Summary and Keywords
Agriculture is a significant source of methane, contributing about 12% of the global anthropogenic methane emissions. Major sources of methane from agricultural activities are fermentation in the reticulo-rumen of ruminant animals (i.e., enteric methane), fermentation in animal manure, and rice cultivation. Enteric methane is the largest agricultural source of methane and is mainly controlled by feed dry matter intake and composition of the animal diet (i.e., fiber, starch, lipids). Processes that lead to generation of methane from animal manure are similar to those taking place in the reticulo-rumen. Methane emissions from manure, however, are greatly influenced by factors such as manure management system and ambient temperature. Systems that handle manure as a liquid generate much more methane than systems in which manure is handled as a solid. Low ambient temperatures drastically decrease methane emissions from manure. Once applied to soil, animal manure does not generate significant amounts of methane. Globally, methane emissions from rice cultivation represent about 10% of the total agricultural greenhouse gas emissions. In the rice plant, methane dissolves in the soil water surrounding the roots, diffuses into the cell-wall water of the root cells, and is eventually released through the micropores in the leaves. Various strategies have been explored to mitigate agricultural methane emissions. Animal nutrition, including balancing dietary nutrients and replacement of fiber with starch or lipids; alternative sinks for hydrogen; manipulation of ruminal fermentation; and direct inhibition of methanogenesis have been shown to effectively decrease enteric methane emissions. Manure management solutions include solid-liquid separation, manure covers, flaring of generated methane, acidification and cooling of manure, and decreasing manure storage time before soil application. There are also effective mitigation strategies for rice that can be categorized broadly into selection of rice cultivars, water regime, and fertilization. Alternate wetting and drying and mid-season drainage of rice paddies have been shown to be very effective practices for mitigating methane emissions from rice production.
Agriculture is a major contributor to anthropogenic greenhouse gas (GHG) emissions. Globally, it is estimated that agricultural activities contributed 5.0 to 5.8 Gt of carbon dioxide equivalent (CO2eq)/yr in 2000–2010, which is about 12% of the total anthropogenic emissions (Intergovernmental Panel on Climate Change [IPCC], 2014). The two major non–carbon dioxide GHGs emitted from agricultural activities are methane and nitrous oxide. Methane is a potent, short-lived (12.2 years; Myhre et al., 2013) GHG emitted from various sources, including fossil fuel-related activities, livestock operations, rice production, landfills, and others. According to the US Environmental Protection Agency (USEPA) (2017), the top three sources of anthropogenic methane in the United States are the energy sector (natural gas, petroleum systems, and coal mining; 40%), livestock (36%), and landfills (18%). Due to methane’s high global warming potential (USEPA, 2017 indicates that methane’s is 25 times that of carbon dioxide for the 100-year time horizon) and its short lifespan in the atmosphere, methane and agriculture become prime targets for mitigation efforts aimed at a quick (relative to other technologies) impact on climate change.
Agricultural methane emissions can come from enteric fermentation in ruminant animals, fermentation processes in animal manure (mostly during storage), rice cultivation, and field burning of crop residues. In the United States, the relative contribution of these sources to the total agricultural methane emissions is 68, 27, 4.6, and about 0.1%, respectively (USEPA, 2017). Globally, methane emissions from enteric fermentation are estimated at 73.5% of the total methane emissions from agriculture, methane emissions from manure management are 7.2%, emissions from rice cultivation are 18.5%, and emissions from burning crop residues are 0.8% (Food and Agriculture Organization of the United Nations [FAO], 2017). On a CO2eq basis, methane emissions from agriculture represent around 56% of the global agricultural GHG emissions (FAO, 2017).
Methane Emissions From Enteric Fermentation
Enteric fermentation, in the context of methane emissions from agriculture, is a term referring to microbial fermentation in the forestomach of ruminant animals. Methane can also be produced from enteric fermentation in the digestive tract of non-ruminant herbivore animals, such as horses, donkeys, and mules, as a result of fermentation processes in their hindgut. Hindgut fermenters, however, do not produce nearly as much methane per unit of fermented feed as ruminants. The Intergovernmental Panel on Climate Change (IPCC) (2006) assumes enteric methane emissions from horses and mules/asses at 18 and 10 kg/head per year, respectively (compared with 128 kg for a high-producing dairy cow). With the world horse population at around 38 million and an additional 18 million asses and 6 million mules (FAO, 2017), global enteric methane emissions from these animals can be estimated at about 0.6% of the total agricultural methane emissions.
Another point to consider with respect to enteric emissions is that wild ruminants (bison, deer, elk, moose, antelopes, giraffe, etc.) have similar methanogenesis processes in their forestomach and also emit enteric methane. Currently, enteric methane emissions from this group of animals are low; as an example, emissions from wild ruminants in the United States were estimated at around 4.3% of the total methane emissions from farmed ruminants (Hristov, 2012). Before the European settlement of the West, however, emissions from wild ruminants (predominantly the bison) in the United States were comparable (depending on the assumed size of bison population) to current emissions from cattle (Hristov, 2012).
Methane synthesis in ruminants is a result of a unique symbiotic relationship between the host animal and the microbial populations (bacteria, protozoa, archaea, and fungi) inhabiting its reticulo-rumen (the largest compartment of the complex stomach of a ruminant animal). One of nature’s wonders, this relationship provides the rumen microbes with a stable, nutrient-rich, and anaerobic (i.e., oxygen-free) environment and the host animal with a continuous source of energy, in the form of volatile fatty acids (VFA), and amino acids (from microbial protein synthesized in the reticulo-rumen that is digested and absorbed in the small intestine).
The main end products of microbial fermentation of carbohydrates in the reticulo-rumen are VFA, methane, and carbon dioxide. Alcohols and lactate are also formed during these processes, but it is generally recognized that they are relatively unimportant in the rumen (except in cases when lactate accumulates, causing rumen acidosis). Formation of methane through the hydrogenotrophic pathway is a mechanism that provides energy to the methanogenic archaea and is the most important hydrogen sink in the rumen. Hydrogen is an end product of the fermentation process, and it has been shown that its accumulation inhibits re-oxidation of co-factors and consequently rumen fermentation (Wolin, Miller, & Stewart, 1997). Although alternative sinks (acetogenesis, for example) for hydrogen do exist in other environments, these processes appear to be of little significance in the rumen (Russell & Wallace, 1997) due to usually low hydrogen concentrations. Production of the major VFA (acetate, propionate, and butyrate) yields various amounts of hydrogen with propionate being a hydrogen sink and thereby decreasing the overall amount of hydrogen available to reduce carbon dioxide to methane. The predominant methanogenic archaea in the rumen are hydrogenotrophic Methanobrevibacter spp., Methanosphaera, Methanobacterium, and Methanomicrobium. A new group of methylotrophic methanogens (Order Thermoplasmatales; the so-called rumen cluster-C) that do not require hydrogen but depend on methyl amines for energy has been described and appears to play a role in methane formation in ruminants (Poulsen et al., 2013).
Because hydrogen is a product of VFA formation, a theoretical fermentation balance for a given molar distribution of fermentation acids can be developed. Assuming VFA molar proportions of 0.65 (acetate), 0.20 (propionate), and 0.15 (butyrate), Wolin (1960) estimated that 1 mol of total VFA arises from fermentation of 0.575 moles of glucose and is associated with 0.60 moles of carbon dioxide and 0.35 moles of methane. In other words, in this example, 1 mol of glucose yields 0.61 moles of methane. This stoichiometric balance is valid only under two general assumptions: (1) that all excess hydrogen appears as methane, which excludes alternative sinks coming naturally with the feed or added to the diet for mitigation purposes, and that no hydrogen accumulates and is expired; and (2) that microbial growth, which may provide an alternative sink for hydrogen in microbial protein and lipids, is not considered.
Enteric methane production in the ruminant animal is driven by dry matter intake (DMI). Various meta-analyses and prediction models have consistently shown that DMI alone is sufficient to predict methane emissions in beef or dairy cattle (Charmley et al., 2016; Hristov et al., 2013). Inclusion of additional animal (body weight, milk production, etc.) or dietary (fiber, fat, starch concentrations) factors improves prediction accuracy (Niu et al., 2017), but this information may not always be readily available, particularly for extensive livestock production systems. Digesta passage rate can also have an effect on enteric methane production. Cold exposure, for example, has been shown to increase passage rate/decrease retention time in the rumen and decrease methane production at the same DMI (Kennedy & Milligan, 1978). On a DMI basis, a dairy cow will produce around 19–20 g methane/kg DMI, whereas a beef cow (fed a higher- or all-forage diet) will produce around 22 g methane/kg DMI. Beef cattle fed high-grain diets, as is the practice in US feedlots, will produce much less methane, around 9–10 g/kg DMI per day (Hristov et al., 2017). With typical DMI ranging from 18 to 27 kg/d, an average lactating dairy cow in the intensive production system in the United States will emit about 430–440 g methane/d (260 to 640 g/d, lower and upper uncertainty bounds, respectively). A non-lactating dairy cow will produce about 40% less methane than a lactating cow due to her lower DMI (partially counteracted by higher fiber content of dry cow diets). For beef cows, the range in daily enteric methane emissions is from about 140 to 280 g/d. Feedlot cattle produce from around 60 to 160 g methane/d (all data from Hristov et al., 2017). Small ruminants, such as sheep and goats, produce considerably less enteric methane, and their impact on the total livestock emissions from enteric fermentation is small, in the United States about 0.8% of the total. Globally, sheep and goats’ contribution to eneteric methane emissions is around 12% (FAO, 2017) due to their relatively greater numbers in Africa, Asia, and Oceania.
Methane Emissions From Manure Management
Processes similar to those taking place in the rumen, methanogenic archaea converting hydrogen and carbon dioxide into methane under anaerobic conditions, drive methane production from animal manure. Before methanogens can proliferate, the substrate (the organic matter in animal manure or other feedstock) has to be converted, through hydrolysis and fermentation, to fermentation end products such as VFA and fermentation gases. Archaea in manure originate from the digestive tract of the animal (reticulo-rumen or the large intestine) and can be classified into hydrogenotrophic (i.e., utilizing hydrogen) or acetoclastic (utilizing acetate). Unlike the rumen, acetate is a major substrate for methanogenesis in manure (or anaerobic digesters). Methanosaeta spp. or Methanosarcina spp. are dominant species in methane digesters; prevalence of one group or the other depends on acetate concentration (Methanosarcina spp. have low affinity for acetate). Factors such as substrate availability, pH, and temperature determine methane generated from manure. Low pH and low temperature inhibit methanogenesis. Anaerobiosis is created in stored manure, particularly in facilities in which manure is handled as liquid and, therefore, there is considerably more methane emitted from manure stored in lagoons, ponds, tanks, etc., than from solid manure stored, stacked, or composted or manure that is directly deposited on pasture (USEPA, 2017). There is very little methane emitted following land application of manure due to aerobic conditions in soil. For the same reason, manure from grazing ruminants does not produce significant quantities of methane.
Livestock production systems that are based on handling manure as liquid result in much greater methane emissions from manure than systems in which manure is either directly deposited on soil or handled as solid. As a result, the Intergovernmental Panel on Climate Change (IPCC) (2006) manure methane emission factors for dairy cattle, beef cattle (largely managed on pasture or in dry feedlots), and swine (whose manure is also managed as liquid) are 74, 1.7, and 14.5 kg methane/head per year, respectively (USEPA, 2017). It is possible that manure methane emissions from dairy cattle in intensive systems that handle manure as a liquid are underestimated by current IPCC/US Environmental Protection Agency (EPA) inventories. Methane is also emitted from the pen surface of beef cattle feedlots. Emission rates from as low as 0.2 to as high as 38 g methane/head/day have been reported for various regions and management and climatic conditions (Bai, Flesch, McGinn, & Chen, 2015; Rahman, Borhan, & Swanson, 2013; Redding et al., 2015). These emission rates are much lower than emissions from liquid dairy manure system, but need to be considered in national inventories. As indicated earlier, manure methane emissions from cow-calf operations (i.e., where animals are raised on pasture) are negligible in comparison to the enteric emissions from these beef cattle systems.
Similar to enteric emissions, methane emissions from manure from small ruminants are negligible; IPCC (2006) emission factors for sheep and goats are 0.5 and 0.3 kg methane/head per year. Similarly, methane emissions from poultry manure are insignificant on a per head basis at 0.1 kg methane/head per year (IPCC, 2006). Due to the large poultry population (23.4 billion birds), however, global methane emissions from poultry manure are estimated at 717 Gg/yr, which is about 7% of the total methane emissions from animal manure (FAO, 2017).
Methane Emissions From Rice Production
Rice is a staple food for the majority of the world’s population, and its cultivation produces significant amounts of GHG in the form of methane; emissions of nitrous oxide, another very potent GHG, from rice cultivation are small. In the rice plant, methane dissolved in the soil water surrounding the roots diffuses into the cell-wall water of the root cells, gasifies in the root cortex, and then is mostly released through the micropores in the leaf sheaths (Nouchi, Mariko, & Aoki, 1990). In 2014, there were over 163 million ha of rice worldwide (FAO, 2017). Global GHG emissions from rice cultivation were 523,825 Gg CO2eq/yr in 2014, which is about 10% of the total agricultural emissions (FAO, 2017). Whereas methane emissions from rice in North America and Europe are small (they constitute about 2% of the total anthropogenic methane emissions in the United States), Southeast Asia contributes 37% of the global GHG emissions from rice cultivation. There are practices based on facilitating oxygen penetration in soil that effectively decrease methane emissions from rice fields, but nitrous oxide emissions, which are low in traditional, continuously flooded systems, tend to increase (Sander, Samson, & Buresh, 2014). Methane can be generated only under anaerobic conditions, and, thus, any practice that prevents anaerobiosis in rice paddies will decrease methane emissions.
Methane Mitigation Options
Comprehensive reviews on enteric and manure methane mitigation techniques have been published (Boadi, Benchaar, Chiquette, & Massé, 2004; Cottle, Nolan, & Wiedemann, 2011; Hristov et al., 2013; Martin, Doreau, & Morgavi, 2010; Montes et al., 2013). The reviews by Hristov et al. (2013) and Montes et al. (2013) were extensively used here.
Enteric Methane Mitigation
Increasing forage digestibility and animal production reduce the overall intensity of greenhouse gas (GHG) emissions from rumen fermentation and stored manure. For example, enteric methane emissions may be reduced when corn silage replaces grass silage in the diet. Legume silages may also have an advantage over grass silage due to their lower fiber content and the additional benefit of replacing inorganic nitrogen fertilizer. Effective silage preservation will improve forage quality and reduce GHG emission efficiency. Dietary lipids have been shown to be effective in reducing enteric methane emissions. Inclusion of lipids in the diet of ruminants should, however, be done with caution as feed intake and consequently animal productivity may decrease. In dairy cows, lipids may also have an adverse effect on milk components (i.e., fat and protein). Inclusion of concentrate feeds in the diet of ruminants will likely decrease the intensity of enteric methane emissions, particularly when the inclusion is above 40% of DMI; at system level, however, feeding more concentrate feeds may, depending on the production system, increase whole-farm GHG emissions. Similar to lipids, this intervention may have negative effects on fiber digestibility and milk components. Supplementation with small amounts of concentrate feed is expected to increase animal production and decrease the intensity of methane emissions when added to all-forage diets. In some parts of the world, improving the nutritive value of low-quality forages or by-products can have a considerable benefit on herd productivity while keeping overall methane output constant. Chemical treatment of low-quality feeds, strategic supplementation of the diet, ration balancing, and crop selection for straw quality may also present effective mitigation strategies.
Nitrates have been shown to be effective enteric methane mitigation agents, particularly in low-protein diets that can benefit from nitrogen supplementation. More research is needed to fully understand the impact of nitrates on whole-farm GHG emissions, animal production, and animal health. Adaptation to these compounds is critical, and toxicity may be an issue. Through their effect on feed efficiency, ionophores are likely to have a moderate methane mitigating effect in ruminants fed high-grain or grain-forage diets. In many parts of the world, however, regulations restrict the availability of this mitigation option. Tannins may also reduce enteric methane emissions, although intake and milk production may be compromised. Other plant-derived bioactive compounds, such as essential oils and saponins, have not been shown to have a consistent methane-mitigating effect. Vaccines against rumen archaea may offer mitigation opportunities in the future, although the extent of methane reduction appears small, and adaptation and persistence of the effect are unknown. An enteric methane inhibitor, 3-nitrooxypropanol, has shown promising results with both beef and dairy cattle. Under industry-relevant conditions, the inhibitor persistently decreased by 30% enteric methane emissions in dairy cows, without negatively affecting animal productivity (Hristov et al., 2015). Similar or even greater mitigation potential has been reported for beef cattle (Romero-Pérez et al., 2015). It is important to keep in mind, however, that any mitigation option has to be cost-effective to be widely adopted by farmers.
Manure Methane Mitigation
Diet can have a significant impact on manure (feces and urine) chemistry and therefore on GHG emissions during storage and following land application. Increased fecal output of potentially fermentable organic matter (as a result of decreased digestibility of dietary nutrients or increased passage rate through the digestive tract) may increase manure methane emission. Most mitigation options for GHG emissions from stored manure, such as reducing the time of manure storage, aeration, using slatted floors, and stacking, are generally aimed at decreasing the time allowed for microbial fermentation processes to occur before manure is land-applied. These mitigation practices are effective, but their economic feasibility is uncertain. Semi-permeable covers are valuable for reducing methane and odor emissions at storage. Impermeable membranes, such as oil layers and sealed plastic covers, are effective in reducing gaseous emissions but are not very practical. Combusting methane that accumulates under impermeable covers to produce electricity or heat is also a mitigation option that will decrease overall GHG emissions from manure storage. Housing, type of manure collection and storage system, and separation of solids and liquid and their processing can all have a significant impact on GHG emissions from animal facilities. Acidification (in areas where soil acidity is not an issue) and cooling have also been shown to reduce methane emissions from stored manure. Anaerobic digesters are an effective mitigation strategy for methane. Management of anaerobic digesters, however, is important to prevent them from becoming net emitters of GHG. Separation of manure solids can have a significant and large impact on methane emissions (Holly et al., 2017). Manure solids are the source of methane, and their removal can drastically decrease total emissions from manure storage. Anaerobic degradation pretreatments can mitigate methane emission from subsurface-applied manure, which may otherwise be greater than that from surface-applied manure.
Rice Methane Mitigation
Generally, selection of rice cultivars, water regime, and fertilization are the most important factors that can have an impact on methane emissions from rice cultivation (Zhao, He, & Cao, 2011). The techniques that are most promising to mitigate methane emissions from rice cultivation include: alternate wetting and drying (AWD) and mid-season drainage, which increase oxygen penetration and decrease anaerobiosis; balanced application of nutrients such as fertilizer, which helps decreasing methane emissions and improves yield (i.e., decreasing emission intensity); use of faster-maturing rice varieties that require less water; and reduced tillage. Studies have shown that water-saving irrigation methods such as AWD reduce net methane emissions, produced under water-saturated conditions (Linquist et al., 2015). A one six-day mid-season drainage event, interrupting anaerobic and reduced soil conditions, can decrease post-drainage methane emissions by 64% with no negative effect on yield (Sigren, Lewis, Fisher, & Sass, 1997). Other irrigation techniques that reduce the inundated soil period also reduce methane emissions from rice paddies. These methods include the use of drill-seeding rather than water-seeding or transplanting rice (Pittelkow et al., 2013). Rice varieties may be selected for low exudation of carbon from the roots, for higher rhizosphere methane oxidation, for higher harvest yields, and adaptation to other mitigation methods (such as AWD) (Malyan et al., 2016). Recently, Su et al. (2015) showed that addition of a single transcription factor gene to rice, leading to allocation of photosynthates to the aboveground biomass versus allocation to roots, increased plant biomass and starch content and decreased methanogenesis, possibly through a reduction in root exudates. Such results are exciting and demonstrate the opportunities that modern molecular techniques offer to GHG mitigation efforts.
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