.R.
      • Mitloehner F.M.
      Clearing the air: Livestock’s contribution to climate change.
      ;

      EPA (Environmental Protection Agency). 2011a. DRAFT: Global Anthropogenic Non-CO2 Greenhouse Gas Emissions: 1990–2030. Publication 430-D-11-003. EPA, Washington, DC.

      ;
      • Petherick A.
      Light is cast on a long shadow.
      ). Land use change (for example, converting forest or permanent pasture to annual crops) contributes a significant portion and, when combined with existing agriculture, accounts for 14 to 22% of global anthropogenic GHG emissions (Figure 1b;
      • Shafer S.R.
      • Walthall C.L.
      • Franzluebbers A.J.
      • Scholten M.
      • Meijs J.
      • Clark H.
      • Reisinger A.
      • Yagi K.
      • Roel A.
      • Slattery B.
      • Campbell I.D.
      • McConkey B.G.
      • Angers D.A.
      • Soussana J.F.
      • Richard G.
      Emergence of the global research alliance on agricultural greenhouse gases.
      ; ), although some analyses attribute little land use change to dairy production (
      • Gerber P.J.
      • Steinfeld H.
      • Henderson B.
      • Mottet A.
      • Opio C.
      • Dijkman J.
      • Falcucci A.
      • Tempio G.
      • et al.
      Tackling Climate Change through Livestock: A Global Assessment of Emissions and Mitigation Opportunities.
      ;
      • Golub A.A.
      • Henderson B.B.
      • Hertel T.W.
      • Gerber P.J.
      • Rose S.K.
      • Sohngen B.
      Global climate policy impacts on livestock, land use, livelihoods, and food security.
      ). Approximately 37% of global agricultural CH4 and N2O arise from direct animal and manure emissions, and the remainder is associated with cropping and deforestation (

      EPA (Environmental Protection Agency). 2011a. DRAFT: Global Anthropogenic Non-CO2 Greenhouse Gas Emissions: 1990–2030. Publication 430-D-11-003. EPA, Washington, DC.

      ). On a world-wide basis, dairy animals, including cull cows and beef cattle from dairy breeds, are estimated to contribute only 4% to anthropogenic GHG emissions (
      FAO (Food and Agriculture Organization of the United Nations)
      ). In many developed countries, the contribution of dairy production to GHG emissions is estimated even lower, due to the higher productivity of livestock agriculture, the dilution by emissions from other sectors, and lack of significant land use change (
      • Hagemann M.
      • Hemme T.
      • Ndambi A.
      • Alqaisi O.
      • Sultana M.N.
      Benchmarking of greenhouse gas emissions of bovine milk production systems for 38 countries.
      ). In the European Union 15, beef and dairy cattle are estimated to contribute 2.1 and 1.2%, respectively (

      EEA (European Environment Agency). 2011. Annual European Union greenhouse gas inventory 1990–2009 and inventory report 2011. European Environment Agency Technical report No. 2/2011. EEA, Copenhagen, Denmark.

      ), to anthropogenic GHG inventories, and in the United States, all livestock (including nonruminants) and dairy cattle are estimated to contribute 2.75 and 0.55%, respectively, to anthropogenic GHG emissions (

      EPA (Environmental Protection Agency). 2011b. Inventory of U. S. Greenhouse Gas Emissions and Sinks: 1990–2009. Publication 430-R-11–005. EPA, Washington, DC.

      ). However, in developed countries where pastoral agriculture is a significant portion of the economy (e.g., Ireland and New Zealand) or developing countries with large cattle populations (e.g., Brazil and India), ruminant livestock can be a very large contributor to the national GHG inventory (
      FAO (Food and Agriculture Organization of the United Nations)
      ).
      Examining CH4 emissions from livestock agriculture as a proportion of total anthropogenic GHG emissions in a given country or region can be misleading. Methane emissions are a function of the population of ruminant animals, their level of production, and the associated manure-handling systems. Thus, the countries or regions with the largest cattle populations in the world contribute the most to global agricultural CH4 emissions on a million-metric-tonne basis (metric tonnes of CO2e; Figure 1c). Why should the dairy industry in any country be concerned about CH4 emissions? First, international policy discussions have focused on non-CO2 emissions such as CH4 and N2O because they are less expensive to mitigate than CO2 emissions (

      EPA (Environmental Protection Agency). 2006. Global Mitigation of Non-CO2 Greenhouse Gases. Publication 430-R-06-005. EPA, Washington, DC.

      ;
      FAO (Food and Agriculture Organization of the United Nations)
      ;
      • Shafer S.R.
      • Walthall C.L.
      • Franzluebbers A.J.
      • Scholten M.
      • Meijs J.
      • Clark H.
      • Reisinger A.
      • Yagi K.
      • Roel A.
      • Slattery B.
      • Campbell I.D.
      • McConkey B.G.
      • Angers D.A.
      • Soussana J.F.
      • Richard G.
      Emergence of the global research alliance on agricultural greenhouse gases.
      ;
      • Gerber P.J.
      • Steinfeld H.
      • Henderson B.
      • Mottet A.
      • Opio C.
      • Dijkman J.
      • Falcucci A.
      • Tempio G.
      • et al.
      Tackling Climate Change through Livestock: A Global Assessment of Emissions and Mitigation Opportunities.
      ). Often, CH4 mitigation approaches can be economically advantageous as well as environmentally beneficial. Second, because the CO2 emitted by livestock, including dairy cattle, arises from metabolism of plant-derived feedstuffs, it is viewed as part of a continuous biological cycle of fixation, utilization, and exhalation. Accordingly, it is defined as biogenic CO2 and livestock are considered to be a zero net source of CO2 (
      • Pitesky M.E.
      • Stackhouse K.R.
      • Mitloehner F.M.
      Clearing the air: Livestock’s contribution to climate change.
      ). Third, enteric and manure CH4 comprise more than 40% of the GHG emissions associated with fluid milk production in the United States (
      • Thoma G.
      • Popp J.
      • Nutter D.
      • Shonnard D.
      • Ulrich R.
      • Matlock M.
      • Kim D.S.
      • Neiderman Z.
      • Kemper N.
      • East C.
      • Adom F.
      Greenhouse gas emissions from milk production and consumption in the United States: A cradle-to-grave life cycle assessment circa 2008.
      ). Last, some retailers and consumers in both domestic and international markets are concerned about the contribution of GHG emissions to the carbon footprint of foods. Ruminant livestock will play a crucial role in future global food security because far more grazing land exists, unusable for human food, than cropping land (
      • Gill M.
      • Smith P.
      • Wilkinson J.M.
      Mitigating climate change: the role of domestic livestock.
      ) and ruminant animals can transform pasture into high-quality human food. Ruminants also are very capable of converting the human-inedible by-products of food production into high-quality human food. If mitigation strategies are implemented that reduce GHG but also reduce production output, then the environmental benefits would be at least partly negated by increased food costs or reduced supply of animal-based foods.
      Enteric CH4 comprises 17 and 3.3% of global CH4 and GHG emissions, respectively, and is largely derived from ruminant livestock (Figures 1a and 1b). Manure CH4 from both ruminant and nonruminant livestock contributes 2 and 0.4% of global CH4 and GHG emissions, respectively (Figures 1a and 1b). Several country and regional GHG inventories do not differentiate between ruminant and nonruminant livestock production systems with regard to manure GHG emissions. Manure CH4 emissions are a larger proportion of total farm CH4 emissions in intensively managed dairy operations with manure storage systems, and much lower in extensive or grazing operations (Figure 1c). Manure N2O emissions contribute <1% of global GHG emissions (). Significant interrelationships exist between enteric CH4 and manure CH4 and N2O emissions, and accordingly, mitigation approaches targeted at reducing enteric CH4 must consider the effect on manure CH4 and N2O emissions. Because of the larger contribution of enteric CH4 than manure CH4 and N2O in dairy production to agricultural GHG emissions, this review focuses on enteric CH4. Readers are referred to
      • Gerber P.J.
      • Steinfeld H.
      • Henderson B.
      • Mottet A.
      • Opio C.
      • Dijkman J.
      • Falcucci A.
      • Tempio G.
      • et al.
      Tackling Climate Change through Livestock: A Global Assessment of Emissions and Mitigation Opportunities.
      ) and
      • Hristov A.N.
      • Oh J.
      • Lee C.
      • Meinen R.
      • Montes F.
      • Ott T.
      • Firkins J.
      • Rotz A.
      • Dell C.
      • Adesogan A.
      • Yang W.
      • Tricarico J.
      • Kebreab E.
      • Waghorn G.
      • Dijkstra J.
      • Oosting S.
      • et al.
      Mitigation of greenhouse gas emissions in livestock production: A review of technical options for non-CO2 emissions.
      ) for an integrated discussion of enteric and manure GHG emissions and mitigation opportunities from ruminant livestock.
      This review will provide a broad, integrated view of CH4 mitigation opportunities in dairy production for agricultural students and scientists. The objectives are to (1) evaluate options that have been demonstrated to mitigate enteric CH4 emissions from dairy cattle on a quantitative basis and in a sustained manner; (2) integrate approaches in genetics, feeding and nutrition, physiology, and health to emphasize why herd productivity, not individual animal productivity, is important to environmental sustainability; and (3) provide perspective on the relative contribution of enteric CH4 emissions from dairy production to global GHG emissions. The majority of the research presented was conducted under intensive management conditions in temperate climates. In principle, the approaches discussed can be applied to any dairy production system because their aim is increasing productivity at the herd level. Enteric CH4 per unit of ECM (g of CH4/kg of ECM) will be the evaluation basis for 2 reasons. First, dairy farmers will not be willing to implement CH4 mitigation strategies if they decrease milk production, for which farmers are not compensated. Second, as the world population continues to grow during this century, agriculture must focus on production efficiency to provide an adequate food supply, and milk and dairy foods are an important source of calories as well as protein and micronutrients. Thus, enteric CH4 emissions per unit of ECM (CH4/ECM) is the correct and most useful basis biologically, nutritionally, environmentally, and economically. Some of the mitigation approaches can be readily implemented at this time, and others need short-term development (2 to 5 yr). In vitro studies are presented where appropriate, but the focus of this article is in vivo research. Although in vitro studies are a valuable way to test ideas, in vivo experiments are imperative for obtaining quantitative results that capture the complexity and dynamics of ruminant digestion and metabolism and the consequences on lactation performance.
      To identify effective mitigation strategies, accurate and repeatable measurement techniques are required. Several direct and indirect methods have been used to quantify CH4 emissions in vivo, many of which were reviewed by
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ),
      • Kebreab E.
      • Clark K.
      • Wagner-Riddle C.
      • France J.
      Methane and nitrous oxide emissions from Canadian animal agriculture: A review.
      ), and
      • Storm I.M.L.D.
      • Hellwing A.L.F.
      • Nielsen N.I.
      • Madsen J.
      Methods for measuring and estimating methane emissions from ruminants.
      ), including their advantages, disadvantages, and limitations. The most common in vivo measurement techniques are respiration calorimetry (either closed or open-circuit), polyethylene tunnel system, isotope dilution, tracer gas [i.e., sulfur hexafluoride (SF6)], and micrometeorological mass balance (
      • Kebreab E.
      • Clark K.
      • Wagner-Riddle C.
      • France J.
      Methane and nitrous oxide emissions from Canadian animal agriculture: A review.
      ). New technologies are also being developed to assess CH4 concentrations on an hourly basis using rumen sensors (
      • Laporte-Uribe J.
      • Gibbs S.J.
      Real time in situ measurement of rumen methane concentration in the rumen of cattle.
      ) or in commercial operations by measuring CH4 eructated during eating in robotic milking stations or at pasture feeders (
      • Utsumi S.
      • Beede D.
      • Zimmerman S.
      • Zimmerman P.
      Whole herd enteric methane emission estimates in three contrasting dairy systems.
      ). Comparisons of the measurement techniques have identified systematic differences (
      • Kebreab E.
      • Clark K.
      • Wagner-Riddle C.
      • France J.
      Methane and nitrous oxide emissions from Canadian animal agriculture: A review.
      ;
      • Muñoz C.
      • Yan T.
      • Wills D.A.
      • Murray S.
      • Gordon A.W.
      Comparison of the sulfur hexafluoride tracer and respiration chamber techniques for estimating methane emissions and correction for rectum methane output from dairy cows.
      ). Respiration chambers remain the gold standard in research settings that permit animal confinement. Improvement of the other existing methodologies or development of new methodologies that allow for repeatable, accurate CH4 emission measurements from groups of animals or in different housing situations is critical in evaluating mitigation strategies.

      Rumen Function: Ecology and Biochemistry

      Ruminant animals and microbes have evolved together, filling a niche based on the conversion of complex plant carbohydrates to energy that is beneficial to both the host animal and the microbial symbionts. The microbes include bacteria, protozoa, fungi, and Archaea (Figure 2). The rumen ecosystem is an anaerobic environment, in which the degradation of plant material occurs in a very short time frame compared with other anaerobic ecosystems such as wetlands and estuaries, and the fermentation products are different. Some of the microbial species have coevolved with ruminants and hindgut-fermenting mammals and do not exist in any other environment (e.g., rumen protozoa). Also, the methanogens of ruminants and other mammalian herbivores are distinct from methanogens in other environments. To date, 3 major genera and 3 minor genera of methanogens belonging to the Archaea domain have been identified, although it is likely that more exist (
      • Wright A.-D. G.
      • Toovey A.F.
      • Pimm C.L.
      Molecular identification of methanogenic Archaea from sheep in Queensland, Australia reveal more uncultured novel Archaea.
      ;
      • Janssen P.H.
      • Kirs M.
      Structure of the archaeal community of the rumen.
      ;
      • Liu Y.
      • Whitman W.B.
      Metabolic, phylogenetic, and ecological diversity of the methanogenic Archaea.
      ;
      • Kong Y.
      • Xia Y.
      • Seviour R.
      • Forster R.
      • McAllister T.A.
      Biodiversity and composition of methanogenic populations in the rumen of cows fed alfalfa hay or triticale straw.
      ;
      • Poulsen M.
      • Schwab C.
      • Jensen B.B.
      • Engberg R.M.
      • Spang A.
      • Canibe N.
      • Højberg O.
      • Milinovich G.
      • Fragner L.
      • Schleper C.
      • Weckwerth W.
      • Lund P.
      • Schramm A.
      • Urich T.
      Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen.
      ). Only 8 methanogen species have been cultured (
      • Kong Y.
      • Xia Y.
      • Seviour R.
      • Forster R.
      • McAllister T.A.
      Biodiversity and composition of methanogenic populations in the rumen of cows fed alfalfa hay or triticale straw.
      ) and the total number of rumen archaeal species is unknown (
      • Janssen P.H.
      • Kirs M.
      Structure of the archaeal community of the rumen.
      ), but has been estimated to be approximately 360 to 1,000 on an operational taxonomic unit basis (
      • Kim M.
      • Morrison M.
      • Yu Z.
      Status of the phylogenetic diversity census of ruminal microbiomes.
      ;
      • Kong Y.
      • Xia Y.
      • Seviour R.
      • Forster R.
      • McAllister T.A.
      Biodiversity and composition of methanogenic populations in the rumen of cows fed alfalfa hay or triticale straw.
      ). Methanogens are found in the hindgut as well as the rumen, although the population structure, ecology, and microbial metabolism differ between the 2 compartments.
      Figure thumbnail gr2
      Figure 2Rumen microorganisms, including bacteria, protozoa, and fungi, ferment carbohydrates to obtain energy and generate significant amounts of reducing equivalents (FADH2, NADH, and others) in the process and VFA (not shown) and H2 as end products. Methanogens, both free living and endosymbionts inside protozoa, convert H2 to CH4. A small amount of reducing equivalents are utilized in lipid synthesis and FA biohydrogenation. Synthesis of amino acids can result in production or utilization of reducing equivalents, but the net amount is small. Protein synthesis utilizes reducing equivalents. Elevated concentrations of H2 inhibit carbohydrate fermentation, providing a negative feedback mechanism. Organisms are not drawn to scale [after
      • Czerkawski J.W.
      )].
      In the reticulorumen and hindgut, simple and complex carbohydrates are hydrolyzed to 5- and 6-carbon sugars by microbial enzyme activity. Sugars are fermented to VFA through multiple-step pathways that produce reducing equivalents (i.e., metabolic hydrogen), which can be summarized in the following equations (
      • Hungate R.E.
      ;
      • Czerkawski J.W.
      ;
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      ):
      Glucose2pyruvate+4H(carbohydratemetabolism);
      [1]


      Pyruvate+4Hacetate+CO2+2H;
      [2]


      Pyruvate+4Hpropionate+H2O;
      [3]


      2acetate+4Hbutyrate+2H2O.
      [4]


      The metabolic hydrogen is converted to H2 by hydrogenase-expressing bacterial species, and the H2 converted to CH4 by Archaea in the combined reaction:
      CO2+8HCH4+2H2O (methanogenesis).
      [5]


      Dissolved H2 inhibits ruminal fermentation pathways through negative feedback mechanisms, and if not removed by the methanogens, will reduce the overall extent of carbohydrate degradation, the rate of microbial growth, and the synthesis of microbial protein (
      • Wolin M.J.
      Metabolic interactions among intestinal microorganisms.
      ;
      • McAllister T.A.
      • Newbold C.J.
      Redirecting rumen fermentation to reduce methanogenesis.
      ). Biohydrogenation of FA provides an alternative hydrogen sink to methanogenesis (Figure 2). Degradation of dietary protein and assimilation into microbial protein can result in either a net consumption or net production of hydrogen (Figure 2;
      • Hungate R.E.
      ;
      • Czerkawski J.W.
      ). Additionally, previously unknown methanogens of the order Thermoplasmatales that use methyl groups rather than H2 have been recently identified in the rumen (
      • Poulsen M.
      • Schwab C.
      • Jensen B.B.
      • Engberg R.M.
      • Spang A.
      • Canibe N.
      • Højberg O.
      • Milinovich G.
      • Fragner L.
      • Schleper C.
      • Weckwerth W.
      • Lund P.
      • Schramm A.
      • Urich T.
      Methylotrophic methanogenic Thermoplasmata implicated in reduced methane emissions from bovine rumen.
      ). This group and other unidentified organisms may help explain the lack of predictability in the effects of various rumen manipulations that has been observed in the past.
      As a consequence of the complex H2 and methyl group metabolism in the reticulorumen, changes in pathways leading to VFA production, biohydrogenation, microbial N metabolism, and microbial growth will alter the amount of CH4 produced (Figure 2). These changes are dynamic functions of both microbial populations (species, abundance, and activity of microbes) and which pathways are being utilized, which contributes to the complexity and difficulty of predicting CH4 emissions and developing mitigation strategies.

      Methane Mitigation Strategies

      An abundance of CH4 mitigation strategies have been studied and they can be classified into 3 broad categories:
      • 1.
        Feeds, feeding management, and nutrition: feeding good-quality feeds can increase animal productivity and feed efficiency. Certain feeds can enhance propionate or decrease acetate production (Equations 2 and 3), decreasing H2 that would be converted to CH4.
      • 2.
        Rumen modifiers: feeding specific substances that directly or indirectly inhibit methanogenesis or using biological control (defaunation, bacteriocins, bacteriophages, and immunization) directed at reducing methanogens.
      • 3.
        Increasing animal production through genetics and other management approaches: improving nutrient utilization for productive purposes to dilute out maintenance on an individual animal or a herd basis, increasing feed efficiency and decreasing CH4 per unit of product (meat or milk). Total CH4 emissions will be decreased if annual production of milk remains constant and fewer cows are needed to produce the same amount of milk.
      Although dairy cows are of primary concern, studies using other ruminant animals (sheep, goats, or beef cattle) are included as appropriate for reference. Many of the principles behind CH4 reduction can be generalized to include all ruminants. However, the right mitigation approach must be adapted to the specific needs of the farmers and animals. Although the majority of the CH4 mitigation approaches discussed were studied with animals in confinement housing and fed feeds grown in temperate climates, with appropriate consideration of the underlying biology, their application can be extended to other production systems. Most importantly, mitigation strategies should be cost effective or cost neutral if we expect farmers to adopt the changes.

      Feeds, Feeding Management, and Nutrition

      Nutritional mitigation of CH4 production is founded on 3 basic approaches: (1) ingredient selection to alter VFA production patterns; (2) increased rate of passage, which can alter microbial populations and VFA production patterns and shift some digestion to the intestines; and (3) feeding better-quality diets to increase milk production per cow, which will dilute the CH4 cost associated with maintenance energy requirements.
      Feed ingredients provide the substrates for microbial fermentation, and differences in feed digestibility and chemical composition alter the amount of energy extracted by the microbes and the patterns of VFA and CH4 produced. The proportions of VFA affect the amount of CH4 produced, because propionate formation consumes reducing equivalents, whereas acetate and butyrate formation generate H2 for methanogenesis (
      • Hungate R.E.
      ). As such, any dietary component or intervention that causes a shift in favor of propionate production will be accompanied by a reduction in CH4 production per unit of feed fermented, whereas the opposite is true for acetate and butyrate (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ). Rumen protein degradation and assimilation into microbial protein can result in either a net consumption or net production of H2 (Figure 2;
      • Hungate R.E.
      ;
      • Czerkawski J.W.
      ). Biohydrogenation of FA will result in a net consumption of H2 (Figure 2). Consequently, variations in rumen N metabolism and biohydrogenation will cause alterations in CH4 production, and because carbohydrate and protein substrates are also used for microbial maintenance and growth, theoretical predictions of VFA patterns and CH4 formation do not always correlate to in vitro and in vivo observations (
      • Hironaka R.
      • Mathison G.W.
      • Kerrigan B.K.
      • Vlach I.
      The effect of pelleting of alfalfa hay on methane production and digestibility by steers.
      ).
      Passage rate also affects the extent of digestion and patterns of VFA formation as well as microbial growth rates and has been found to explain 28% of the variation in CH4 emissions (
      • Okine E.K.
      • Mathison G.W.
      • Hardin R.T.
      Effects of changes in frequency of reticular contractions on fluid and particulate passage rates in cattle.
      ). Faster passage of feed material out of the rumen means a lower extent of rumen fermentation and possibly less CH4 production per unit of feed, depending on whether the feed nutrients are digested in the small intestine (sugars and starches) or fermented in the hindgut (pectin, glucans, and NDF). Increased passage rates also increase microbial energy requirements because cells have to divide more frequently to maintain rumen populations.
      High-quality (more energy-dense or more digestible) diets provide more energy for production as a proportion of the gross energy intake (GEI) and dilute the costs of maintenance than low-quality diets; therefore less CH4/ECM is generated (Figure 3). More energy-dense diets usually contain higher proportions of starch relative to NDF, and less CH4 is produced per unit of starch digested than NDF (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ). These diets also can increase net energy intake and if the net energy is partitioned to milk, it will decrease CH4/ECM production. However, reducing enteric CH4 has a small effect on animal energetics. For a cow producing 30 kg of ECM and 450 g of CH4 per day, a 15% reduction in CH4/ECM would provide an additional 0.9 Mcal/d to an estimated ME intake of 53 to 57 Mcal/d, assuming that digestibility is not affected.
      Figure thumbnail gr3
      Figure 3(a) Energy-corrected milk yield (dashed line) increases more rapidly than CH4 production (solid line) with increasing DMI, resulting in less enteric CH4 emissions per unit of ECM (CH4/ECM; dotted line). (b) Corresponding decreases in CH4 as a proportion of gross energy intake [GEI; g of CH4/kg of GEI (Ym; CH4/GEI); dashed + dotted line] are predicted. Predictions are based on a model that accounts for the effects of DMI on starch and NDF digestibility, as described in the text. Note that although the methane production functions CH4/ECM and CH4/GEI appear linear over the range shown, they are in fact curvilinear, decreasing with increasing intakes.
      These alterations in digestibility, proportions of VFA produced, and microbial growth affect energy and protein availability to the cow and, ultimately, the efficiency at which the feed nutrients are used for productive functions, including growth and milk synthesis (
      NRC
      ). Based on these 3 principles, CH4 emissions can be affected by the level of feed intake, type of carbohydrate, forage quality and species, physical processing, forage preservation, and feeding frequency (Table 1).
      Table 1Summary of feeding management approaches to altering rumen fermentation and reducing CH4 emissions per unit of ECM
      Many of the biological effects are interrelated and interdependent and, accordingly, the changes in enteric CH4 emissions per unit of ECM (CH4/ECM) are not likely to be additive. Expected decreases in CH4/ECM range from 0 to 15%. These changes are modest because the range of alterations was restricted to what might reasonably be implemented or occur in commercial dairy production without compromising milk yield significantly (except as noted for rumen pH) compared with previously published reviews where the manipulations ranged from all-forage to all-concentrate diets for nonlactating and lactating animals. Manipulations that alter carbohydrate digestibility and thus energy availability will affect milk yield as well as CH4 emissions.
      Feeding alterationCH4/ECMAssumption(s) and comments
      Increased DMIDecreased 2 to 6% for each kilogram increase in DMI(a) Increased fill; (b) increased rate of solids passage; (c) decreased rumen NDF digestibility will be compensated by increased hindgut NDF digestibility; (d) decreased rumen starch digestibility; (e) increased starch digestion in small intestine; (f) no difference in total-tract starch digestion; (g) increased production
      Decreased forage particle sizeNeutral(a) Increased passage of forage particles from the rumen; (b) decreased rumen NDF digestibility will be compensated by increased hindgut NDF digestibility
      Grain processingDecreased 1 to 2.5% with 5% increase in apparent total-tract starch digestibility(a) Decreased grain particle passage from rumen; (b) increased VFA yield with increased proportion of propionate; (c) no increase in intake of digestible DM (which may or may not be true)
      Rumen pH <5.5Decreased 15 to 20%(a) Decreased rumen NDF digestibility not fully compensated for by hindgut fermentation; (b) assumes 50% reduction in apparent total-tract NDF digestibility; (c) milk yield reduced 10 to 15%; (d) no change in rumen starch digestibility and no effect on DMI
      Increased concentrate feedingDecreased 2% for every 1% increase in ration NFC; maximum reduction ~15%(a) Effects manifested by less NDF fermented in total tract, shift of starch digestion from rumen to small intestine, and possibly lower rumen pH; (b) potential to increase intake; (c) higher proportions of propionate
      Increased forage quality achieved by better management of harvesting and storage or pasture managementDecreased up to 5% with a 5 percentage unit increase in apparent total-tract NDF digestibility(a) Increased yield of VFA (energy) is greater than increases in CH4; (b) increased milk yield
      Forage type/strain selection and genetics (e.g., brown midrib corn)Decreased 0 to 4%Improvements in digestibility lead to increased DMI, energy availability, and milk yields
      Lipid feedingDecreased 5% per unit of ether extract in rationPotential for (a) decreased DMI, (b) decreased NDF digestibility, (c) decreased lactation performance, and (d) decreased milk components
      1 Many of the biological effects are interrelated and interdependent and, accordingly, the changes in enteric CH4 emissions per unit of ECM (CH4/ECM) are not likely to be additive. Expected decreases in CH4/ECM range from 0 to 15%. These changes are modest because the range of alterations was restricted to what might reasonably be implemented or occur in commercial dairy production without compromising milk yield significantly (except as noted for rumen pH) compared with previously published reviews where the manipulations ranged from all-forage to all-concentrate diets for nonlactating and lactating animals. Manipulations that alter carbohydrate digestibility and thus energy availability will affect milk yield as well as CH4 emissions.

      Level of Intake, Digestibility, and Passage

      Many studies have found that variation in DMI accounts for 52 to 64% of the variation in CH4 production on a per day basis when cattle were fed ad libitum (
      • 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.
      ;
      • Pinares-Patiño C.S.
      • Waghorn G.C.
      • Machmüller A.
      • Vlaming B.
      • Molano G.
      • Cavanagh A.
      • Clark H.
      Methane emissions and digestive physiology of non-lactating dairy cows fed pasture forage.
      ;
      • Hammond K.J.
      • Muetzel S.
      • Waghorn G.C.
      • Pinares-Patino C.S.
      • Burke J.L.
      • Hoskin S.O.
      The variation in methane emissions from sheep and cattle is not explained by the chemical composition of ryegrass.
      ). To account for the effects of DMI on digestibility, a static model was developed based on reductions in starch digestibility (
      • Firkins J.L.
      • Eastridge M.L.
      • St-Pierre N.R.
      • Noftsger S.M.
      Effects of grain variability and processing on starch utilization by lactating dairy cattle.
      ) and NDF digestibility (
      • Huhtanen P.
      • Rinne M.
      • Nousiainen J.
      A meta-analysis of feed digestion in dairy cows. 2. The effects of feeding level and diet composition on digestibility.
      ) with increasing DMI and using CH4 prediction equations based on digestible carbohydrate fractions (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ). Dry matter intake was predicted from milk yield and composition using the dairy
      NRC
      ) model, and results for a 680-kg lactating cow consuming a ration with 50% forage, 30% NDF, and 25% starch are shown in Figure 3. Total CH4 production (g or Mcal/d) increases with increasing DMI because there is more feed to be fermented (Figure 3a). However, CH4 as a proportion of DMI or GEI (g of CH4/kg of GEI) usually decreases as DMI increases above maintenance (
      • Blaxter K.L.
      • Clapperton J.L.
      Prediction of the amount of methane produced by ruminants.
      ;
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ;
      • Pinares-Patiño C.S.
      • Waghorn G.C.
      • Hegarty R.S.
      • Hoskin S.O.
      Effects of intensification of pastoral farming on greenhouse gas emissions in New Zealand.
      ) and is related to decreases in DM digestibilities observed at higher intakes and the associated increases in passage rates (Figure 3b). The relationship between CH4 emitted (kg/d or Mcal/d) and DMI or GEI is not constant, but decreases as intake increases. Accordingly, CH4/ECM decreases with increasing DMI and milk yield (Figure 3a). For example, a cow producing 30 kg of milk/d and consuming a 50% forage and 50% concentrate ration is predicted to emit 12.7 g of CH4/kg of ECM compared with a cow producing 35 kg of milk/d with the same diet, emitting 11.9 g of CH4/kg of ECM.
      Whereas digestibility was estimated to decrease 4.6% per multiple of maintenance in the older literature (
      • Tyrell H.F.
      • Moe P.W.
      Effect of intake on digestive efficiency.
      ), under current feeding situations with better-quality forages and improved feeding management, digestibility depression is probably <2 or 3% per multiple of maintenance (
      • Vandehaar M.J.
      Efficiency of nutrient use and relationship to profitability on dairy farms.
      ;
      • Sauvant D.
      • Giger-Reverdin S.
      Modélisation des ineractions digestives et de la production de méthane chez les ruminants.
      ). Also, it is possible that genetic selection for higher milk yields in dairy cattle has been accompanied by increased digestive capacity. No definitive research is available on whether the increased capacity is due to increases in rumen or total gastrointestinal tract volume, absorptive surface, changes in host-microbe interactions, or combinations of these effects. In dairy cattle diets, most of the decrease in DM digestibility observed as intake increases is associated with a decrease in total-tract NDF digestibility, but not total-tract starch digestibility (
      • Huhtanen P.
      • Rinne M.
      • Nousiainen J.
      A meta-analysis of feed digestion in dairy cows. 2. The effects of feeding level and diet composition on digestibility.
      ), although starch digestion will be shifted from the rumen to the small intestine (
      • Firkins J.L.
      • Eastridge M.L.
      • St-Pierre N.R.
      • Noftsger S.M.
      Effects of grain variability and processing on starch utilization by lactating dairy cattle.
      ).
      • Huhtanen P.
      • Rinne M.
      • Nousiainen J.
      A meta-analysis of feed digestion in dairy cows. 2. The effects of feeding level and diet composition on digestibility.
      ) predicted that for every kilogram increase in DMI, total-tract NDF digestibility is reduced 0.485 ± 0.143% for grass silages. Whether a similar reduction may be observed with NDF digestibility in legume or corn silages with increasing DMI is not known, but is presumed to be different. Assuming unchanged patterns of fermentation, the reduction in total-tract NDF digestibility with increasing DMI of the same diet will result in a proportional reduction in CH4 emissions on a per-head-per-day basis.
      Methane emission would also be expected to be affected by depression of ruminal starch digestibility with increasing intakes. Apparent ruminal starch digestibility was found to decrease linearly with increasing DMI by 1.21 ± 0.59%/kg of DMI (
      • Firkins J.L.
      • Eastridge M.L.
      • St-Pierre N.R.
      • Noftsger S.M.
      Effects of grain variability and processing on starch utilization by lactating dairy cattle.
      ). When ruminal starch digestibility is decreased, the majority of the starch passing out of the rumen will be digested in the small intestine rather than being fermented in the hindgut (
      • Firkins J.L.
      • Eastridge M.L.
      • St-Pierre N.R.
      • Noftsger S.M.
      Effects of grain variability and processing on starch utilization by lactating dairy cattle.
      ;
      • Huntington G.B.
      • Harmon D.L.
      • Richards C.J.
      Sites, rates, and limits of starch digestion and glucose metabolism in growing cattle.
      ). In theory, intestinal digestion of starch should be more energetically favorable to the animal than ruminal fermentation to VFA, but in practice, no difference in energy availability has been demonstrated between the two (
      • Huntington G.B.
      • Harmon D.L.
      • Richards C.J.
      Sites, rates, and limits of starch digestion and glucose metabolism in growing cattle.
      ). With lower ruminal digestibility of NDF, more NDF will pass out of the rumen and be passed to the hindgut, where it can be fermented and produce CH4. Although the decrease in total-tract NDF digestibility with increasing DMI is less than the decrease in ruminal starch digestibility, in terms of CH4 production, the impact on NDF digestibility is expected to be larger because fermentation of hemicellulose and cellulose results in 2 to 5 times more CH4 than fermentation of NFC (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ). The quantitative extent of the decrease in CH4 emission with increasing DMI will depend on the proportions of starch and NDF in the diet and the proportions of cellulose and hemicellulose in the forages (legumes vs. grasses; further discussion in the next section).
      Typically, the rate of passage increases with increasing DMI, decreasing the extent of ruminal degradation of the OM (
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ). Associated CH4 losses decrease by 0.77 to 1.6% GEI for each multiple or unit increase of intake (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ;
      • Beauchemin K.
      • McGinn S.
      Enteric methane emissions from growing beef cattle as affected by diet and level of intake.
      ;
      • Sauvant D.
      • Giger-Reverdin S.
      Modélisation des ineractions digestives et de la production de méthane chez les ruminants.
      ). The dairy NRC model (
      NRC
      ) models the decrease in digestibility with increasing intake using the same discount factor for all feed nutrients (NDF, NFC, and CP). To account for the observation that the digestibility of all feed components are not equally depressed with increasing DMI, models are needed that allow for variable digestibility discount factors by individual nutrients. Also, interactions between intake level and diet composition exist in CH4 as a proportion of gross energy (
      • Sauvant D.
      • Giger-Reverdin S.
      Modélisation des ineractions digestives et de la production de méthane chez les ruminants.
      ). The relationships between digestibility, passage, and DMI are complex and have a major impact on rumen production of CH4. Both the rate and the extent of rumen carbohydrate digestion determine the amount of CH4 produced and the energy available for milk synthesis.

      Type of Carbohydrates

      Greater DMI with greater milk yields and lesser CH4 yields are often achieved by feeding more digestible carbohydrates. The relative proportion of fermentation end products in the rumen, especially the VFA, is influenced by the proportion of NDF versus NFC in the ration (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ;
      • Murphy M.R.
      • Baldwin R.L.
      • Koong L.J.
      Estimation of stoichiometric parameters for rumen fermentation of roughage and concentrate diets.
      ;
      • Sutton J.D.
      • Dhanoa M.S.
      • Morant S.V.
      • France J.
      • Napper D.J.
      • Schuller E.
      Rates of production of acetate, propionate, and butyrate in the rumen of lactating dairy cows given normal and low-roughage diets.
      ;
      • Bannink A.
      • Kogut J.
      • Dijkstra J.
      • France J.
      • Kebreab E.
      • Van Vuuren A.M.
      • Tamminga S.
      Estimation of the stoichiometry of volatile fatty acid production in the rumen of lactating cows.
      ). Forage-based diets high in cellulose, hemicellulose, and lignin favor production of acetate and butyrate (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ), whereas starch-based diets favor propionate production (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ). Soluble sugars tend to stimulate greater proportions of butyrate and also increase fiber digestibility (
      • Hindrichsen I.K.
      • Wettstein H.-R.
      • Machmüller A.
      • Jörg B.
      • Kreuzer M.
      Effect of the carbohydrate composition of feed concentrates on methane emission from dairy cows and their slurry.
      ). However, selecting ryegrass forage for increased soluble carbohydrates did not reduce CH4/ECM due to reduced NDF digestibility that negatively affected milk yield (
      • Staerfl S.M.
      • Amelchanka S.L.
      • Kälber T.
      • Soliva C.R.
      • Kreuzer M.
      • Zeitz J.O.
      Effect of feeding dried high-sugar ryegrass (‘AberMagic’) on methane and urinary nitrogen emissions of primiparous cows.
      ). In contrast, increasing NFC by altering the nonforage portion of the ration from 32 to 53% with corn grain, soybean meal, and whole roasted soybeans decreased CH4/ECM by 20% in early-lactation cows (
      • Aguerre M.J.
      • Wattiaux M.A.
      • Powell J.M.
      • Broderick G.A.
      • Arndt C.
      Effect of forage-to-concentrate ratio in dairy cow diets on emission of methane, carbon dioxide, and ammonia, lactation performance, and manure excretion.
      ).
      Neutral detergent fiber is heterogeneous with respect to chemical composition, digestibility, and potential to produce CH4. The highly digestible NDF in brewers and distillers by-products produces half to one-third of the CH4 per kilogram of DM digested in vitro compared with forages with similar DM digestibilities (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ). Given that distillers and brewers grains have high hemicellulose:cellulose ratios (1.5 to 1.6:1) compared with grasses (0.67:1) and legumes (0.35:1), this observation fits well with the
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ) equation, where digested hemicellulose produces only 37% CH4 relative to digested cellulose. Cows fed increasing amounts of dried distillers grains with solubles that replaced corn and soybean meal emitted less CH4 (g/d) and CH4/ECM (
      • Benchaar C.
      • Hassanat F.
      • Gervais R.
      • Chouinard P.Y.
      • Julien C.
      • Petit H.V.
      • Massé D.I.
      Effects of increasing amounts of corn dried distillers grains with solubles in dairy cow diets on methane production, ruminal fermentation, digestion, N balance, and milk production.
      ). In that study, changes in carbohydrate sources were confounded by treatment changes in diet lipid content sulfur intakes, and DMI. Tropical grasses (C4) tend to be less digestible than temperate (C3) forages due to their higher NDF content and greater lignification, and produce more CH4 per unit of intake (
      • Pinares-Patiño C.S.
      • Waghorn G.C.
      • Hegarty R.S.
      • Hoskin S.O.
      Effects of intensification of pastoral farming on greenhouse gas emissions in New Zealand.
      ;
      • Archimède H.
      • Eugène M.
      • Marie Magdeleine C.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes.
      ). In contrast, tropical legumes are significantly less digestible and produce less CH4 per unit of intake than temperate legumes (
      • Archimède H.
      • Eugène M.
      • Marie Magdeleine C.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes.
      ). The greater content of tannins and other secondary metabolites in tropical legumes affects NDF digestibility and CH4 production (
      • Archimède H.
      • Eugène M.
      • Marie Magdeleine C.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes.
      ); however, the authors did not use NDF digestibility in their analysis.
      High-starch, cereal grain-based diets stimulate the growth and metabolic activity of propionate-producing microbes (
      • Ominski K.H.
      • Wittenberg K.M.
      Strategies for reducing enteric methane emissions in forage-based beef production systems.
      ;
      • Martin C.
      • Morgavi D.P.
      • Doreau M.
      Methane mitigation in ruminants: From microbe to farm scale.
      ). Because the formation of propionate consumes reducing equivalents (Equation 3), enhancing propionate production reduces the amount of metabolic H2 available for methanogenesis in the rumen. Ruminal pH also decreases with increasing NFC concentrations, which can inhibit the growth of methanogens and ciliate protozoa (
      • van Kessel J.A.S.
      • Russell J.B.
      The effect of pH on ruminal methanogenesis.
      ;
      • Hegarty R.S.
      Reducing rumen methane emissions through elimination of rumen protozoa.
      ). However, it can also reduce NDF digestibility. In general, decreasing the NDF:NFC ratio of ruminant diets can reduce the percentage of GEI lost as CH4 (
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ;
      • Chagunda M.G.G.
      • Römer D.A.M.
      • Roberts D.J.
      Effect of genotype and feeding regime on enteric methane, non-milk nitrogen and performance of dairy cows during the winter feeding period.
      ). Very low CH4 emissions (2–3% GEI) are reported from cattle fed low- (10–30%) forage diets, such as beef finishing rations (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ). Although in beef cattle research CH4 is often expressed as percentage of GEI, it should be expressed as CH4 per ADG or CH4 per kilogram of carcass yield in an analogous manner to the CH4/ECM approach for evaluating CH4 emissions in dairy cattle. If grain supplementation increases GEI and ADG even though CH4/GEI is unchanged, fewer days on feed will be required to reach target weight and less total CH4 will be emitted during the growing and finishing periods. Accordingly, whole-farm GHG inventory models usually predict lower GHG emissions from on-farm animal and manure emissions and from off-farm feed production with increased grain and by-product feeding (
      • Phetteplace H.W.
      • Johnson D.E.
      • Seidl A.F.
      Greenhouse gas emissions from simulated beef and dairy livestock systems in the United States.
      ;
      • Lovett D.K.
      • Shalloo L.
      • Dillon P.
      • O’Mara F.P.
      A systems approach to quantify greenhouse gas fluxes from pastoral dairy production as affected by management regime.
      ).
      Although the word concentrates is broadly used many different feed ingredients can be incorporated into the nonforage portion of a ration.
      • Hindrichsen I.K.
      • Wettstein H.-R.
      • Machmüller A.
      • Jörg B.
      • Kreuzer M.
      Effect of the carbohydrate composition of feed concentrates on methane emission from dairy cows and their slurry.
      ) examined nonforage ingredients with lignified fiber, nonlignified fiber, pectin, fructans, sugar, or starch and found them to have differing effects on DM and NDF digestibilities, but not on CH4 emissions when expressed as grams of CH4 per kilogram of milk protein. Regression analysis of results from the same experiment (
      • Hindrichsen I.K.
      • Wettstein H.-R.
      • Machmüller A.
      • Jörg B.
      • Kreuzer M.
      Effect of the carbohydrate composition of feed concentrates on methane emission from dairy cows and their slurry.
      ) provided the following equation:
      CH4(g/d)=91+50×digested cellulose(kg/d)+40×digested hemicellulose(kg/d)+24×digested starch(kg/d)+67×digested sugars(kg/d),


      which can be compared with the equation from
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ):
      CH4(kg/d)=33.0+104.6×digested cellulose(kg/d)+38.5×digested hemicellulose(kg/d)+20.5×digested neutral detergent-soluble residue(kg/d).


      In both data sets, the digested cellulose and hemicellulose would be from combined forage and nonforage feed ingredients. In
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ), the neutral detergent-soluble residue fraction would include starch, sugars, silage acids, other organic acids, and the pectins and fructans not precipitated in NDF. Both equations clearly show that starch generates less CH4 than hemicellulose or cellulose per unit digested. The high coefficient for sugars in
      • Hindrichsen I.K.
      • Wettstein H.-R.
      • Machmüller A.
      • Jörg B.
      • Kreuzer M.
      Effect of the carbohydrate composition of feed concentrates on methane emission from dairy cows and their slurry.
      ) may reflect the stimulatory effect of sugars on fiber digestion.
      The difference in CH4 produced per unit of starch versus cellulose is not a function of their chemical composition; both are hydrolyzed to glucose before being fermented. In contrast, hemicellulose, as a mixture of 5- and 6-C sugars, would be expected to result in a different VFA pattern and proportion of CH4 than starch or cellulose. Rather than a chemical basis for the difference in CH4 production between starch, hemicellulose, and cellulose, the difference appears to be a function of the microbial species that degrade and ferment the majority of each substrate (
      • Hungate R.E.
      ;
      • Baldwin R.L.
      • Allison M.J.
      Rumen metabolism.
      ). Thus, as microbial species adapt to changing dietary substrates and rumen conditions, patterns of VFA and CH4 production will change. Improving our understanding of the interrelationships between substrate availability and microbial maintenance and growth that affect overall rumen fermentation will lead to better predictions of CH4 generation and identification of opportunities to manipulate fermentation and reduce CH4 production. The observation that CH4 production is influenced by associative factors between nutrient fractions in the diet implies that CH4 can only be predicted for the diet or ration, not for the individual feed ingredients, which is analogous to the prediction of NEL or MP (
      NRC
      ).

      Forage Quality, Species, Harvesting, and Storage

      • Leng R.A.
      Quantitative ruminant nutrition—A green science.
      ) estimated that 75% of global ruminant CH4 emissions came from ruminants grazing low-quality feeds. Increasing the quality of the feed is an overarching concept related to feed efficiency and animal productivity, which can decrease CH4 emissions per unit of product. Increasing forage quality is favorably received by livestock farmers because feeding high-quality forages is central to good farming practice and often increases profitability (
      • Waghorn G.C.
      • Clark D.A.
      Greenhouse gas mitigation opportunities with immediate application to pastoral grazing for ruminants.
      ). Forage quality can be improved by harvesting or grazing less mature forages, selection of genetic strains or species that have superior digestibility (e.g., brown midrib corn and sorghum), and proper storage, especially ensiling, to conserve digestible nutrient content, improve dietary utilization, and increase feed efficiency. In general, better-quality forages will contain a greater proportion of NSC to NDF or the NDF will be less lignified (
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      ;
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ).
      Several studies have compared different forages in terms of CH4 emissions (
      • McCaughey W.P.
      • Wittenberg K.M.
      • Corrigan D.
      Impact of pasture type on methane production by lactating beef cows.
      ;
      • Boadi D.
      • Wittenberg K.M.
      • McCaughey W.P.
      Effects of grain supplementation on methane production of grazing steers using the sulphur (SF6) tracer gas technique.
      ,
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ;
      • 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.
      ;
      • Robertson L.J.
      • Waghorn G.C.
      Dairy industry perspectives on methane emissions and production from cattle fed pasture or total mixed rations in New Zealand.
      ;
      • van Dorland H.A.
      • Wettstein H.-R.
      • Leuenberger H.
      • Kreuzer M.
      Effect of supplementation of fresh and ensiled clovers to ryegrass on nitrogen loss and methane emission of dairy cows.
      ;
      • O’Neill B.F.
      • Deighton M.H.
      • O’Loughlin B.M.
      • Galvin N.
      • O’Donovan M.
      • Lewis E.
      The effects of supplementing grazing dairy cows with partial mixed ration on enteric methane emissions and milk production during mid to late lactation.
      ). The diets compared legumes versus grasses, stage of maturity, and grazed versus harvested forages. However, some comparisons were confounded with other dietary changes to maintain energy density or nitrogen intakes. A comprehensive evaluation of the effect of forage quality on CH4 emissions requires an approach that considers diet composition and level of intake. In essence, this has been done in the research to develop CH4 prediction equations (
      • Moe P.W.
      • Tyrrell H.F.
      Methane production in dairy cows.
      ;
      • Mills J.A.N.
      • Kebreab E.
      • Yates C.M.
      • Crompton L.A.
      • Cammell S.B.
      • Dhanoa M.S.
      • Agnew R.E.
      • France J.
      Alternative approaches to predicting methane emissions from dairy cows.
      ) and in the meta-analysis of
      • Archimède H.
      • Eugène M.
      • Marie Magdeleine C.
      • Boval M.
      • Martin C.
      • Morgavi D.P.
      • Lecomte P.
      • Doreau M.
      Comparison of methane production between C3 and C4 grasses and legumes.
      ), which accounted for intake and NDF digestibility (discussed in the previous section).
      The effects of forage preservation on CH4 production have not been studied at length. The ensiling process results in fermentation of the forages, which can reduce digestion in the rumen (
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ). Cows fed either a partial or total mixed ration with ensiled forages with OM digestibilities >80% had similar CH4/ECM as cows consuming high-quality pasture with similar digestibilities (
      • Robertson L.J.
      • Waghorn G.C.
      Dairy industry perspectives on methane emissions and production from cattle fed pasture or total mixed rations in New Zealand.
      ;
      • O’Neill B.F.
      • Deighton M.H.
      • O’Loughlin B.M.
      • Galvin N.
      • O’Donovan M.
      • Lewis E.
      The effects of supplementing grazing dairy cows with partial mixed ration on enteric methane emissions and milk production during mid to late lactation.
      ). When expressed as percentage of GEI, ensiled forages have been shown to produce less CH4 than dried forages (
      • Sundstol F.
      Methods for treatment of low quality roughages.
      ). Some evidence exists that maize and whole-crop small-grain silages will yield less CH4 than grass silage, which likely reflects differences in carbohydrate composition and digestibility, but a need still exists for direct in vivo comparisons and whole-farm GHG analyses for all of these situations (
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ). Different additives and inoculants have been added to silage with limited success in reducing CH4 production (
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ).

      Feed Processing

      Feed processing reduces the particle size distribution of the feed and alters the rates of fermentation and passage of the particles, with the benefit depending on the feed. Particles that are too small can pass undigested out of the rumen and will not increase the amount fermented (
      • Russell J.B.
      • Hespell R.B.
      Microbial rumen fermentation.
      ). Processing forages by grinding, chopping, or pelleting will decrease rumen NDF digestibility and can decrease CH4 emissions as a result of increased passage rate (Table 1;
      • Johnson D.E.
      • Ward G.M.
      • Ramsey J.J.
      Livestock methane: Current emissions and mitigation potential.
      ;
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      ) with decreased acetate:propionate ratios (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ). This effect is not usually evident with restricted intakes, but at high levels of intake CH4 reductions of 20 to 40% per unit of DM could be achieved (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ). Pelleting can decrease CH4 production to a greater extent than chopping, but the effect of pelleting is most pronounced with low-quality forages (
      • Hironaka R.
      • Mathison G.W.
      • Kerrigan B.K.
      • Vlach I.
      The effect of pelleting of alfalfa hay on methane production and digestibility by steers.
      ). Also, the CH4 reductions may not be great enough to justify the extra energy expenditure and the likely increased associated GHG production required to pellet the feed (
      • Hironaka R.
      • Mathison G.W.
      • Kerrigan B.K.
      • Vlach I.
      The effect of pelleting of alfalfa hay on methane production and digestibility by steers.
      ). Fine grinding of forages has proven to be uneconomical due to the greater incidence of acidosis associated with deficient effective NDF and decreased milk fat concentration (
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ). Last, the acetate:propionate ratio has been decreased through alkali treatment of cereal straw (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ), a strategy that could reduce CH4 by 10% (
      • Johnson D.E.
      • Ward G.M.
      • Ramsey J.J.
      Livestock methane: Current emissions and mitigation potential.
      ). Experimentation with feeding alkali-treated straw to sheep found CH4 per unit of apparently digested OM to be reduced, and the volume of CH4 produced per animal was significantly increased due to increased intakes (
      • Moss A.R.
      • Givens D.I.
      • Garnsworthy P.C.
      The effect of alkali treatment of cereal straws on digestibility and methane production by sheep.
      ). If alkali treatment of poor-quality forages were to be used for feeding cattle and digestibility were increased, CH4/ECM or CH4 per ADG would be expected to decrease.
      Processing grains by grinding, rolling, or flaking can increase rumen fermentation and decrease the amount passing to the intestines (Table 1). Extensive rolling of barley increased DMI and maximized ruminal and postruminal digestibility of starch (
      • Yang W.Z.
      • Beauchemin K.A.
      • Rode L.M.
      Effects of grain processing, forage to concentrate ratio, and forage particle size on rumen pH and digestion by dairy cows.
      ). Heat treatment through pelleting, flaking, extruding, and toasting can change the degradation rates of protein and carbohydrates and decrease the acetate:propionate ratio (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ) but the relationship with CH4 emissions depends on the feed as well as composition of the total diet and intake.
      Overall, processing could have mixed effects. Processing forages alters rumen fermentation and decreases rumen NDF digestibility. If NDF is digested in the hindgut or in manure storage, no net change in whole-farm CH4 emissions will occur. Conversely, processing grains increases rumen DM and starch digestibility (
      • Firkins J.L.
      • Eastridge M.L.
      • St-Pierre N.R.
      • Noftsger S.M.
      Effects of grain variability and processing on starch utilization by lactating dairy cattle.
      ), with more CH4 being produced from rumen fermentation than if starch were digested in the small intestine, assuming no negative effects on fiber digestion. Processing that improves DM digestibility will reduce CH4/ECM by increasing energy available for productive purposes and diluting CH4 associated with maintenance. In contrast, processing that decreases digestibility and CH4 per day per head is not desirable, as more feed inputs will be required to produce the same amount of milk.

      Lipid and FA Supplementation

      Lipid supplementation is an extensively researched enteric CH4 mitigation strategy, and several reviews are available on this topic (
      • Giger-Reverdin S.
      • Morand-Fehr P.
      • Tran G.
      Literature survey of the influence of dietary fat composition on methane production in dairy cattle.
      ;
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ;
      • Eugene M.
      • Masse D.
      • Chiquette J.
      • Benchaar C.
      Meta-analysis on the effects of lipid supplementation on methane production in lactating dairy cows.
      ).

      Climate Change Central. 2012. Climate Change Central, Alberta, Canada. Accessed Apr. 1, 2014. http://environment.gov.ab.ca/info/library/8255.pdf

      ) in Alberta, Canada already recognizes oil supplementation as a mitigation strategy under their protocols. The effect of dietary lipids on CH4 production is dependent on the source, FA profile, inclusion rate (% of DMI), and diet composition (
      • Beauchemin K.A.
      • McGinn S.M.
      • Petit H.V.
      Methane abatement strategies for cattle: Lipid supplementation of diets.
      ;
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ). The form of the lipid supplement affects its availability in the rumen, and this appears to be more important than the FA profile (
      • Beauchemin K.A.
      • McGinn S.M.
      • Benchaar C.
      • Holtshausen L.
      Crushed sunflower, flax, or canola seeds in lactating dairy cow diets: Effects on methane production, rumen fermentation, and milk production.
      ).
      In vitro, lipid additives suppress ciliate protozoa (
      • Dohme F.
      • Machmüller A.
      • Wasserfallen A.
      • Kreuzer W.
      Comparative efficiency of various fats rich in medium-chain fatty acids to suppress ruminal methanogenesis as measured with RUSITEC.
      ) and methanogen populations in the rumen (
      • Machmüller A.
      • Kreuzer M.
      Methane suppression by coconut oil and associated effects on nutrient and energy balance in sheep.
      ) by differing modes of action, depending on the primary FA (
      • Dohme F.
      • Machmüller A.
      • Wasserfallen A.
      • Kreuzer M.
      Ruminal methanogenesis as influenced by individual fatty acids supplemented to complete ruminant diets.
      ). They decrease OM and fiber degradability and reduce fermentable substrate (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ;
      • Dong Y.
      • Bae H.D.
      • McAllister T.A.
      • Mathison G.W.
      • Cheng K.-J.
      Lipid-induced depression of methane production and digestibility in the artificial rumen system (RUSITEC).
      ;
      • Dohme F.
      • Machmüller A.
      • Wasserfallen A.
      • Kreuzer M.
      Ruminal methanogenesis as influenced by individual fatty acids supplemented to complete ruminant diets.
      ;
      • McGinn S.M.
      • Beauchemin K.A.
      • Coates T.
      • Colombatto D.
      Methane emissions from beef cattle: Effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid.
      ), which means less CH4 production but is not a desirable effect in itself. Biohydrogenation of unsaturated FA can be an alternative sink for H2, but this is trivial compared with methanogenesis (
      • Johnson K.A.
      • Johnson D.E.
      Methane emissions from cattle.
      ;
      • Hegarty R.S.
      Mechanisms for competitively reducing ruminal methanogenesis.
      ). In animals that are not rumen-fill limited but eat to meet energy requirements, lipids create a dilution effect because they replace fermentable carbohydrates in the energy supply. Also, they often reduce DMI. Finally, rumen inert or protected fats (such as calcium soaps) do not show the same effects as other lipid sources (
      • Dohme F.
      • Machmüller A.
      • Wasserfallen A.
      • Kreuzer W.
      Comparative efficiency of various fats rich in medium-chain fatty acids to suppress ruminal methanogenesis as measured with RUSITEC.
      ). In a meta-analysis by
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ) using 33 treatments, each 1% addition of fat to the diet resulted in a 5.6% reduction in CH4 (g/kg of DMI) up to 36%. Another meta-analysis concluded that lipid supplementation to dairy cows reduces daily CH4 production by 0.305 g/kg of DMI for each 1% increase in ration ether extract (EE), and mainly as a consequence of lower DMI (
      • Eugene M.
      • Masse D.
      • Chiquette J.
      • Benchaar C.
      Meta-analysis on the effects of lipid supplementation on methane production in lactating dairy cows.
      ). The effect of lipid composition or type was not evaluated.
      Given our focus on CH4/ECM, we conducted a meta-analysis on the effects of lipid supplementation on CH4 emissions. Eleven studies were identified in the published literature with different sources of lipid (whole seed, crushed seed, oils, calcium salts of FA, and FFA), and include the work of
      • Andrew S.M.
      • Tyrrell H.R.
      • Reynolds C.K.
      • Erdman R.A.
      Net energy for lactation of calcium salts of long-chain fatty acids for cows fed silage-based diets.
      ),
      • Holter J.B.
      • Hayes H.H.
      • Urban Jr., W.E.
      • Duthie A.H.
      Energy balance and lactation response in Holstein cows supplemented with cottonseed with or without calcium soap.
      ),
      • Johnson K.A.
      • Kincaid R.L.
      • Westberg H.H.
      • Gaskins C.T.
      • Lamb B.K.
      • Cronrath J.D.
      The effect of oilseeds in diets of lactating cows on milk production and methane emissions.
      ),
      • Dohme F.
      • Machmüller A.
      • Sutter F.
      • Kreuzer M.
      Digestive and metabolic utilization of lauric, myristic and stearic acid in cows, and associated effects on milk fat quality.
      ),
      • Odongo N.E.
      • Or-Rashid M.M.
      • Kebreab E.
      • France J.
      • Bride B.W.
      Effect of supplementing myristic acid in dairy cow rations on ruminal methanogenesis and fatty acid profile in milk.
      ),
      • Martin C.
      • Rouel J.
      • Jouany J.P.
      • Doreau M.
      • Chilliard Y.
      Methane output and diet digestibility in response to feeding dairy cows crude linseed, extruded linseed, or linseed oil.
      ),
      • Beauchemin K.A.
      • McGinn S.M.
      • Benchaar C.
      • Holtshausen L.
      Crushed sunflower, flax, or canola seeds in lactating dairy cow diets: Effects on methane production, rumen fermentation, and milk production.
      ),
      • Hristov A.N.
      • Vander Pol M.
      • Agle M.
      • Zaman S.
      • Schneider C.
      • Ndegwa P.
      • Vaddella V.K.
      • Johnson K.
      • Shingfield K.J.
      • Karnati S.K.R.
      Effect of lauric acid and coconut oil on ruminal fermentation, digestion, ammonia losses from manure, and milk fatty acid composition in lactating cows.
      ,
      • Hristov A.N.
      • Lee C.
      • Cassidy T.
      • Long M.
      • Heyler K.
      • Corl B.
      • Forster R.
      Effects of lauric and myristic acids on ruminal fermentation, production, and milk fatty acid composition in lactating dairy cows.
      )
      • Grainger C.
      • Williams R.
      • Clarke T.
      • Wright A.-D. G.
      • Eckard R.J.
      Supplementation with whole cottonseed causes long-term reduction of methane emissions from lactating dairy cows offered a forage and cereal grain diet.
      ),
      • Mohammed R.
      • McGinn S.M.
      • Beauchemin K.A.
      Prediction of enteric methane output from milk fatty acid concentrations and rumen fermentation parameters in dairy cows fed sunflower, flax, or canola seeds.
      ), and
      • Hollmann M.
      • Powers W.J.
      • Fogiel A.C.
      • Liesman J.S.
      • Bello N.M.
      • Beede D.K.
      Enteric methane emissions and lactational performance of Holstein cows fed different concentrations of coconut oil.
      ). Most of the studies were designed to compare different lipid sources; only 1 study used the same supplement at different levels (
      • Hollmann M.
      • Powers W.J.
      • Fogiel A.C.
      • Liesman J.S.
      • Bello N.M.
      • Beede D.K.
      Enteric methane emissions and lactational performance of Holstein cows fed different concentrations of coconut oil.
      ). Often, more than 2 ingredients were different between treatments and nutrients other than EE varied between treatments within the same study. Five studies used open-circuit respiratory chambers, 1 study used hoods, and 5 studies used SF6 methodology to measure CH4 emissions. Measurement method was a significant effector of observed CH4/ECM (data not shown). The data were analyzed using the following model:
      yk=β0+si+βj×ee+errork,


      where yk = CH4/ECM and are the treatment means (k = 1 to 35), β0 = a common intercept across studies, si = the random study effect (i = 1 to 11), βj = the regression coefficient for the jth lipid source (j = 1 to 4), and ee = the EE content of the ration. Lipid sources were identified as either rumen inert (calcium salts of FA or stearic acid), oils (medium-chain FA or vegetable oils), seeds (whole, crushed, or extruded), or endogenous lipids in feedstuffs (control treatments). The standard error of CH4 emissions across studies varied over a 3-fold range, and this variation was used to weight studies accordingly using the inverse of the reported standard error for CH4 (g/d). The variance component due to the interaction between study effect and EE content was very small compared with the study effect and thus was removed from the model to improve parameter estimates.
      Observed treatment means of CH4/ECM as a function of ration EE content can be seen in Figure 4a, with lines connecting the individual treatment means within a study. Overall, a trend for decreasing CH4/ECM could be seen as EE increased, although some studies showed little change (I, J, and K) or an increase (D and F). The differences between studies are large, and may be attributable to measurement method, diet, and animal characteristics, and other experimental variation, and all of these are captured in the study effect in the statistical analysis. After accounting for the study effect, the results show that increasing EE content in the ration reduced CH4/ECM, and that significant differences existed in the interaction between lipid sources and EE content (Figure 4b). Each percentage unit of ration EE from inert, seed, oil, and endogenous lipid sources decreased CH4/ECM by 0.78 ± 0.20, 0.71 ± 0.20, 1.12 ± 0.20, and 1.01 ± 0.38 g/kg, respectively. The slopes of inert and seed lipid sources were not significantly different from each other (P > 0.48), but differed significantly from the slope of oil lipid source (P < 0.006 and <0.002, respectively). The slope of endogenous lipid source was intermediate between that of inert and seed sources versus oil sources, and not significantly different from any treatment (P > 0.17 to 0.51). The endogenous lipids in feedstuffs contain greater concentrations of MUFA and PUFA than SFA. The intermediate slope for endogenous lipid diets may be indicative of an effect of FA composition on rumen function and CH4 production.
      Figure thumbnail gr4
      Figure 4(a) Summary of enteric CH4 emissions per unit of ECM (CH4/ECM) as a function of ration ether extract (EE) content from 11 studies and 35 dietary treatments. Observed treatment means for each study are connected by lines. Study A:
      • Hollmann M.
      • Powers W.J.
      • Fogiel A.C.
      • Liesman J.S.
      • Bello N.M.
      • Beede D.K.
      Enteric methane emissions and lactational performance of Holstein cows fed different concentrations of coconut oil.
      ), B:
      • Grainger C.
      • Williams R.
      • Clarke T.
      • Wright A.-D. G.
      • Eckard R.J.
      Supplementation with whole cottonseed causes long-term reduction of methane emissions from lactating dairy cows offered a forage and cereal grain diet.
      ), C:
      • Hristov A.N.
      • Vander Pol M.
      • Agle M.
      • Zaman S.
      • Schneider C.
      • Ndegwa P.
      • Vaddella V.K.
      • Johnson K.
      • Shingfield K.J.
      • Karnati S.K.R.
      Effect of lauric acid and coconut oil on ruminal fermentation, digestion, ammonia losses from manure, and milk fatty acid composition in lactating cows.
      ), D:
      • Hristov A.N.
      • Lee C.
      • Cassidy T.
      • Long M.
      • Heyler K.
      • Corl B.
      • Forster R.
      Effects of lauric and myristic acids on ruminal fermentation, production, and milk fatty acid composition in lactating dairy cows.
      ), E:
      • Martin C.
      • Rouel J.
      • Jouany J.P.
      • Doreau M.
      • Chilliard Y.
      Methane output and diet digestibility in response to feeding dairy cows crude linseed, extruded linseed, or linseed oil.
      ), F:
      • Johnson K.A.
      • Kincaid R.L.
      • Westberg H.H.
      • Gaskins C.T.
      • Lamb B.K.
      • Cronrath J.D.
      The effect of oilseeds in diets of lactating cows on milk production and methane emissions.
      ), G:
      • Dohme F.
      • Machmüller A.
      • Sutter F.
      • Kreuzer M.
      Digestive and metabolic utilization of lauric, myristic and stearic acid in cows, and associated effects on milk fat quality.
      ), H:
      • 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.
      ), I:
      • Beauchemin K.A.
      • McGinn S.M.
      • Benchaar C.
      • Holtshausen L.
      Crushed sunflower, flax, or canola seeds in lactating dairy cow diets: Effects on methane production, rumen fermentation, and milk production.
      ) and
      • Mohammed R.
      • McGinn S.M.
      • Beauchemin K.A.
      Prediction of enteric methane output from milk fatty acid concentrations and rumen fermentation parameters in dairy cows fed sunflower, flax, or canola seeds.
      ), J:
      • Holter J.B.
      • Hayes H.H.
      • Urban Jr., W.E.
      • Duthie A.H.
      Energy balance and lactation response in Holstein cows supplemented with cottonseed with or without calcium soap.
      ), and K:
      • Andrew S.M.
      • Tyrrell H.R.
      • Reynolds C.K.
      • Erdman R.A.
      Net energy for lactation of calcium salts of long-chain fatty acids for cows fed silage-based diets.
      ). (b) Predicted reductions in CH4/ECM for inert, seed, oil, and endogenous (nonsupplemented) sources of lipid. Intercept = 17.25 ± 2.07 g/kg. Slopes for different lipid sources are given in the text. (c) Predicted reductions in DMI for inert, seed, oil, and endogenous (nonsupplemented) sources of lipid. Intercepts and slopes for different lipid sources are given in the text.
      Different lipid sources may affect CH4 emissions by altering DMI and this could affect CH4/ECM. Previous reviews have observed a reduction in DMI with lipid supplementation (
      • Chilliard Y.
      Dietary fat and adipose tissue metabolism in ruminants, pigs, and rodents: A review.
      ;
      • Allen M.S.
      Effects of diet on short-term regulation of feed intake by lactating dairy cattle.
      ;
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ). In this analysis, the best fit model for DMI was yk = si + βj + βj × ee + errork, with separate intercepts and slopes for each lipid source. Analysis of the effect of lipid source and ration EE content showed that inert and endogenous lipid sources did not affect DMI (kg/d; Figure 4c; P > 0.85 and P > 0.77, respectively). However, oil sources (vegetable oils and medium-chain FFA) significantly reduced DMI by 1.51 ± 0.40 kg per percentage unit increase in ration EE (Figure 4c; P < 0.001; intercept = 28.0 ± 3.10). Seeds also reduced DMI by 0.90 ± 0.52 kg per percentage unit increase in ration EE (Figure 4c; P < 0.09, intercept = 25.8 ± 3.47). This effect of ration EE for seeds followed a quadratic pattern, with reductions in DMI occurring at ration EE approximating 7% DM (Figure 4c). The greater variation observed with seeds is reasonable, given that these treatments included whole, crushed, and extruded seeds.
      In summary, increasing ration EE with endogenous lipid in feedstuffs, inert lipids, or seed sources reduces enteric CH4/ECM, and it appears that this is achieved by dilution of the fermentable carbohydrates in the DMI and potentially reduced DMI. No difference existed in CH4/ECM between the inert, seed, or endogenous feed sources of lipids. Some seeds, vegetable oils, and medium-chain FFA further reduced CH4/ECM, but it appears that this was largely achieved at the expense of reduced DMI, which could be detrimental to energy balance and milk yield over longer periods of time. Vegetable oils and medium-chain FA are known to alter rumen function and decrease NDF digestibility. Whether these lipid sources reduce enteric CH4/ECM by this mechanism cannot be ascertained in this analysis, as rumen digestibilities were not measured. However, it is supported by subsequent research of
      • Hollmann M.
      • Powers W.J.
      • Fogiel A.C.
      • Liesman J.S.
      • Bello N.M.
      • Beede D.K.
      Response profiles of enteric methane emissions and lactational performance during habituation to dietary coconut oil in dairy cows.
      ) that demonstrated reduced DMI and total-tract NDF digestibility with increasing dietary inclusion of coconut oil. Also, most of the studies used in this analysis were short-term feeding trials (2 to 5 wk), with the exception of
      • Grainger C.
      • Williams R.
      • Clarke T.
      • Wright A.-D. G.
      • Eckard R.J.
      Supplementation with whole cottonseed causes long-term reduction of methane emissions from lactating dairy cows offered a forage and cereal grain diet.
      ; 12 wk). Future research in this area should focus on dose-response relationships by using multiple levels of lipid supplementation and longer-term trials where energy balance can be determined (
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ;
      • Grainger C.
      • Clarke T.
      • Beauchemin K.A.
      • McGinn S.M.
      • Eckard R.J.
      Supplementation with whole cottonseed reduces methane emissions and can profitably increase milk production of dairy cows offered a forage and cereal grain diet.
      ;
      • Martin C.
      • Rouel J.
      • Jouany J.P.
      • Doreau M.
      • Chilliard Y.
      Methane output and diet digestibility in response to feeding dairy cows crude linseed, extruded linseed, or linseed oil.
      ). Furthermore, the effect of lipid supplementation on emissions of CH4 and other GHG must be evaluated on a whole-farm basis. If lipids reduce fiber digestibility, then more CH4 may be emitted from the manure during storage and anaerobic fermentation (
      • Hristov A.N.
      • Oh J.
      • Lee C.
      • Meinen R.
      • Montes F.
      • Ott T.
      • Firkins J.
      • Rotz A.
      • Dell C.
      • Adesogan A.
      • Yang W.
      • Tricarico J.
      • Kebreab E.
      • Waghorn G.
      • Dijkstra J.
      • Oosting S.
      • et al.
      Mitigation of greenhouse gas emissions in livestock production: A review of technical options for non-CO2 emissions.
      ).
      Typically, lactating cow rations contain 4 to 5% EE, with fat supplementation increasing levels to 5 to 7% DM. Current recommendations are for ration EE to not exceed 6 to 7% DM (
      NRC
      ). With decreases in enteric CH4/ECM of 0.71 to 1.21 g/kg for each percentage of ration EE and typical CH4 emissions of 5 to 25 g/kg of ECM, a 2% increase in ration EE would be expected to decrease CH4 approximately 10%. This reduction is comparable with the low end of the range of 10 to 25% reductions given on a CH4/DM in
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      ). Reductions on a CH4/ECM basis should be less than reductions on a CH4/DM basis, given the strong, positive relationship between DMI and ECM. The effects of fat supplementation on milk and milk component yields are variable, and depend on the nutrient composition of the basal diet, FA composition of the endogenous and supplemental lipids, and stage of lactation as well the amount of fat supplemented (
      NRC
      ). Excellent reviews on this topic can be found in
      • Chilliard Y.
      Dietary fat and adipose tissue metabolism in ruminants, pigs, and rodents: A review.
      ),
      • Jenkins T.C.
      Success of fat in dairy rations depends on the amount.
      ), and
      • Schroeder G.G.
      • Gagliostro G.A.
      • Bargo F.
      • Delahoy J.E.
      • Muller L.D.
      Effects of fat supplementation on milk production and composition by dairy cows on pasture: A review.
      ).

      Summary of Nutrition and Feeding Management Strategies

      Many of these enteric CH4 mitigation strategies are mechanistically geared toward enhancing the propionate:acetate ratio from fermentation. Although methanogens are a crucial part of the rumen ecology, CH4 formation should be minimized and the yield of VFA maximized. The potential for reducing CH4/ECM through nutrition and feeding management is modest (Figure 5) and will be mostly achieved by approaches that improve feed efficiency (Figure 6). Feeding nonstructural or starchy carbohydrates, high-quality forages at greater intake levels, or optimally processing the forages can reduce enteric CH4/ECM emissions by 5 to 15% (Table 1; Figure 5).
      Figure thumbnail gr5
      Figure 5Feeding and nutritional approaches to reducing enteric CH4 emissions per unit of ECM (CH4/ECM) range from 0 to 15% and are largely nonadditive, with a maximum reduction of 15% or approximately 2.25 g of CH4/kg of ECM.
      Figure thumbnail gr6
      Figure 6Enteric CH4 emissions per unit of ECM (CH4/ECM; solid and dotted lines, primary axis) decreases with increasing productivity and increasing feed efficiency (dashed line, secondary axis) and can vary by more than ±20%. Estimates do not consider improved diet quality or decreased digestibility for high-producing cows, which would further lower enteric CH4/ECM. Predictions of CH4 production were calculated as described in the text at Ym = 5.6% GEI (solid line) and at Ym= 4.6 and 6.6% (dotted lines, primary axis), where Ym = CH4 as a percentage of gross energy intake (GEI).
      It may be possible to combine some of the feeding and nutritional management approaches to reduce enteric CH4/ECM (e.g., forage genetics and improved forage quality via management). Some of the approaches are redundant with respect to mechanisms and outcome (e.g., feeding more concentrate and reducing rumen pH <5.5). Some result in reduced DMI, which reduces both CH4 and ECM, with no decrease or potentially increasing CH4/ECM (e.g., decreasing rumen pH <5.5 or lipid feeding). Some approaches may lead to other undesirable outcomes, such as reduced feed efficiency, liver abscesses, and so on. With the redundancy in effects and the robust ability of the rumen microbes to adjust to changing conditions through several mechanisms, responses to different nutritional approaches are expected to be significantly less than fully additive (Figure 5). The implementation of many of the feeding and nutritional approaches is limited to lactating dairy cattle rations for practical or economic reasons and, thus, the reductions in enteric CH4 would be less on a whole-herd basis than on an individual-cow basis.

      Rumen Modifiers: Feed Additives and Biological Control

      A wide variety of supplements exist that can be administered to reduce CH4, such as chemical inhibitors, organic acids, and plant secondary compounds. The mode of action depends on the specific additive, but can include direct inhibition of methanogens or methanogenesis, suppression of ciliate protozoa, or providing or stimulating a competitive pathway for H2 disposal. A wide variety of inhibitors have been studied, including halogenated CH4 analogs, coenzyme-M analogs, and proton-motive force uncouplers (
      • Czerkawski J.W.
      • Breckenridge G.
      Fermentation of various glycolytic intermediates and other compounds by rumen micro-organisms, with particular reference to methane production.
      ;
      • Martin S.A.
      • Macy J.M.
      Effects of monensin, pyromellitic diimide and 2-bromoethanesulfonic acid on rumen fermentation in vitro.
      ).
      In vitro, many additives and inhibitors suppress methanogenesis by 60 to 100% (Table 2). When these additives are fed to animals, however, the reduction in CH4 emissions has been either not evident or transient (<30 d; Table 3). Basic ecological principles need to be kept in mind when targeting microbial populations. With the incredible diversity of ruminal microbes, it is very likely that the removal or suppression of one group will result in another group adapting to fill its niche (
      • Hungate R.E.
      ;
      • Czerkawski J.W.
      ;
      • Weimer P.J.
      Manipulating ruminal fermentation: A microbial ecological perspective.
      ). Recent studies indicate that CH4 emission reductions resulting from short- and long-term defaunation do not correlate with the relative abundance of methanogens measured by quantitative PCR (
      • Mosoni P.
      • Martin C.
      • Forano E.
      • Morgavi D.P.
      Long-term defaunation increases the abundance of cellulolytic ruminococci and methanogens but does not affect the bacterial and methanogen diversity in the rumen of sheep.
      ;
      • Morgavi D.P.
      • Martin C.
      • Jouany J.P.
      • Ranilla M.J.
      Rumen protozoa and methanogenesis: Not a simple cause-effect relationship.
      ). In fact,
      • Mosoni P.
      • Martin C.
      • Forano E.
      • Morgavi D.P.
      Long-term defaunation increases the abundance of cellulolytic ruminococci and methanogens but does not affect the bacterial and methanogen diversity in the rumen of sheep.
      ) reported that although defaunation reduced CH4 emissions, ruminal methanogen density increased 10-fold. Second, if methanogenesis is reduced or eliminated, another route must exist for hydrogen disposal, or else rumen hydrogen concentrations will rise and potentially inhibit fermentation (
      • Weimer P.J.
      Manipulating ruminal fermentation: A microbial ecological perspective.
      ). Ideally, this hydrogen or electron sink would result in the production of a compound that can be absorbed and metabolized by the animal so that the energy is not lost (
      • Brown E.G.
      • Anderson R.C.
      • Carstens G.E.
      • Gutierrez-Bañuelos H.
      • McReynolds J.L.
      • Slay L.J.
      • Callaway T.R.
      • Nisbet D.J.
      Effects of oral nitroethane administration on enteric methane emissions and ruminal fermentation in cattle.
      ).
      Table 2Summary of rumen modifiers that have been tested in vitro but not in vivo
      In addition to the references given, extensive reviews are available (Van Nevel and Demeyer, 1996; Moss et al., 2000; Boadi et al., 2004; Martin et al., 2010; Hristov et al., 2013).
      Approach/compoundCH4 reduction relative to control (%)Effect on NDF digestibilityReferencesComments
      Electron acceptors (methylene blue, riboflavin, nicotinamide adenine dinucleotide, nitrate, sulfate, methyl- and benzyl viologenReviewed in
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      )
      Nonspecific action; function as alternative H2 sinks; often required to be in stoichiometric proportions
      Specific inhibitors of methanogenesis (p-aminobenzoic acid derivatives, mevastatin, lovastatin)50–100
      • Dumitru R.
      • Palencia H.
      • Schroeder S.D.
      • DeMontigny B.A.
      • Takacs J.M.
      • Rasche M.E.
      • Miner J.L.
      • Ragsdale S.W.
      Targeting methanopterin biosynthesis to inhibit methanogenesis.
      );

      Machmüller, A., M. Tavendale, J. Lee, H. Clark, and L. Meagher. 2007. Review of inhibitors of methane production. Chapter 2 in Rumen Ecology, Pastoral Greenhouse Gas Research Consortium 2002–2007 Review, New Zealand. Accessed June 27, 2013. http://www.pggrc.co.nz/Portals/0/annual%20reports/PGgRc_5yearfull%20chapter%202.pdf

      )
      Bacteriocins (bovicin HC5)50
      • Lee S.S.
      • Hsu J.-T.
      • Mantovani H.C.
      • Russell J.B.
      The effect of bovicin HC5, a bacteriocin from Streptococcus bovis HC5, on ruminal methane production in vitro.
      )
      Bacteriophage
      • McAllister T.A.
      • Newbold C.J.
      Redirecting rumen fermentation to reduce methanogenesis.
      )
      High host specificity, but none identified that infect ruminal methanogens
      Aspergillus oryzae50Yes
      • Frumholtz P.P.
      • Newbold C.J.
      • Wallace R.J.
      Influence of Aspergillus oryzae fermentation extract on the fermentation of a basal ration in the rumen simulation technique (Rusitec).
      )
      Saccharomyces cerevisiae10Yes
      • Mutsvangwa T.
      • Edwards I.E.
      • Topps J.H.
      • Paterson G.F.M.
      The effect of dietary inclusion of yeast culture (Yea-Sacc) on patterns of rumen fermentation, food intake and growth of intensively fed bulls.
      )
      Exogenous fibrolytic enzymes14–43Yes
      • Dong Y.
      • Bae H.D.
      • McAllister T.A.
      • Mathison G.W.
      • Cheng K.-J.
      Effects of exogenous fibrolytic enzymes, α-bromoethanesulfonate and monensin on fermentation in a rumen simulation (RUSITEC) system.
      );
      • Giraldo L.A.
      • Ranilla M.J.
      • Tejido M.L.
      • Carro M.D.
      Influence of exogenous fibrolytic enzymes and fumarate on methane production, microbial growth, and fermentation in Rusitec fermenters.
      ,
      • Giraldo L.A.
      • Ranilla M.J.
      • Tejido M.L.
      • Carro M.D.
      Effects of exogenous cellulase supplementation on microbial growth and ruminal fermentation of a high-forage diet in Rusitec fermenters.
      )
      1 In addition to the references given, extensive reviews are available (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ;
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      ;
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      ;
      • Martin C.
      • Morgavi D.P.
      • Doreau M.
      Methane mitigation in ruminants: From microbe to farm scale.
      ;
      • Hristov A.N.
      • Oh J.
      • Lee C.
      • Meinen R.
      • Montes F.
      • Ott T.
      • Firkins J.
      • Rotz A.
      • Dell C.
      • Adesogan A.
      • Yang W.
      • Tricarico J.
      • Kebreab E.
      • Waghorn G.
      • Dijkstra J.
      • Oosting S.
      • et al.
      Mitigation of greenhouse gas emissions in livestock production: A review of technical options for non-CO2 emissions.
      ).
      Table 3Summary of rumen modifiers that have been tested in vivo
      For sheep, goats, and beef cattle, CH4 reduction is given as grams per head per day relative to the control and growth rates may or may not have been affected. For dairy cattle, CH4 reduction is given as grams of CH4 per kilogram of ECM relative to the control. Extensive reviews can be found in Van Nevel and Demeyer (1996), Boadi et al. (2004), Beauchemin et al. (2008), Martin et al. (2010), and Hristov et al. (2013).
      Approach/compoundCH4 reduction relative to controlTransient or sustained effect (>30 d)
      If cell is blank, the experiment was either not designed to test whether effect on CH4 reduction was transient or sustained or the experiment was less than 30d in duration.
      Animal toxicityReferencesComments
      Monensin4 to 10%Sustained in one study; transient in the rest of the studiesNone at recommended feeding levels
      • 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.
      );
      • Guan H.
      • Wittenberg K.M.
      • Ominski K.H.
      • Krause D.O.
      Efficacy of ionophores in cattle diets for mitigation of enteric methane.
      );
      • 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.
      );
      • Beauchemin K.A.
      • Kreuzer M.
      • O’Mara F.
      • McAllister T.A.
      Nutritional management for enteric methane abatement: A review.
      )
      CH4 reductions achieved at feeding levels of 24 to 35 mg/kg (above feeding levels currently approved in the United States)
      Monensin controlled-release capsules0%No effectNone
      • Moate P.J.
      • Clarke T.
      • Davis L.H.
      • Laby R.H.
      Rumen gases and bloat in grazing dairy cattle.
      );
      • Grainger C.
      • Auldist M.J.
      • Clarke T.
      • Beauchemin K.A.
      • McGinn S.M.
      • Hannah M.C.
      • Eckard R.J.
      • Lowes L.B.
      Use of monensin controlled-release capsules to reduce methane emissions and improve milk production of dairy cows offered pasture supplemented with grain.
      );
      • Waghorn G.C.
      • Clark H.
      • Taufa V.
      • Cavanagh A.
      Monensin controlled-release capsules for methane mitigation in pasture-fed dairy cows.
      )
      One study was short-term (<14 d); the others were long-term (11 and ~29 wk)
      Halogenated CH4 analogs80 to 100%Sustained in 1 study; transient in the rest of the studiesYes
      • McCrabb G.J.
      • Berger K.T.
      • Magner T.
      • May C.
      • Hunter R.A.
      Inhibiting methane production in Brahman cattle by dietary supplementation with a novel compound and the effects on growth.
      );
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      );
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      );
      • McAllister T.A.
      • Newbold C.J.
      Redirecting rumen fermentation to reduce methanogenesis.
      )
      Reduced feed intake in beef cattle with improved feed efficiency
      9,10-Anthraquinone50%Tissue residues
      • Kung Jr., L.
      • Smith K.A.
      • Smagala A.M.
      • Endres K.M.
      • Bessett C.A.
      • Ranjit N.K.
      • Yaissle J.
      Effects of 9,10 anthraquinone on ruminal fermentation, total-tract digestion, and blood metabolite concentrations in sheep.
      )
      Dicarboxylic acids50 to 75% in 1 study; 0% in othersTransientPossible sodium toxicity if sodium salt is used
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      );
      • Boadi D.
      • Benchaar C.
      • Chiquette J.
      • Masse D.
      Mitigation strategies to reduce enteric methane emissions from dairy cows: Update review.
      );
      • McGinn S.M.
      • Beauchemin K.A.
      • Coates T.
      • Colombatto D.
      Methane emissions from beef cattle: Effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid.
      );
      • Mohammed N.
      • Lila Z.A.
      • Ajisaka N.
      • Hara K.
      • Mikuni K.
      • Kanda S.
      • Itabashi H.
      Inhibition of ruminal microbial methane production by β-cyclodextrin iodopropane, malate and their combination in vitro.
      );
      • Beauchemin K.A.
      • McGinn S.M.
      Methane emissions from beef cattle: Effects of fumaric acid, essential oil, and canola oil.
      );
      • Wallace R.J.
      • Wood T.A.
      • Rowe A.
      • Price J.
      • Yanez D.R.
      • Williams S.P.
      • Newbold C.J.
      Encapsulated fumaric acid as a means of decreasing ruminal methane emissions.
      );
      • McAllister T.A.
      • Newbold C.J.
      Redirecting rumen fermentation to reduce methanogenesis.
      );
      • Foley P.A.
      • Kenny D.A.
      • Lovett D.K.
      • Callan J.J.
      • Boland T.M.
      • O’Mara F.P.
      Effect of dl-malic acid supplementation on feed intake, methane emissions, and performance of lactating dairy cows at pasture.
      );
      • Molano G.
      • Knight T.W.
      • Clark H.
      Fumaric acid supplements have no effect on methane emissions per unit of feed intake in wether lambs.
      )
      Also expensive
      Essential oils0 to 19%
      • Mohammed N.
      • Ajisaka N.
      • Lila Z.A.
      • Hara K.
      • Mikuni K.
      • Hara K.
      • Kanda S.
      • Itabashi H.
      Effect of Japanese horseradish oil on methane production and ruminal fermentation in vitro and in steers.
      );
      • Beauchemin K.A.
      • McGinn S.M.
      Methane emissions from beef cattle: Effects of fumaric acid, essential oil, and canola oil.
      )
      May require encapsulation to slow volatilization; see also reviews by
      • Calsamiglia S.
      • Busquet M.
      • Cardozo P.W.
      • Castillejos L.
      • Ferret A.
      Invited review: Essential oils as modifiers of rumen microbial fermentation.
      ) and
      • Benchaar C.
      • Calsamiglia S.
      • Chaves A.V.
      • Fraser G.R.
      • Colombatto D.
      • McAllister T.A.
      • Beauchemin K.A.
      A review of plant-derived essential oils in ruminant nutrition and production.
      )
      Saponins0 to 16%
      • Hess H.D.
      • Beuret R.A.
      • Lötscher M.
      • Hindrichsen I.K.
      • Machmüller A.
      • Carulla J.E.
      • Lascano C.E.
      • Kreuzer M.
      Ruminal fermentation, methanogenesis and nitrogen utilization of sheep receiving tropical grass hay-concentrate diets offered with Sapindus saponaria fruits and Cratylia argentea foliage.
      );
      • Santoso B.
      • Mwenya B.
      • Sar C.
      • Gamo Y.
      • Kobayashi T.
      • Morikawa R.
      • Kimura K.
      • Mizukoshi H.
      • Takahashi J.
      Effects of supplementing galactooligosaccharides, Yucca schidigera or nisin on rumen methanogenesis, nitrogen and energy metabolism in sheep.
      );
      • Lila Z.A.
      • Mohammed N.
      • Kanda S.
      • Kurihara M.
      • Itabashi H.
      Sarsaponin effects on ruminal fermentation and microbes, methane production, digestibility and blood metabolites in steers.
      );
      • Pen B.
      • Takaura K.
      • Yamaguchi S.
      • Asa R.
      • Takahashi J.
      Effects of Yucca schidigera and Quillaja saponaria with or without β 1-4 galacto-oligosaccharides on ruminal fermentation, methane production and nitrogen utilization in sheep.
      );
      • Holtshausen L.
      • Chaves A.V.
      • Beauchemin K.A.
      • McGinn S.M.
      • McAllister T.A.
      • Odongo N.E.
      • Cheeke P.R.
      • Benchaar C.
      Feeding saponin-containing Yucca schidigera and Quillaja saponaria to decrease enteric methane production in dairy cows.
      );
      • Wang C.J.
      • Wang S.P.
      • Zhou H.
      Influences of flavomycin, ropadiar, and saponin on nutrient digestibility, rumen fermentation, and methane emission from sheep.
      )
      Only short-term studies
      Condensed tannins12 to 46% in sheep and goats; 0% in beef cattle; 0 to 26% in dairy cattleNone
      • Woodward S.L.
      • Waghorn G.C.
      • Lassey K.R.
      • Laboyrie P.G.
      Does feeding sulla (Hedysarum coronarium) reduce methane emissions from dairy cows?.
      );
      • Carulla J.E.
      • Kreuzer M.
      • Machmüller A.
      • Hess H.D.
      Supplementation of Acacia mearnsii tannins decreases methanogenesis and urinary nitrogen in forage-fed sheep.
      );
      • Hess H.D.
      • Tiemann T.T.
      • Noto F.
      • Carulla J.E.
      • Kreuzer M.
      Strategic use of tannins as means to limit methane emission from ruminant livestock.
      );
      • Beauchemin K.A.
      • McGinn S.M.
      • Martinez T.F.
      • McAllister T.A.
      Use of condensed tannin extract from quebracho trees to reduce methane emissions from cattle.
      );
      • de Oliveira S.G.
      • Berchielli T.T.
      • dos Santos Pedreira M.
      • Primavesi O.
      • Frighetto R.
      • Lima M.A.
      Effect of tannin levels in sorghum silage and concentrate supplementation on apparent digestibility and methane emission in beef cattle.
      );
      • Animut G.
      • Puchala R.
      • Goetsch A.L.
      • Patra A.K.
      • Sahlu T.
      • Varel V.H.
      • Wells J.
      Methane emission by goats consuming diets with different levels of condensed tannins from lespedeza.
      );
      • Grainger C.
      • Clarke T.
      • Auldist M.J.
      • Beauchemin K.
      • McGinn S.
      • Waghorn G.C.
      • Eckard R.J.
      Potential use of Acacia mearnsii condensed tannins to reduce methane emissions and nitrogen excretion from grazing dairy cows.
      )
      Potential negative effect on protein nutrition, fiber digestibility, and milk yield; see also review by
      • Waghorn G.
      Beneficial and detrimental effects of dietary condensed tannins for sustainable sheep and goat production—Progress and challenges.
      )
      Nitrate and sulfate16 to 57%Sustained (1 study)Yes
      • Sar C.
      • Santoso B.
      • Mwenya B.
      • Gamo Y.
      • Kobayashi T.
      • Morikawa R.
      • Kimura K.
      • Mizukoshi H.
      • Takahashi J.
      Manipulation of rumen methanogenesis by the combination of nitrate with β1-4 galacto-oligosaccharides or nisin in sheep.
      );
      • van Zijderveld S.M.
      • Gerrits W.J.J.
      • Apajalahti J.A.
      • Newbold J.R.
      • Dijkstra J.
      • Leng R.A.
      • Perdok H.B.
      Nitrate and sulfate: Effective alternative hydrogen sinks for mitigation of ruminal methane production in sheep.
      ,
      • van Zijderveld S.M.
      • Gerrits W.J.J.
      • Dijkstra J.
      • Newbold J.R.
      • Hulshof R.B.A.
      • Perdok H.B.
      Persistency of methane mitigation by dietary nitrate supplementation in dairy cows.
      )
      As electron acceptors, these compounds have to be supplied in stoichiometric proportions, which may make them unrealistic (
      • Weimer P.J.
      Manipulating ruminal fermentation: A microbial ecological perspective.
      ); risk of nitrite toxicity
      Nitro-ethane and 2-nitropropanol0% to 23% in steersTransient
      • Anderson R.C.
      • Carstens G.E.
      • Miller R.K.
      • Callaway T.R.
      • Schultz C.L.
      • Edrington T.S.
      • Harvey R.B.
      • Nisbet D.J.
      Effect of nitroethane administration on ruminal VFA production and specific activity of methane production.
      );
      • Anderson R.C.
      • Carstens G.E.
      • Miller R.K.
      • Callaway T.R.
      • Schultz C.L.
      • Edrington T.S.
      • Harvey R.B.
      • Nisbet D.J.
      Effect of oral nitroethane and 2-nitropropanol administration on methane-producing activity and volatile fatty acid production in the ovine rumen.
      );
      • Gutierrez-Bañuelos H.
      • Anderson R.C.
      • Carstens G.E.
      • Slay L.J.
      • Ramlachan N.
      • Horrocks S.M.
      • Callaway T.R.
      • Edrington T.S.
      • Nisbet D.J.
      Zoonotic bacterial populations, gut fermentation characteristics and methane production in feedlot steers during oral nitroethane treatment and after the feeding of an experimental chlorate product.
      );
      • Anderson R.C.
      • Krueger N.A.
      • Stanton T.B.
      • Callaway T.R.
      • Edrington T.S.
      • Harvey R.B.
      • Jung Y.S.
      • Nisbet D.J.
      Effects of select nitrocompounds on in vitro ruminal fermentation during conditions of limiting or excess added reductant.
      );
      • Brown E.G.
      • Anderson R.C.
      • Carstens G.E.
      • Gutierrez-Bañuelos H.
      • McReynolds J.L.
      • Slay L.J.
      • Callaway T.R.
      • Nisbet D.J.
      Effects of oral nitroethane administration on enteric methane emissions and ruminal fermentation in cattle.
      )
      Acetogens100%SustainedNone
      • Fonty G.
      • Joblin K.
      • Chavarot M.
      • Roux R.
      • Naylor G.
      • Michallon F.
      Establishment and development of ruminal hydrogenotrophs in methanogen-free lambs.
      )
      Only demonstrated in gnotobiotically raised lambs; likely requires elimination of methanogens
      Saccharomyces cerevisiae0%None
      • McGinn S.M.
      • Beauchemin K.A.
      • Coates T.
      • Colombatto D.
      Methane emissions from beef cattle: Effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid.
      )
      • Hristov A.N.
      • Varga G.
      • Cassidy T.
      • Long M.
      • Heyler K.
      • Karnati S.K.
      • Corl B.
      • Hovde C.J.
      • Yoon I.
      Effect of Saccharomyces cerevisiae fermentation product on ruminal fermentation and nutrient utilization in dairy cows.
      );
      • Chung Y.-H.
      • Walker N.D.
      • McGinn S.M.
      • Beauchemin K.A.
      Differing effects of 2 active dried yeast (Saccharomyces cerevisiae) strains on ruminal acidosis and methane production in nonlactating dairy cows.
      )
      Direct-fed microbes18%None
      • Takahashi J.
      • Chaudhry A.S.
      • Beneke R.G.
      • Suhubdy
      • Young B.A.
      Modification of methane emission in sheep by cysteine and a microbial preparation.
      )
      Defaunation10 to 40%SustainedYes
      • Morgavi D.P.
      • Forano E.
      • Martin C.
      • Newbold C.J.
      Microbial ecosystem and methanogenesis in ruminants.
      ); many others
      Decreased NDF digestibility
      Nisin10%None
      • Santoso B.
      • Mwenya B.
      • Sar C.
      • Gamo Y.
      • Kobayashi T.
      • Morikawa R.
      • Kimura K.
      • Mizukoshi H.
      • Takahashi J.
      Effects of supplementing galactooligosaccharides, Yucca schidigera or nisin on rumen methanogenesis, nitrogen and energy metabolism in sheep.
      )
      Immunization against methanogens0 to 8%None
      • 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.
      );
      • Williams Y.J.
      • Rea S.M.
      • Popovski S.
      • Pimm C.L.
      • Williams A.J.
      • Toovey A.F.
      • Skillman L.C.
      • Wright A.-D. G.
      Reponses of sheep to a vaccination of entodinial or mixed rumen protozoal antigens to reduce rumen protozoal numbers.
      )
      • Williams Y.J.
      • Popovski S.
      • Rea S.M.
      • Skillman L.C.
      • Toovey A.F.
      • Northwood K.S.
      • Wright A.D.
      A vaccine against rumen methanogens can alter the composition of archaeal populations.
      )
      1 For sheep, goats, and beef cattle, CH4 reduction is given as grams per head per day relative to the control and growth rates may or may not have been affected. For dairy cattle, CH4 reduction is given as grams of CH4 per kilogram of ECM relative to the control. Extensive reviews can be found in
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ),
      • 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.
      ),
      • Martin C.
      • Morgavi D.P.
      • Doreau M.
      Methane mitigation in ruminants: From microbe to farm scale.
      ), and
      • Hristov A.N.
      • Oh J.
      • Lee C.
      • Meinen R.
      • Montes F.
      • Ott T.
      • Firkins J.
      • Rotz A.
      • Dell C.
      • Adesogan A.
      • Yang W.
      • Tricarico J.
      • Kebreab E.
      • Waghorn G.
      • Dijkstra J.
      • Oosting S.
      • et al.
      Mitigation of greenhouse gas emissions in livestock production: A review of technical options for non-CO2 emissions.
      ).
      2 If cell is blank, the experiment was either not designed to test whether effect on CH4 reduction was transient or sustained or the experiment was less than 30 d in duration.
      Several reviews have summarized the potential of using rumen modifiers on a qualitative basis (
      • Van Nevel C.J.
      • Demeyer D.I.
      Control of rumen methanogenesis.
      ;
      • 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.
      ;
      • Martin C.
      • Morgavi D.P.
      • Doreau M.
      Methane mitigation in ruminants: From microbe to farm scale.
      ;
      • Hristov A.N.
      • Oh J.
      • Lee C.
      • Meinen R.
      • Montes F.
      • Ott T.
      • Firkins J.
      • Rotz A.
      • Dell C.
      • Adesogan A.
      • Yang W.
      • Tricarico J.
      • Kebreab E.
      • Waghorn G.
      • Dijkstra J.
      • Oosting S.
      • et al.
      Mitigation of greenhouse gas emissions in livestock production: A review of technical options for non-CO2 emissions.
      ). Many of these CH4 reduction strategies have not been evaluated to determine the sustained effects of the additive, the appropriate in vivo dose, or the economics of the approach in terms of effect on milk production, all of which are important considerations for large-scale implementation. To date, no feed additives have demonstrated sustained reduction in CH4 emissions without a negative effect on milk production in lactating dairy cattle other than the use of nitrate as an alternative electron acceptor, which has the issue of animal toxicity (Table 3;
      • van Zijderveld S.M.
      • Gerrits W.J.J.
      • Dijkstra J.
      • Newbold J.R.
      • Hulshof R.B.A.
      • Perdok H.B.
      Persistency of methane mitigation by dietary nitrate supplementation in dairy cows.
      ). Successful biological control to reducing CH4 emissions has been achieved with defaunation in sheep, goats, and growing cattle, but has had mixed effects on animal growth (
      • Jouany J.P.
      Effect of rumen protozoa on nitrogen utilization by ruminants.
      ). Given the extensive review of these strategies by others (above) and the focus in this review on quantitative reductions in CH4/ECM, rumen modifiers will not be discussed further. At this time, greater opportunities exist in reducing enteric CH4 emissions from dairy cattle through nutrition, feeding management, genetic selection, and improvements in herd health and productivity than with the use of feed additives as rumen modifiers (
      • Waghorn G.C.
      Can livestock production be increased without increasing greenhouse gas emissions?.
      ). However, research should continue in identifying and developing rumen modifiers because of its value in elucidating rumen microbial interactions and increasing our knowledge of rumen function.

      Genetic Approaches to Increasing Productivity and Reducing CH4/ECM

      Differences between individual animals in plant selection during grazing, rumen digesta retention rates, and host-microbe interactions may be heritable and thus amenable to genetic selection for animals with lesser enteric CH4 emissions on a per-day or per-DMI basis (
      • Pinares-Patiño C.S.
      • Waghorn G.C.
      • Machmüller A.
      • Vlaming B.
      • Molano G.
      • Cavanagh A.
      • Clark H.
      Methane emissions and digestive physiology of non-lactating dairy cows fed pasture forage.
      ;
      • Clark H.
      Nutritional and host effects on methanogenesis in the grazing ruminant.
      ;
      • Ross E.M.
      • Moate P.J.
      • Marett L.
      • Cocks B.G.
      • Hayes B.J.
      Investigating the effect of two methane-mitigating diets on the rumen microbiome using massively parallel sequencing.
      ). Poor repeatability of some CH4 measurements and high within-animal variation may limit selection on this basis (
      • Pinares-Patiño C.S.
      • Waghorn G.C.
      • Machmüller A.
      • Vlaming B.
      • Molano G.
      • Cavanagh A.
      • Clark H.
      Methane emissions and digestive physiology of non-lactating dairy cows fed pasture forage.
      ;
      • Vlaming J.B.
      • Lopez-Villalobos N.
      • Brookes I.M.
      • Hoskin S.O.
      • Clark H.
      Within- and between-animal variance in methane emissions in non-lactating dairy cows.
      ). Although genetic selection for reduced CH4 emissions has been used in sheep and beef cattle (
      • Hegarty R.S.
      • McEwan J.C.
      Genetic opportunities to reduce enteric methane emissions from ruminant livestock..
      ;
      • Clark H.
      Nutritional and host effects on methanogenesis in the grazing ruminant.
      ;
      • 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.
      ), the relationship between CH4 emissions and animal growth has not been evaluated. Also, although metagenomic tools are being developed that may accelerate the selection process (
      • Ross E.M.
      • Moate P.J.
      • Marett L.
      • Cocks B.G.
      • Hayes B.J.
      Investigating the effect of two methane-mitigating diets on the rumen microbiome using massively parallel sequencing.
      ), to date no published evidence exists supporting the potential for this approach in dairy cattle, and by comparison with genetic selection for residual feed intake, it is likely to take more than 10 yr to develop.
      Widespread consensus exists that increasing the productivity of an animal will decrease the proportion of CH4 produced per unit of product (
      • Johnson D.E.
      • Ward G.M.
      • Ramsey J.J.
      Livestock methane: Current emissions and mitigation potential.
      ;
      • Moss A.R.
      • Jouany J.P.
      • Newbold J.
      Methane production by ruminants: Its contribution to global warming.
      ;
      • 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.
      ;
      • Pinares-Patiño C.S.
      • Waghorn G.C.
      • Hegarty R.S.
      • Hoskin S.O.
      Effects of intensification of pastoral farming on greenhouse gas emissions in New Zealand.
      ;
      • Clark H.
      Nutritional and host effects on methanogenesis in the grazing ruminant.
      ). The Environmental Protection Agency has clearly stated that “Improving livestock productivity so that less CH4 is emitted per unit of product is the most promising and cost-effective technique for reducing emission” (

      EPA (Environmental Protection Agency). 2005. Opportunities to Reduce Anthropogenic Methane Emissions in the United States. Publication 430-R-93-012. EPA, Washington, DC.

      ) and is in concordance with global efforts (Global Research Alliance on Agricultural Greenhouse Gases;
      • Shafer S.R.
      • Walthall C.L.
      • Franzluebbers A.J.
      • Scholten M.
      • Meijs J.
      • Clark H.
      • Reisinger A.
      • Yagi K.
      • Roel A.
      • Slattery B.
      • Campbell I.D.
      • McConkey B.G.
      • Angers D.A.
      • Soussana J.F.
      • Richard G.
      Emergence of the global research alliance on agricultural greenhouse gases.
      ). More-efficient dairy cows will produce more milk relative to the amount of feed ingested and energy lost as CH4 (Figure 6). Production efficiency can be improved by genetic selection and management practices that address not only nutrition and feeding, but also reproduction, heat stress tolerance, disease incidence, culling rates, and heifer replacement programs. Although the effects of genetic selection and management improvements are commonly examined on an individual-cow basis, from a CH4 mitigation perspective, it is more important to view them on a herd-productivity basis. Genetic selection and management approaches detailed below have the potential to increase yield while reducing the number of replacement animals needed, contributing to reduced CH4 production by the herd and increased ECM.

      Genetic Selection for Yield and Energetic Efficiency

      Tremendous progress in genetic selection of dairy cattle has been made over the past 60 yr and, combined with improvements in animal management, has resulted in a 400% increase in North American milk yields (
      • Hansen L.B.
      Consequences of selection for milk yield from a geneticist’s viewpoint.
      ;
      • VanRaden P.M.
      Invited review: Selection on net merit to improve lifetime profit.
      ;
      • Shook G.E.
      Major advances in determining appropriate selection goals.
      ;
      • Capper J.L.
      • Cady R.A.
      • Bauman D.E.
      The environmental impact of dairy production: 1944 compared with 2007.
      ). This increase in milk yield is paralleled by a corresponding 64% reduction in the US dairy cattle population and 57% reduction in CH4 emitted per unit of product (
      • Capper J.L.
      • Cady R.A.
      • Bauman D.E.
      The environmental impact of dairy production: 1944 compared with 2007.
      ). Genetic selection has also increased milk yields in other countries and regions, including Argentina, Chile, Australia, New Zealand, Israel, and the European Union (
      • VanRaden P.M.
      Invited review: Selection on net merit to improve lifetime profit.
      ;

      FAOSTAT. 2014. Time series and cross sectional data relating to food and agriculture for some 200 countries. Accessed Feb. 21, 2014. http://faostat.fao.org/site/291/default.aspx

      ). Although remarkable gains have been made in milk yield through genetic selection, no indication exists that the genetic potential for milk yield is approaching a maximum (
      • Cole J.B.
      • VanRaden P.M.
      Use of haplotypes to estimate Mendelian sampling effects and selection limits.
      ). Cow-to-cow variation is large (SD = ±2,500 kg/lactation), indicating that substantial heterogeneity still exists in the population to permit selection.
      On an individual-cow basis, CH4/ECM can be reduced by 3 different approaches. The first is to increase milk yield per cow with correspondingly smaller increases in DMI, which dilutes the maintenance energy costs of the cow and increases gross energy efficiency. The second is to reduce body size without reducing yields of milk and milk components, which also has the effect of increasing gross energy efficiency, but by decreasing the maintenance energy requirements of the animal. The third is to select for residual feed intake or residual solids production, which are both measures of feed efficiency. These approaches are all based on the concept that maintenance energy is a fixed cost and a function of body size. Because CH4 production is proportional to the energy intake of the animal, reducing the proportion of energy utilized for maintenance while maintaining or increasing milk yield would decrease CH4/ECM.
      Genetic selection over the past 6 decades has been based largely on the first approach, with increasing yields of milk and milk fat. Selection for yields of milk protein has been implemented over the past 2 decades in the US dairy industry. Reductions in enteric CH4/ECM with genetic selection for milk yield follow a diminishing returns pattern (Figure 6). Predictions are based on a 680-kg Holstein cow producing milk with 3.7% milk fat and 3.0% true protein. Predictions for other breeds will follow a similar pattern, albeit at different milk yields. Dry matter intake was calculated using [1], [2] (
      NRC
      ; page 4). Methane production was calculated at 3 levels of GEI that are within the range observed in the published literature and currently being used for US regional estimates by the Environmental Protection Agency (
      • Kebreab E.
      • Johnson K.A.
      • Archibeque S.L.
      • Pape D.
      • Wirth T.
      Model for estimating enteric methane emissions from United States dairy and feedlot cattle.
      ;

      EPA (Environmental Protection Agency). 2011b. Inventory of U. S. Greenhouse Gas Emissions and Sinks: 1990–2009. Publication 430-R-11–005. EPA, Washington, DC.

      ). Increases of 100 kg of milk per lactation are predicted to result in a 7.3% decrease in CH4/ECM at a 7,000-kg production level, but only 3.1% decrease at a 13,000-kg production level, assuming no change in digestibility or rumen fermentation.
      Although selection for reduced body size is theoretically possible, it has not been widely pursued. The ability to reduce body size while maintaining milk yield is limited due to the amount of feed that can be consumed by smaller animals. Also, a smaller animal contributes less to the beef supply. Currently in the United States, Holstein steers and culled dairy cows of all breeds account for 22% of domestically produced beef. In Europe, dairy animals account for 50% of the beef supply (
      • Zehetmeier M.
      • Baudracco J.
      • Hoffmann H.
      • Heißenhuber A.
      Does increasing milk yield per cow reduce greenhouse gas emissions? A system approach.
      ) and worldwide, meat from dairy breed animals is estimated to be 57% of the beef supply (
      FAO (Food and Agriculture Organization of the United Nations)
      ).
      Although it is often speculated in the dairy industry that Jersey cows are more energy efficient than Holsteins due to their smaller body sizes and higher content of milk solids, the research literature does not generally support this concept. Research on energy metabolism of mature Jersey and Holstein cows did not show any breed differences for maintenance and production requirements per unit of metabolic BW (BW0.75;

      Tyrrell, H. F., C. K. Reynolds, and H. D. Blaxter. 1991. Utilization of dietary energy by Jersey compared to Holstein cows during the lactation cycle. Proc. 12th Symp. Energy Metabolism of Farm Animals. EAAP Publ. 58. European Federation for Animal Science (EAAP), Rome, Italy.

      ). Consequently, CH4 production per unit of milk was not different between the 2 breeds. In a 3-breed comparison with direct measurements of CH4 and milk production, no differences were found between Jerseys and Holsteins in CH4 per DMI or CH4/ECM (
      • Münger A.
      • Kreuzer M.
      Methane emission as determined in contrasting dairy cattle breeds over the reproduction cycle.
      ). The third breed, Simmental, had similar CH4 per DMI but more CH4/ECM during lactation as a consequence of the lower milk production as a proportion of body size and correspondingly greater proportio