Next Article in Journal
Water Quality Prediction Based on LSTM and Attention Mechanism: A Case Study of the Burnett River, Australia
Previous Article in Journal
Life Cycle Assessment (LCA) in Earth Construction: A Systematic Literature Review Considering Five Construction Techniques
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Strategies to Mitigate Enteric Methane Emissions in Ruminants: A Review

by
Valiollah Palangi
1,*,
Akbar Taghizadeh
2,
Soheila Abachi
3 and
Maximilian Lackner
4,5,*
1
Department of Animal Science, Agricultural Faculty, Ataturk University, Erzurum 25240, Turkey
2
Department of Animal Science, Faculty of Agriculture, University of Tabriz, Tabriz 5166616471, Iran
3
Institute of Nutrition and Functional Foods (INAF), Université Laval, Quebec, QC G1V 0A6, Canada
4
Department of Industrial Engineering, University of Applied Sciences Technikum Wien, Hoechstaedtplatz 6, 1200 Vienna, Austria
5
Circe Biotechnologie GmbH, Kerpengasse 125, 1210 Vienna, Austria
*
Authors to whom correspondence should be addressed.
Sustainability 2022, 14(20), 13229; https://doi.org/10.3390/su142013229
Submission received: 26 August 2022 / Revised: 25 September 2022 / Accepted: 12 October 2022 / Published: 14 October 2022

Abstract

:
Methane is the main greenhouse gas (GHG) emitted by ruminants. Mitigation strategies are required to alleviate this negative environmental impact while maintaining productivity and ruminants’ health. To date, numerous methane mitigation strategies have been investigated, reported and suggested by scientists to the livestock industry. In this review, the authors will focus on the commonly practiced and available techniques expanding the knowledge of the reader on the advances of methane mitigation strategies with a focus on the recent literature. Furthermore, the authors will attempt to discuss the drawbacks of the strategies in terms of animal health and performance reduction as well as the concept of feed and energy loss, adding an economic perspective to methane emission mitigation which is in the farmers’ direct interest. As a whole, many factors are effective in reducing undesired methane production, but this is definitely a complex challenge. Conclusively, further research is required to offer effective and efficient methane production mitigation solutions in ruminants worldwide, thus positively contributing to climate change.

1. Introduction

The agricultural sector is a major emitter of greenhouse gasses, and animal husbandry is one of the largest sources therein, particularly concerning ruminant breeding carried out on feedlots with feed concentrates and/or on pastures where animals graze for forage. Ruminants obtain their nutrients from plant-based, difficult-to-digest lignocellulosic food by fermenting it in a specialized stomach (the multi-chambered “rumen”) before digestion. The process is termed “enteric fermentation”, a digestive process in which carbohydrates are broken down by microorganisms into small molecules. Ruminal anaerobic fermentation of nutrients is a common pathway to reduce carbon dioxide and hydrogen ions (H+) to methane [1]. Approximately 200 species of both domesticated and wild ruminants, including cattle (dairy and beef), goats and sheep, exist in the world. Methane (CH4), together with nitrous oxide (N2O) and carbon dioxide (CO2), constitute the major greenhouse gases (GHG) produced by ruminants. Yet, there is growing concern over their negative effect on global climate change, see Figure 1.
Cattle breeding and production, due to their size and number (~1.5 billion cattle globally), is the main source of methane emission compared to other ruminants such as sheep. Global demand for livestock products is expected to double by 2050, mainly due to improvements in the worldwide standard of living [2]. According to Rojas-Downing et al., animal husbandry not only contributes to climate change but is also affected by it. Climate change threatens livestock production because of the “impact on quality of feed crop and forage, water availability, animal and milk production, livestock diseases, animal reproduction, and biodiversity” [2]. Prasad et al. [3] reviewed the ways in which climate change impacts livestock production, concluding that increasing temperatures, drought, flooding and variation in rainfall trends all negatively affect the livestock industry.
Apart from causing climate change, at least in part, methane emission from ruminants is also a direct cost factor for farmers due to the energy loss from feed. According to the FAO, up to 12% of the energy contained in feed is usually lost to CH4 production [4]. Under anaerobic conditions, the microbial population in the animals’ digestive system produces volatile fatty acids (VFA) through the fermentation of nutrients. Major VFAs include acetate, propionate and butyrate, which can both act as sources of energy for the animal and as sources of CH4 and CO2 [5]. Fermentation is an oxidative process, during which reduced cofactors (NADH, NADPH and FADH) are re-oxidized (NAD+, NADP+ and FAD+) through dehydrogenation reactions releasing hydrogen that is then used by methanogenic archaea, a microbial group distinct from eubacteria, to reduce CO2 into CH4 [6]. The microbial fermentation of fodder in the rumen yields different end products and, therefore, is different in terms of hydrogen production efficiency. From the production of acetate and butyrate, pure hydrogen is released, while the formation of propionate creates a competitive pathway for H+ use in the rumen. Thus, metabolic pathways in hydrogen production and utilization are among the main factors that need further attention in the development of ruminant methane mitigation strategies, as well as addressing the methanogenic community composition.
The properties of the ration have a direct effect on the production level and rumen metabolism of the animal. Enteric methane emission is greatly affected by diet composition, of which fiber is the most important. There is a positive correlation between enteric methane emission and fiber content, while this correlation is negative with dietary lipid content [7]. Gaviria-Uribe et al. [8] reported that dry matter intake (DMI) has a high correlation with CH4 emissions. Moreover, treatments with higher nutritional quality and higher DMI resulted in lower CH4 emission and, thus, lower energy loss. In the following sections, the authors will discuss the main dietary manipulation strategies: forage-to-concentrate ratio and dietary additives with methane production reducing or inhibiting properties.
Over the past few years, review papers and meta-analyses have been published on how different mitigation strategies influence CH4 production in ruminants. However, given the importance of the topic and the fast pace of growing knowledge in the area, in this article, the authors attempt to focus on bringing together and discussing the most recent findings as well as new methane mitigation strategies in ruminants.

2. Background and Significance

Anthropogenic greenhouse gas (GHG) emissions [9] have detrimental effects on the climate [10]. Natural methane emissions from wetland ecosystems constitute a relevant part of the global CH4 amount. There are many factors which influence unwanted CH4 production by ruminants: level of feed intake, type and quality of feed, energy consumption, animal size, growth rate, level of production and environmental temperature [11]. The methane emissions in dairy cows range from 151 to 497 g per day [11]. Lactating cows produce more CH4 (354 g per day) [11]. In a study by Harper et al. [12], pasture-grazing cattle produced 0.23 kg CH4 per animal per day, which corresponded to the conversion of 7.7 to 8.4% of gross energy into CH4. The same cattle fed with a highly digestible, high-grain diet produced 0.07 kg CH4 per animal per day, corresponding to a conversion of only 1.9 to 2.2% of the feed energy to CH4 [12]; hence, four times more CH4 was produced when low-grade feed was used.
Methane emissions from ruminants can be measured using either respiration chambers (RC) or sulphur hexafluoride tracer (SF6) techniques [13]. Another method is laser spectroscopy, carried out by line-averaging sensors [14]. Wu et al. reported measurement techniques in cattle buildings [15]. To determine ruminants’ CH4 emissions, in vitro or in vivo trials can be carried out. Rossi et al. described an in vitro volatile fatty acids (VFA) production-based method for the assessment of CH4 emission using high energy, high protein and forage feedstuffs (fermented in vitro using rumen fluid from dairy cows as inoculum) [16].
The atmosphere contains approximately 1.9 ppm of methane, whereas the respiration air of cattle is roughly 1000 ppm [17]. The National Oceanic and Atmospheric Administration’s (NOAA) recent findings [18] surface that the annual increase in methane level in the atmosphere in 2021 was 17 parts per billion (ppb). This rate constitutes the largest annual increase measured since the beginning of systematic recordings. Atmospheric methane levels averaged 1.898 ppm last year, which is approximately 162% greater than pre-industrial levels. Figure 2 illustrates the increasing trend in atmospheric CH4 levels.
As seen in Figure 2, over the past three centuries, the atmospheric methane burden has grown 2.5-fold, reaching levels unprecedented in at least 650,000 years [19]. Marielle Saunois et al., in the “Global Methane Budget 2000–2017” seminar [20], stated that “domestic ruminants such as cattle, buffalo, sheep, goats, and camels emit methane as a by-product of the anaerobic microbial activity in their digestive systems. The very stable temperatures (about 39 °C) and pH (6.5–6.8) values within the rumen of domestic ruminants, along with a constant plant matter flow from grazing (cattle graze many hours per day), allow methanogenic archaea residing within the rumen to produce methane. Methane is released from the rumen mainly through the mouth of multi-stomached ruminants (eructation, 87% of emissions) or absorbed into the blood system.

3. Strategies to Reduce CH4 Emissions

There are several routes to reduce CH4 emissions from livestock operations. Ricci et al. [21] carried out a systematic investigation of methane emissions from beef and dairy, where they attempted to quantify the effects of physiological stage and diet characteristics, lactating or nonlactating status, local conditions and available fodder. Nutrition plays a critical role [22] in CH4 emissions. Difford et al. [23] found that the host genome and rumen microbiome play a critical role in CH4 emissions and that these two factors were independent. The authors suggested addressing these two points separately. Zang et al. [24] summarized mitigation and adaptation strategies for developed versus developing countries (Figure 3).
Wallace et al. [25] stated that the rumen microbial metagenome of cattle is associated with high methane production. Microorganisms in the rumen of dairy cows are the cause of methane production in these animals [26]. There are many strategies devised by scholars to reduce enteric methane emissions. Although there is a common goal for breeders and those seeking to protect the climate, it can be difficult to convince animal breeders to deploy them [27]. Better feed utilization efficiency in ruminants not only accelerates animal production and lowers the farmers’ costs but also reduces the environmental impact [28]. Both the farmer and the environment would benefit substantially from so-far-elusive measures to reduce enteric methane production [19]. Hence, strategies on how to roll out the best methane reduction methods so that farmers can be reached and motivated are essential.

3.1. Genetic Selection

There is increasing evidence that feed conversion efficiency (FCE), as well as methane emission, are heritable traits of dairy cows [29], and for determination of these traits, the composition of the rumen microbiome shall be considered. Correspondingly, to exploit the genetic factor, those with lower CH4 emissions shall be selected [30].

3.2. Ratio of Forage to Concentrate (F:C)

Of all the enteric methane emission mitigation strategies suggested and practiced, forage-to-concentrate ratio (F:C) management, introduced in many studies, may be the most common one. Concentrates (supplements) are often administered to cattle and other ruminants in grazing systems when the availability and/or quality of pasture is limiting animal performance [31]. Supplementary feeding covers the animals’ needs for protein, energy, roughage and minerals. Table 1 shows a typical example of supplements (concentrates) for the tropical region in Northern Australia.
High-forage diet-fed dairy cows produced 35% more methane in comparison to the period when they were fed a high-concentrate diet [32]. Among carbohydrates, cellulose fermentation produces the highest amount of methane [6]. High-concentrate diets produce less methane than high-forage diets [33]. Thakur et al. [34] concluded that increasing the concentrate ratio reduced methane emissions and improved the growth performance of crossbred goat kids. As previously discussed by Barbosa et al. [35], methane emission was reduced linearly by increasing the dietary concentrate ratio. Accordingly, in the study of Alqaisi et al. [36], high-concentrate diet-fed rams exhibited a significant reduction in methane production. According to the study of Li et al. [37], bacterial community structure and methane production in the rumen changed via changing F:C, and lowering the F:C ratio resulted in a decrease in methane production. Forage quality [38], increased levels of concentrates [38], feeding high-forage diets as pelleted form and increased propionic acid production resulted in lower methane formation. Molano and Clark [39] noted that methane emissions per unit of DMI were not associated with diet quality. Chagunda et al. [40] demonstrated that high-quality silage and a high proportion of concentrate in the ration resulted in low methane emissions. Silage is ruminant fodder that is prepared from foliage crops preserved by lactic acid bacteria fermentation.
According to Thompson and Rowntree [41], forage type and forage maturity stage affect methane emissions. Lima et al. [42] indicated that lower hemicellulose content leads to increased methane production. Nascimento et al. [43] observed that higher concentration improved weight gain and the meat quality of lambs. Huhtanen and Huuskonen [44] reported that increasing concentrate levels led to decreased crude protein (CP) digestibility and nitrogen excretion (N) flow from the rumen. There is a negative correlation between concentrate amounts and methane production [45]; therefore, increasing concentrate level in the ration leads to decreasing acetate and increasing propionate. Propionate acts as a hydrogen sink and reduces hydrogen availability to methane production. The main drawback of the strategy is lower milk quality as well as metabolic problems, thus limiting its application in the livestock industry. However, diets containing high amounts of concentrate, due to the high fermentation rate of fermentable carbohydrates, increase the production of volatile fatty acids in the rumen. A sudden increase and accumulation of volatile fatty acids leads to a decrease in ruminal pH and can reduce the ability to absorb volatile fatty acids by damaging ruminal tissue. Therefore, maintaining a balance between the ratio of forage to concentrate is essential to sustain the quantity and quality of production while maintaining animal health. Concentrate is more costly than grazing grass, so a balance needs to be found. Singh and Sharma [46] recorded higher body weight gain in concentrate-fed goat kids. Accordingly, animals were fed concentrate at the early growth stage, followed by green fodder after weaning. Fodder quality and type are decisive factors.

3.3. Addition of Dietary Oils/Lipids to Ration

Using fat as a source of energy in the ration would lead to significant changes in the efficiency of microbial flora and energy usage in the rumen, followed by a reduction in methane production [47,48]. McGinn et al. showed that the utilization of sunflower oil and possibly some yeast products could decrease gross energy (GE) loss as methane from cattle on a high forage diet but would impair fiber digestibility [48]. Vargas et al. [49] concluded that the addition of vegetable oils reduced methane production and increased the formation of propionic acid. The inclusion of lipids in the ruminants’ ration reduces enteric methane emission by inhibiting the methanogen’s growth and decreasing the ruminal ration fermentation capacity [50]. Consequently, this reduces microorganisms’ access to the diet and/or increases the ruminal passage rate. The inhibitory effects of lipids on methane emissions are not transitory but persist over time [51]. Judy et al. [52] showed that the addition of corn oil and calcium sulfate to diets reduced methane production and improved net energy balance in lactating dairy cows. In agreement, Embaby et al. [53] reported that supplementation of hemp and blueberry oils moderately reduced ruminal in vitro methane formation without compromising rumen fermentation and digestibility. Lima et al. [54] similarly reported that the inclusion of soybean oil significantly reduced methane production. Karlsson et al. [55] observed that supplementation of diets with glycerol could increase methane production. Winders et al. [56] reported that the inclusion of corn oil leads to a considerable methane production reduction. It can be concluded that oils and lipids might effectively be used, alone and or in combination with other strategies, for enteric methane mitigation. Five possibilities have been identified for reducing methane production by adding fat to the diet: decreased fiber digestion (especially long-chain fatty acids), reduced feed intake (total dietary fat exceeding 6–7%), decreased methanogens, decreased rumen protozoan populations and increased biohydrogenation process [57]. Pirondini et al. investigated the effect of fish oil supplements on methane emission and reported its potential mitigation effects [58].

3.4. Tannin-Rich Feedstuffs

Tannins (tannic acid derivatives) are a chemically diverse group of water-soluble phenolics which bind to proteins and form soluble or insoluble complexes found on the skin, leaves and roots of most plants [59]. Tannins are known to have direct and indirect effects on rumen microbes, decreasing ruminal protein degradability and methanogenesis as well as biohydrogenation of unsaturated fatty acids [60]. Nevertheless, these effects may partially be due to the antimicrobial properties of the tannins reducing fiber digestion, thus leading to incomplete digestion of the diet by the ruminal microbial population [61]. It is noteworthy that hydrolyzable tannins express toxic effects in ruminants rather than acting as a digestion inhibitor [62]. Molina-Botero et al. [63] observed that the total ruminal microbial population, methanogenic archaea and total protozoa were not affected by the increasing levels of condensed tannins in rations. Petlum et al. [64] found that the efficacy of condensed tannins as ruminal methane production inhibitors is greatly influenced by their molecular weights.
The potency of tannins has also been shown to be dose dependent. Lima et al. [54] reported that methane production was not affected by tannins at a concentration of 30 g/kg DM (dry matter). The findings of Adejoro et al. [65] show the in vitro potency of lipid-encapsulated Acacia extracted tannins in reducing enteric methane production. In the study of Deuri et al. [66], Bauhinia leaves supplementation considerably reduced the production of enteric methane. In another study, the inclusion of sainfoin (Onobrychis viciifolia Scop) and/or hazelnut (Corylus avellana L.) in ruminant rations reduced rumen fermentability, methane production and protein degradability [67].
The effects of condensed tannins on rumen fermentation depend on their sources and concentrations [68]. However, studies have proposed that the chemical structure and molecular weight of these metabolites have a vital role in their efficacy for the manipulation of rumen fermentation and methane mitigation [69]. Decreased ruminal protein breakdown is the most pronounced effect of tannins [70,71]. Hydrolyzable tannins and condensed tannins bind to proteins making those proteases resistant and nutritionally inaccessible to the animal. Tannins prevent the attachment of microorganisms to the cell wall of plants, and this binding is essential for degradation. In addition, the formation of complexes with proteins and carbohydrates prevents microorganisms from accessing nutrients [72]. Tannins are also chelating agents that reduce the availability of metal ions required for the metabolism of rumen microorganisms [73]. Additionally, tannins, due to their inhibitory enzyme activities, react with microbial enzymes and inhibit their activity [74].

3.5. Use of Microalgae and Macroalgae

Another inhibitor of CH4 production as a substitute for fish oil is microalgae. Similar to fish oil, microalgae are rich in the fatty acids C20:5n−3 and C22:6,n−3. Eicosapentaenoic acid (EPA; C20:5 n−3) and docosahexaenoic acid (DHA; C22:6 n−3) are the primary marine-derived omega-3 fatty acids. In vitro experiments have shown that microalgae are capable of inhibiting methanogenesis, reducing acetate concentration and increasing propionate concentration. Their inhibitory effects can be attributed to their unsaturated fatty acid content, in particular C22:6,n−3 [75]. A recent experiment by Sucu [76] reported that under in vitro conditions, using Chlorella Vulgaris, C. variabilis and/or both not only reduced acetate and increased propionate concentrations but also mitigated CH4 production. Anele et al. [77] reported a significant reduction in CH4 production under in vitro incubation by Tetracystic sp., Scenedesmus sp. and Nannochloropsis granulatab compared to Chlorella Vulgaris and Micractinium reisseri. Similar to microalgae, Dictyota bartayresii and Asparagopsis taxiformis algae reduced in vitro methane production after 72 h compared with the control group [78]. Furthermore, Vijn et al. [79] successfully used seaweed for enteric methane mitigation.
These beneficial effects of algae could be due to the existence of various secondary metabolites. The presence of bromoform (CHBr3) with known antibacterial properties, which is chemically similar to bromochloromethane (CH2BrCl), in Asparagopsis has been shown to reduce CH4 [80]. The inclusion of different levels of Asparagopsis taxiformis resulted in a linear reduction of CH4 production and CH4/DMI in sheep by up to 81.3% for CH4 and up to 62.6% for CH4/DMI compared with the control group [37]. Furthermore, findings on ruminal fermentation patterns showed an increased concentration of propionate and decreased concentration of acetate in the algae-fed group. This VFA profile change suggests that Asparagopsis can lead to the diversion of hydrogen to propionate, making hydrogen less available for methanogenesis [37]. Accordingly, the inclusion of Asparagopsis armata at 0.5 and 1% of organic matter basis led to a reduction in CH4 production (g/day) by 26.4% and 67.2%, respectively. A decrease in CH4 and milk yield was observed by 18.2% and 60.1%, respectively, compared with the control group in dairy cattle [81]. Similar to the results found in dairy cattle, Kinley et al. [82] reported that the inclusion of Asparagopsis taxiformis at 0.05, 0.1 and 0.2% (organic matter basis) in the beef cattle diet for 90 days reduced CH4/DMI by 9, 38 and 98%, respectively. In contrast, algae inclusion in ruminant animal feeds did not affect methane production [83]. Similarly, Choi et al. [84] stated that Sargassum fulvellum (macroalgae) inclusion in ruminants’ diet did not affect methane production in 24 h of incubation. It is noteworthy that the use of many algae species in ruminant nutrition is limited due to the presence of bromoform which is a carcinogenic compound [85].

3.6. Pasture Quality

The quality of the fodder depends on many factors. As stated, enteric methane emissions are directly related to the quantity and type of feed intake, and several studies have reported the positive effect of adding legumes to feed. Dini et al. [86] studied the effect of different levels of pasture quality on CH4 emissions. The CH4 emissions were 14% lower, expressed as % of gross energy intake, and 11 % lower, expressed as g CH4/kg dry matter intake, in the high-quality pasture grazing animals than the control group. Desmanthus, a tropical legume, reduced in vivo methane when used as a nutritional supplement [31]. The addition of herbs to fodder was investigated by Vázquez-Carrillo et al. [87]. The authors conducted research on the antimethanogenic effects of lemon grass (Cymbopogon citratus), chamomile (Matricaria chamomilla) and Mexican aster (Cosmos bipinnatus) on high-in-concentrate diet-fed beef cattle. Lemon grass significantly reduced methane yield (g of CH4/kg of DMI) by 33%, Mexican aster reduced methane yield by 28% and chamomile had no significant effect. Tea-extracted saponins rich in pentacyclic triterpenes (from seeds, leaves or roots) with antiprotozoal attributes had little effect on the methanogen population in sheep [88]. The authors speculate that the “addition of tea saponins in animal diets may be an effective way to inhibit methanogenesis and hence has implications not only for global environmental protection but also for efficient animal production”. Dey et al. [28] looked into the reduction of enteric methane production from buffalo (Bubalus bubalis) by garlic oil (Allium sativum) supplementation in an in vitro rumen fermentation system.

3.7. Commercial Feed Additives

Antibiotics use in livestock is banned throughout Europe due to their detrimental effects. For instance, the supplementation of ionophore antibiotics and other chemicals has been prohibited by the European Union since 2006 due to the development of microbial resistance. Correspondingly, researchers, due to the presence of such traits in animal products, are looking for alternatives to increase animal production, concomitantly lowering environmental pollution [28]. Many natural and synthetic products (e.g., probiotics, polyphenols) to date have been successfully studied for their effect on CH4 emission mitigation. For instance, per instruction of the manufacturer, a quarter teaspoon of Bovaer per day suppresses the enzyme that triggers methane production in the rumen and consistently reduces enteric methane emission by up to 90% in cows (30% in dairy cows and 90% in beef cows). In 2021, DSM received full regulatory approval to commercialize Bovaer® from the Brazilian and Chilean authorities for its application in beef, dairy, sheep and goats. In addition, in 2022, DSM received EU market approval for Bovaer® for dairy cows, following a positive EFSA opinion which confirms that the product reduces enteric methane emissions from dairy cows and is safe for the animal and the consumer. This is the first time the EU has marketed a product as a feed additive for its environmental benefits [89].

3.8. Other Approaches

Leng et al. [90] studied the effect of biochar and potassium nitrate administration on CH4 emissions. Biochar at 0.6% of diet DM and potassium nitrate at 6% of diet DM reduced methane production by 22% and 29%, respectively. Effects were additive (41% reduction) for the combination of biochar and potassium nitrate. Rani et al. [91] state that methane-utilizing bacteria are found in methane-rich environments such as natural wetlands, rice fields, livestock rumen, peats and bogs. Finn et al. [92] proposed methanotrophs from natural ecosystems as biocontrol agents for ruminant methane emissions. Methanotrophic bacteria use CH4 as the sole carbon and energy source in an aerobic process and can be used to obtain single-cell proteins (SCP) as feed and food ingredients and biopolymers [93]. Finn et al. [92] reasoned that since methanotrophs (methane-oxidizing bacteria) act as CH4 sinks in nature, they can be used to reduce CH4 levels in rumens. The authors stated that methanotrophs which are native to the rumen, have received little attention and that future work will be required to address the potential for methanotrophs to act as biocontrol agents for ruminant CH4 emissions.
Fungi might also be deployed to mitigate CH4 in natural and engineered systems. As per Jason et al. [94], fungi may indirectly influence carbon mineralization and methanogen/methanotroph communities and/or directly oxidize and dissolve gaseous CH4. Anaerobic fungi were first detected in the rumen of sheep in the late 1970s and, not long after, were observed growing in close proximity to rumen methanogens. An initial meta-analysis showed that anaerobic fungi probiotics-fed cows could reduce enteric CH4 production, yet the effects vary depending on the experimental conditions. Most of the early fungal probiotics were only used to improve milk production, not specifically to reduce CH4, yet anaerobic fungi probiotics can specifically enhance acetogenesis and mitigate CH4 emissions.
Another idea is to capture and/or destroy exhaled CH4 from the animals, see Figure 4.
The invention in Figure 4 suggests collecting emitted methane for later utilization, whereas the invention in Figure 4 targets oxidizing methane, which is exhaled by ruminants. The inventors claim to reach >50% efficiency. Additionally, in 2004, a vaccine was proposed for the same purpose [96]. The Commonwealth Scientific and Industrial Research Organisation in Perth, Western Australia, purportedly developed a vaccine against archaean microbes that produce methane in sheep rumens.

4. The Economics of CH4 Abatement from Ruminants

A recent report by DeFabrizio et al. [97] evaluated CH4 abatement costs and reported that feed additives are seen as one of the costly measures, whereas “animal health monitoring” has an equal impact in terms of CH4 potential and can even bring cost savings. As stated before, there are more than 1.5 billion cattle all over the globe, and any individual smallholder and cattle breeder of different herd sizes needs to be educated on the application of a set of measure (s) suitable for that specific industry. This task is critical and must be based on the consensus of which levers make the most sense to mitigate CH4 emissions.

5. Other Ruminants

While the focus of his review has been on cattle, there are other ruminants of importance too, such as buffalo, sheep, goats and camels [20], which are all domesticated. For instance, there are almost 40 million camels on Earth [98]. Emission rates were estimated by ref. [99]: 5 to 8 kg for sheep, 1 to 1.5 kg for pigs, 58 kg for camels, 50 kg for water buffalos, 5 kg for goats, 18 kg for horses and 15 kg for caribous per year.
Let us take Peru as an example. The share of livestock in the countries’ GHG emissions is reported to be 14.5%, of which 64% stem from enteric fermentation and manure emissions from ruminants [100]. Peru is home to 27% of the world’s llama population, 0.75 million animals, and a study using tannins in the diet of these animals found that methane production could be reduced by 30% in llamas [100].
Figure 5 summarizes the daily CH4 emissions by different mammals as a function of their body mass.
It had been suggested to use alternative animals for meat production with lower specific CH4 emissions, such as ostriches. In ref. [102], the previously reported low methane emissions from these birds were revisited, and it was concluded that data from juvenile animals, which tend to be lower, cannot be extrapolated to an adult population [101]. Still, it can be worthwhile to consider animals with superior feed conversion efficiency as primary meat producers.

6. Conclusions

Serval approaches were found to be promising in reducing enteric CH4 formation and emission; however, caution is required when assessing the findings. The effects may be transient, and further studies might be needed to confirm whether such reductions are maintained over longer feeding periods [103]. The main concern of animal nutritionists is to reduce diet energy loss while mitigating the greenhouse gasses emitted in the form of methane and CO2 without adverse effects on the animals’ health, performance and productivity, along with the quality of meat and milk. In some of the above strategies, ruminal microflora are also affected, and, most likely, ruminal fermentation is reduced, creating a challenge in animal breeding. Therefore, considering the economic situation, the relations of greenhouse gas costs with animal yields, animal feed processing and type of farm management are important. Conclusively, all the strategies mentioned above can effectively reduce methane production, yet the topic is a serious challenge requiring further research and attention. Mitigating CH4 from cattle has both long-term environmental and short-term economic benefits [48], and it should be fostered. Apart from reducing CH4 emissions from ruminant livestock, alternative approaches could also be studied, such as non-traditional protein sources. Alternative proteins can be plant-based, such as soybean or pea, or single-cell proteins (SCP), e.g., created using fungi, algae or bacteria. Lab-grown meat and insect proteins are further approaches that could be investigated to provide proteins.

Author Contributions

Conceptualization, V.P and M.L.; writing—original draft preparation, V.P., A.T., S.A. and M.L.; writing—review and editing, V.P. and M.L. All authors give their consent for the publication of identifiable details, which can include details within the text, to be published in the above Article. All authors have read and agreed to the published version of the manuscript.

Funding

Open Access Funding by the University of Applied Sciences Technikum Wien.

Institutional Review Board Statement

This study neither involved human/animal participation, experiment nor human data/tissue.

Informed Consent Statement

Not applicable.

Data Availability Statement

All data generated during the study are included in the published article (s) cited within the text and acknowledged in the reference section.

Conflicts of Interest

The authors declare that they have no conflict of interest. The authors understand that they will not benefit directly from participating in this research.

References

  1. Palangi, V.; Macit, M.; Nadaroglu, H.; Taghizadeh, A. Effects of green-synthesized CuO and ZnO nanoparticles on ruminal mitigation of methane emission to the enhancement of the cleaner environment. Biomass Convers. Biorefin. 2022, 2022, 1–9. [Google Scholar] [CrossRef]
  2. Rojas-Downing, M.M.; Nejadhashemi, A.P.; Harrigan, T.; Woznicki, S.A. Climate change and livestock: Impacts, adaptation, and mitigation. Clim. Risk Manag. 2017, 16, 145–163. [Google Scholar] [CrossRef]
  3. Prasad, J.M.; Waqa-Sakiti, H.; Viliamu Iese, L. An Analysis of Ecosystem-Based Adaptations in Pacific Island Countries. 2022. Available online: https://ir.canterbury.ac.nz/handle/10092/103409 (accessed on 25 August 2022).
  4. FAO. Enteric Methane (fao.org). 2022. Available online: https://www.fao.org/in-action/enteric-methane/background/en/ (accessed on 25 August 2022).
  5. Sharifi, M.; Taghizadeh, A.; Hosseinkhani, A.; Mohammadzadeh, H.; Palangi, V.; Macit, M.; Salem, A.Z.M.; Abachi, S. Nitrate supplementation at two forage levels in dairy cows feeding: Milk production and composition, fatty acid profiles, blood metabolites, ruminal fermentation, and hydrogen sink. Ann. Anim. Sci. 2022, 22, 711–722. [Google Scholar] [CrossRef]
  6. Palangi, V. Effects of Processing Legume Forages with Organic Acids on In Vitro Gas Production, Rumen Fermantation and Methan Production. In Animal Science; Ataturk University: Yakutiye, Turkey, 2019; p. 83. [Google Scholar]
  7. Benaouda, M.; Martin, C.; Li, X.; Kebreab, E.; Hristov, A.N.; Yu, Z.; Eugène, M. Evaluation of the performance of existing mathematical models predicting enteric methane emissions from ruminants: Animal categories and dietary mitigation strategies. Anim. Feed Sci. Technol. 2019, 255, 114207. [Google Scholar] [CrossRef]
  8. Gaviria-Uribe, X.; Bolivar, D.M.; Rosenstock, T.S.; Molina-Botero, I.C.; Chirinda, N.; Barahona, R.; Arango, J. Nutritional quality, voluntary intake and enteric methane emissions of diets based on novel Cayman grass and its associations with two Leucaena shrub legumes. Front. Vet. Sci. 2020, 7, 764. [Google Scholar] [CrossRef] [PubMed]
  9. IEA. Available online: https://www.iea.org/reports/methane-tracker-2020 (accessed on 25 August 2022).
  10. Lackner, M.; Sajjadi, B.; Chen, W. (Eds.) Handbook of Climate Change Mitigation and Adaptation. Available online: https://link.springer.com/referencework/10.1007/978-3-030-72579-2 (accessed on 25 August 2022).
  11. Broucek, J. Production of Methane Emissions from Ruminant Husbandry: A Review. J. Environ. Prot. 2014, 5, 51796. [Google Scholar] [CrossRef]
  12. Harper, L.A.; Denmead, O.T.; Freney, J.R.; Byers, F.M. Direct measurements of methane emissions from grazing and feedlot cattle. J. Anim. Sci. 1999, 77, 1392–1401. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  13. Hammond, K.; Humphries, D.; Crompton, L.; Green, C.; Reynolds, C. Methane emissions from cattle: Estimates from short-term measurements using a Green Feed system compared with measurements obtained using respiration chambers or sulphur hexafluoride tracer. Anim. Feed. Sci. Technol. 2015, 203, 41–52. [Google Scholar] [CrossRef]
  14. Flesch, T.K.; Basarab, J.A.; Baron, V.S.; Wilson, J.D.; Hu, N.; Tomkins, N.W.; Ohama, A.J. Methane emissions from cattle grazing under diverse conditions: An examination of field configurations appropriate for line-averaging sensors. Agric. For. Meteorol. 2018, 258, 8–17. [Google Scholar] [CrossRef]
  15. Wu, W.; Zhang, G.; Kai, P. Ammonia and methane emissions from two naturally ventilated dairy cattle buildings and the influence of climatic factors on ammonia emissions. Atmos. Environ. 2012, 61, 232–243. [Google Scholar] [CrossRef]
  16. Rossi, F.; Vecchia, P.; Masoero, F. Estimate of methane production from rumen fermentation. Nutr. Cycl. Agroecosystems 2001, 60, 89–92. [Google Scholar] [CrossRef]
  17. Madsen, J.; Bjerg, B.; Hvelplund, T.; Weisbjerg, M.; Lund, P. Methane and carbon dioxide ratio in excreted air for quantification of the methane production from ruminants. Livest. Sci. 2010, 129, 223–227. [Google Scholar] [CrossRef]
  18. NOAA (National Oceanic and Atmospheric Administration). U.S. Department of Commerce, Increase in Atmospheric Methane Set Another Record during 2021; 2022. Available online: https://www.noaa.gov/news-release/increase-in-atmospheric-methane-set-another-record-during-2021 (accessed on 25 August 2022).
  19. Keith, R. Lassey, Livestock methane emission and its perspective in the global, methane cycle. Aust. J. Exp. Agric. 2008, 48, 114–118. [Google Scholar]
  20. Saunois, M.; Stavert, A.R.; Poulter, B.; Bousquet, P.; Canadell, J.G.; Jackson, R.B.; Raymond, P.A.; Dlugokencky, E.J.; Houweling, S.; Patra, P.K.; et al. The Global Methane Budget 2000–2017. Earth Syst. Sci. Data 2020, 12, 1561–1623. [Google Scholar] [CrossRef]
  21. Ricci, P.; Rooke, J.A.; Nevison, I.; Waterhouse, A. Methane emissions from beef and dairy cattle: Quantifying the effect of physiological stage and diet characteristics. J. Anim. Sci. 2013, 91, 5379–5389. [Google Scholar] [CrossRef] [PubMed]
  22. Terry, S.A.; Romero, C.M.; Chaves, A.V.; McAllister, T.A. McAllister, T.A. McAllister, Nutritional factors affecting greenhouse gas production from ruminants: Implications for enteric and manure emissions. In Improving Rumen Function, 1st ed.; Burleigh Dodds Science Publishing: Cambridge, UK, 2020; ISBN 9781003047841. [Google Scholar]
  23. Difford, G.F.; Plichta, D.R.; Løvendahl, P.; Lassen, J.; Noel, S.J.; Højberg, O.; Wright, A.-D.G.; Zhu, Z.; Kristensen, L.; Nielsen, H.B.; et al. Host genetics and the rumen microbiome jointly associate with methane emissions in dairy cows. PLoS Genet. 2018, 14, e1007580. [Google Scholar] [CrossRef] [Green Version]
  24. Zhang, Y.-X.; Chao, Q.-C.; Zheng, Q.-H.; Huang, L. The withdrawal of the U.S. from the Paris Agreement and its impact on global climate change governance. Adv. Clim. Chang. Res. 2017, 8, 213–219. [Google Scholar] [CrossRef]
  25. Wallace, R.J.; Rooke, J.A.; McKain, N.; Duthie, C.-A.; Hyslop, J.J.; Ross, D.W.; Waterhouse, A.; Watson, M.; Roehe, R. The rumen microbial metagenome associated with high methane production in cattle. BMC Genom. 2015, 16, 839. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  26. Saborío-Montero, A.; Gutierrez-Rivas, M.; Goiri, I.; Atxaerandio, R.; García-Rodriguez, A.; López-Paredes, J.; Jiménez-Montero, J.A.; González-Recio OJimenez-Montero, O. Rumen eukaryotes are the main phenotypic risk factors for larger methane emissions in dairy cattle. Livest. Sci. 2022, 26, 105023. [Google Scholar] [CrossRef]
  27. Yucheng, C.; Cel, W. Sustainable Mitigation of Methane Emission by Natural Processes. Probl. Ekorozw. Probl. Sustain. Dev. 2015, 10, 117–121. [Google Scholar]
  28. Dey, A.; Paul, S.S.; Lailer, P.C.; Dahiya, S.S. Reducing enteric methane production from buffalo (Bubalus bubalis) by garlic oil supplementation in in vitro rumen fermentation system. SN Appl. Sci. 2021, 3, 187. [Google Scholar] [CrossRef]
  29. Løvendahl, P.; Difford, G.F.; Li, B.; Chagunda, M.G.G.; Huhtanen, P.; Lidauer, M.H.; Lassen, J.; Lund, P. Review: Selecting for improved feed efficiency and reduced methane emissions in dairy cattle. Animal 2018, 12, s336–s349. [Google Scholar] [CrossRef]
  30. Lassen, J.; Løvendahl, P. Heritability estimates for enteric methane emissions from Holstein cattle measured using noninvasive methods. J. Dairy Sci. 2016, 99, 1959–1967. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  31. Suybeng, B.; Charmley, E.; Gardiner, C.P.; Malau-Aduli, B.S.; Malau-Aduli, A.E. Methane emissions and the use of desmanthus in beef cattle production in Northern Australia. Animals 2019, 9, 542. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  32. Kurihara, M.; Shibata, M.; Nishida, T.; Purnomoadi, A.; Terada, F. Methane production and its dietary manipulation in ruminants. In Rumen Microbes and Digestive Physiology in Ruminants; Japan Scientific Societies Press: Tokyo, Japan, 1997; pp. 199–208. ISBN 4-7622-0864-7. [Google Scholar]
  33. Nampoothiri, V.M.; Mohini, M.; Malla, B.A.; Mondal, G.; Pandita, S. Animal performance, and enteric methane, manure methane and nitrous oxide emissions from Murrah buffalo calves fed diets with different forage-to-concentrate ratios. Anim. Prod. Sci. 2020, 60, 780. [Google Scholar] [CrossRef]
  34. Thakur, S.; Mohini, M.; Malik, T.A.; Howal, S.; Varun, T.K.; Madavi, A.; Yadev, R.D.; Mondal, G.; Datt, C. Performance of crossbred goat kids fed with diets varying in concentrate-to-forage ratio: Intake, nutrient utilization, enteric methane emission and body weight changes. Biol. Rhythm Res. 2019, 52, 1334–1341. [Google Scholar] [CrossRef]
  35. Barbosa, A.L.; Voltolini, T.V.; Menezes, D.R.; Nascimento, J.C.S.; De Moraes, S.A.; Rodrigues, R.T.D.S. Intake, digestibility, growth performance, and enteric methane emission of Brazilian semiarid non-descript breed goats fed diets with different forage to concentrate ratios. Trop. Anim. Health Prod. 2018, 50, 283–289. [Google Scholar] [CrossRef] [PubMed]
  36. Alqaisi, O.; Al-Jazmi, F.; Al-Abri, M.; Al Kalaldeh, M.; Al Sabahi, J.; Al-Marzooqi, W. Effect of diet quality and shearing on feed and water intake, in vitro ruminal methane production, and blood parameters of Omani sheep. Trop. Anim. Heal. Prod. 2019, 52, 1115–1124. [Google Scholar] [CrossRef]
  37. Li, R.; Teng, Z.; Lang, C.; Zhou, H.; Zhong, W.; Ban, Z.; Yan, X.; Yang, H.; Farouk, M.H.; Lou, Y. Effect of different forage-to-concentrate ratios on ruminal bacterial structure and real-time methane production in sheep. PLoS ONE 2019, 14, e0214777. [Google Scholar] [CrossRef]
  38. Van Gastelen, S.; Dijkstra, J.; Bannink, A. Are dietary strategies to mitigate enteric methane emission equally effective across dairy cattle, beef cattle, and sheep? J. Dairy Sci. 2019, 102, 6109–6130. [Google Scholar] [CrossRef] [Green Version]
  39. Molano, G.; Clark, H. The effect of level of intake and forage quality on methane production by sheep. Aust. J. Exp. Agric. 2008, 48, 219–222. [Google Scholar] [CrossRef]
  40. Chagunda, M.G.G.; Flockhart, J.F.; Roberts, D.J. The effect of forage quality on predicted enteric methane production from dairy cows. Int. J. Agric. Sustain. 2010, 8, 250–256. [Google Scholar] [CrossRef]
  41. Thompson, L.; Rowntree, J. Invited Review: Methane sources, quantification, and mitigation in grazing beef systems. Appl. Anim. Sci. 2020, 36, 556–573. [Google Scholar] [CrossRef]
  42. Lima, D.M.; Filho, A.L.A.; Lima, P.D.M.T.; Sakita, G.Z.; e Silva, T.P.D.; McManus, C.; Abdalla, A.L.; Louvandini, H. Morphological characteristics, nutritive quality, and methane production of tropical grasses in Brazil. Pesqui. Agropecuária Bras. 2018, 53, 323–331. [Google Scholar] [CrossRef] [Green Version]
  43. Nascimento, C.D.O.; Santos, S.; Pina, D.D.S.; Tosto, M.; Pinto, L.; Eiras, D.; de Assis, D.; Perazzo, A.; de Araújo, M.; Azevêdo, J.; et al. Effect of roughage-to-concentrate ratios combined with different preserved tropical forages on the productive performance of feedlot lambs. Small Rumin. Res. 2019, 182, 15–21. [Google Scholar] [CrossRef]
  44. Huhtanen, P.; Huuskonen, A. Modelling effects of carcass weight, dietary concentrate and protein levels on the CH4 emission, N and P excretion of dairy bulls. Livest. Sci. 2020, 232, 103896. [Google Scholar] [CrossRef]
  45. Holter, J.; Young, A. Methane Prediction in Dry and Lactating Holstein Cows. J. Dairy Sci. 1992, 75, 2165–2175. [Google Scholar] [CrossRef]
  46. Singh, T.; Sharma, M. Feeding of Concentrate and Green Fodder at an Early Age and its Effects on Growth Rate in Goat Kids. J. Krishi Vigyan 2019, 8, 133. [Google Scholar] [CrossRef]
  47. Beauchemin, K.A.; McGinn, S.M. Methane emissions from beef cattle: Effects of fumaric acid, essential oil, and canola oil1. J. Anim. Sci. 2006, 84, 1489–1496. [Google Scholar] [CrossRef]
  48. McGinn, S.M.; Beauchemin, K.A.; Coates, T.; Colombatto, D. Methane emissions from beef cattle: Effects of monensin, sunflower oil, enzymes, yeast, and fumaric acid1. J. Anim. Sci. 2004, 82, 3346–3356. [Google Scholar] [CrossRef] [PubMed]
  49. Vargas, J.E.; Andrés, S.; López-Ferreras, L.; Snelling, T.J.; Yáñez-Ruíz, D.R.; García-Estrada, C.; López, S. Dietary supplemental plant oils reduce methanogenesis from anaerobic microbial fermentation in the rumen. Sci. Rep. 2020, 10, 1613. [Google Scholar] [CrossRef] [Green Version]
  50. Villar, M.; Hegarty, R.; Nolan, J.; Godwin, I.; McPhee, M. The effect of dietary nitrate and canola oil alone or in combination on fermentation, digesta kinetics and methane emissions from cattle. Anim. Feed Sci. Technol. 2020, 259, 114294. [Google Scholar] [CrossRef]
  51. Guyader, J.; Tavendale, M.; Martin, C.; Muetzel, S. Dose-response effect of nitrate on hydrogen distribution between rumen fermentation end products: An in vitro approach. Anim. Prod. Sci. 2016, 56, 224–230. [Google Scholar] [CrossRef]
  52. Judy, J.V.; Bachman, G.C.; Brown-Brandl, T.M.; Fernando, S.C.; Hales, K.E.; Miller, P.S.; Stowell, R.R.; Kononoff, P.J. Reducing methane production with corn oil and calcium sulfate: Responses on whole-animal energy and nitrogen balance in dairy cattle. J. Dairy Sci. 2019, 102, 2054–2067. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  53. Embaby, M.G.; Southern Illinois University; Günal, M.; AbuGhazaleh, A.; Isparta University of Applied Sciences. Effect of Unconventional Oils on in Vitro Rumen Methane Production and Fermentation. Int. J. Agric. Nat. Resour. 2019, 46, 276–285. [Google Scholar] [CrossRef]
  54. Lima, P.R.; Apdini, T.; Freire, A.S.; Santana, A.S.; Moura, L.M.L.; Nascimento, J.C.S.; Rodrigues, R.T.S.; Dijkstra, J.; Garcez Neto, A.F.; Queiroz, M.A.Á.; et al. Dietary supplementation with tannin and soybean oil on intake, digestibility, feeding behavior, ruminal protozoa and methane emission in sheep. Anim. Feed Sci. Tech. 2019, 249, 10–17. [Google Scholar] [CrossRef]
  55. Karlsson, J.; Ramin, M.; Kass, M.; Lindberg, M.; Holtenius, K. Effects of replacing wheat starch with glycerol on methane emissions, milk production, and feed efficiency in dairy cows fed grass silage-based diets. J. Dairy Sci. 2019, 102, 7927–7935. [Google Scholar] [CrossRef] [PubMed]
  56. Winders, T.M.; Boyd, B.M.; Hilscher, H.F.; Fernando, S.C.; Stowell, R.R.; Erickson, G.E. Corn Oil Supplementation on Performance and Methane Production in Finishing Steers. Neb. Beef Cattle Rep. 2019, 62, 1–5. [Google Scholar]
  57. Machmüller, A. Medium-chain fatty acids and their potential to reduce methanogenesis in domestic ruminants. Agric. Ecosyst. Environ. 2006, 112, 107–114. [Google Scholar] [CrossRef]
  58. Pirondini, M.; Colombini, S.; Mele, M.; Malagutti, L.; Rapetti, L.; Galassi, G.; Crovetto, G.M. Effect of dietary starch concentration and fish oil supplementation on milk yield and composition, diet digestibility, and methane emissions in lactating dairy cows. J. Dairy Sci. 2015, 98, 357–372. [Google Scholar] [CrossRef] [Green Version]
  59. Hagerman, A.E.; Robbins, C.T.; Weerasuriya, Y.; Wilson, T.C.; McArthur, C. Tannin Chemistry in Relation to Digestion. Rangel. Ecol. Manag. 1992, 45, 57. [Google Scholar] [CrossRef]
  60. Denninger, T.; Schwarm, A.; Birkinshaw, A.; Terranova, M.; Dohme-Meier, F.; Münger, A.; Eggerschwiler, L.; Bapst, B.; Wegmann, S.; Clauss, M.; et al. Immediate effect of Acacia mearnsii tannins on methane emissions and milk fatty acid profiles of dairy cows. Anim. Feed Sci. Technol. 2020, 261, 114388. [Google Scholar] [CrossRef]
  61. Min, B.R.; Solaiman, S.; Waldrip, H.M.; Parker, D.; Todd, R.W.; Brauer, D. Dietary mitigation of enteric methane emissions from ruminants: A review of plant tannin mitigation options. Anim. Nutr. 2020, 6, 231–246. [Google Scholar] [CrossRef] [PubMed]
  62. Mehansho, H.; Butler, L.G.; Carlson, D.M. Dietary tannins and salivary proline-rich proteins: Interactions, induction, and defense mechanisms. Annu. Rev. Nutr. 1987, 7, 423–440. [Google Scholar] [CrossRef]
  63. Molina-Botero, I.C.; Arroyave-Jaramillo, J.; Valencia-Salazar, S.; Barahona-Rosales, R.; Aguilar-Pérez, C.F.; Burgos, A.A.; Ku-Vera, J.C. Effects of tannins and saponins contained in foliage of Gliricidia sepium and pods of Enterolobium cyclocarpum on fermentation, methane emissions and rumen microbial population in crossbred heifers. Anim. Feed. Sci. Technol. 2019, 251, 1–11. [Google Scholar] [CrossRef]
  64. Petlum, A.; Paengkoum, P.; Liang, J.B.; Vasupen, K. Molecular weight of condensed tannins of some tropical feed-leaves and their effect on in vitro gas and methane production. Anim. Prod. Sci. 2019, 59, 2154. [Google Scholar] [CrossRef]
  65. Adejoro, F.A.; Hassen, A.; Akanmu, A.M. Effect of Lipid-Encapsulated Acacia Tannin Extract on Feed Intake, Nutrient Digestibility and Methane Emission in Sheep. Animals 2019, 9, 863. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  66. Deuri, P.; Sood, N.; Wadhwa, M.; Bakshi, M.P.S.; Salem, A.Z.M. Screening of tree leaves for bioactive components and their impact on in vitro fermentability and methane production from total mixed ration. Agrofor. Syst. 2020, 94, 1455–1468. [Google Scholar] [CrossRef]
  67. Niderkorn, V.; Barbier, E.; Macheboeuf, D.; Torrent, A.; Mueller-Harvey, I.; Hoste, H. In vitro rumen fermentation of diets with different types of condensed tannins derived from sainfoin (Onobrychis viciifolia Scop.) pellets and hazelnut (Corylus avellana L.) pericarps. Anim. Feed Sci. Technol. 2020, 259, 114357. [Google Scholar] [CrossRef]
  68. Hagerman, A.E.; Butler, L.G. Tannins and lignins. In Herbivores: Their Interactions with Secondary Plant Metabolites; Academic Press: New York, NY, USA, 1991; Volume 1, pp. 355–388. [Google Scholar]
  69. Huang, X.; Liang, J.; Tan, H.; Yahya, R.; Khamseekhiew, B.; Ho, Y. Molecular weight and protein binding affinity of Leucaena condensed tannins and their effects on in vitro fermentation parameters. Anim. Feed Sci. Technol. 2010, 159, 81–87. [Google Scholar] [CrossRef]
  70. Sinz, S.; Marquardt, S.; Soliva, C.R.; Braun, U.; Liesegang, A.; Kreuzer, M. Phenolic plant extracts are additive in their effects against in vitro ruminal methane and ammonia formation. Asian-Australas. J. Anim. Sci. 2019, 32, 966–976. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  71. Kholif, A.E.; Olafadehan, O.A. Essential oils and phytogenic feed additives in ruminant diet: Chemistry, ruminal microbiota and fermentation, feed utilization and productive performance. Phytochem. Rev. 2021, 20, 1087–1108. [Google Scholar] [CrossRef]
  72. Mueller-Harvey, I.; McAllan, A.B. Tannins: Their biochemistry and nutritional properties. Adv. Plant Cell Biochem. Biotechnol. 1992, 1, 151–217. [Google Scholar]
  73. Scalbert, A. Antimicrobial properties of tannins. Phytochemistry 1991, 30, 3875–3883. [Google Scholar] [CrossRef]
  74. McSweeney, C.S.; Palmer, B.; McNeill, D.M.; Krause, D.O. Microbial interactions with tannins: Nutritional consequences for ruminants. Anim. Feed. Sci. Technol. 2001, 91, 83–93. [Google Scholar] [CrossRef]
  75. Fievez, V.; Boeckaert, C.; Vlaeminck, B.; Mestdagh, J.; Demeyer, D. In vitro examination of DHA-edible micro-algae: 2. Effect on rumen methane production and apparent degradability of hay. Anim. Feed Sci. Technol. 2007, 136, 80–95. [Google Scholar] [CrossRef]
  76. Sucu, E. Effects of Microalgae Species on In Vitro Rumen Fermentation Pattern and Methane Production. Ann. Anim. Sci. 2020, 20, 207–218. [Google Scholar] [CrossRef] [Green Version]
  77. Anele, U.; Yang, W.; McGinn, P.; Tibbetts, S.; McAllister, T. Ruminal in vitro gas production, dry matter digestibility, methane abatement potential, and fatty acid biohydrogenation of six species of microalgae. Can. J. Anim. Sci. 2016, 96, 354–363. [Google Scholar] [CrossRef] [Green Version]
  78. Machado, L.; Magnusson, M.; Paul, N.A.; de Nys, R.; Tomkins, N. Effects of Marine and Freshwater Macroalgae on In Vitro Total Gas and Methane Production. PLoS ONE 2014, 9, e85289. [Google Scholar] [CrossRef] [Green Version]
  79. Vijn, S.; Compart, D.P.; Dutta, N.; Foukis, A.; Hess, M.; Hristov, A.N.; Kalscheur, K.F.; Kebreab, E.; Nuzhdin, S.V.; Price, N.N.; et al. Key Considerations for the Use of Seaweed to Reduce Enteric Methane Emissions From Cattle. Front. Veter.-Sci. 2020, 7, 1135. [Google Scholar] [CrossRef]
  80. Kinley, R.D.; De Nys, R.; Vucko, M.J.; Machado, L.; Tomkins, N.W. The red macroalgae Asparagopsis taxiformis is a potent natural antimethanogenic that reduces methane production during in vitro fermentation with rumen fluid. Anim. Prod. Sci. 2016, 56, 282–289. [Google Scholar] [CrossRef]
  81. Roque, B.M.; Brooke, C.G.; Ladau, J.; Polley, T.; Marsh, L.J.; Najafi, N.; Pandey, P.; Singh, L.; Kinley, R.; Salwen, J.K.; et al. Effect of the macroalgae Asparagopsis taxiformis on methane production and rumen microbiome assemblage. Anim. Microbiome 2019, 1, 3. [Google Scholar] [CrossRef] [Green Version]
  82. Kinley, R.D.; Martinez-Fernandez, G.; Matthews, M.K.; de Nys, R.; Magnusson, M.; Tomkins, N.W. Mitigating the carbon footprint and improving productivity of ruminant livestock agriculture using a red seaweed. J. Clean. Prod. 2020, 259, 120836. [Google Scholar] [CrossRef]
  83. Maia, M.R.; Fonseca, A.J.; Cortez, P.P.; Cabrita, A.R. In vitro evaluation of macroalgae as unconventional ingredients in ruminant animal feeds. Algal Res. 2019, 40, 101481. [Google Scholar] [CrossRef]
  84. Choi, Y.Y.; Lee, S.J.; Kim, H.S.; Eom, J.S.; Kim, D.H.; Lee, S.S. The potential nutritive value of Sargassum fulvellum as a feed ingredient for ruminants. Algal Res. 2020, 45. [Google Scholar] [CrossRef]
  85. Magnusson, M.; Vucko, M.J.; Neoh, T.L.; de Nys, R. Using oil immersion to deliver a naturally-derived, stable bromoform product from the red seaweed Asparagopsis taxiformis. Algal Res. 2020, 51, 102065. [Google Scholar] [CrossRef]
  86. Dini, Y.; Gere, J.I.; Cajarville, C.; Ciganda, V.S. Using highly nutritious pastures to mitigate enteric methane emissions from cattle grazing systems in South America. Anim. Prod. Sci. 2017, 58, 2329. [Google Scholar] [CrossRef]
  87. Vázquez-Carrillo, M.F.; Montelongo-Pérez, H.D.; González-Ronquillo, M.; Castillo-Gallegos, E.; Castelán-Ortega, O.A. Effects of Three Herbs on Methane Emissions from Beef Cattle. Animals 2020, 10, 1671. [Google Scholar] [CrossRef]
  88. Wang, J.-K.; Ye, J.-A.; Liu, J.-X. Effects of tea saponins on rumen microbiota, rumen fermentation, methane production and growth performance—A review. Trop. Anim. Heal. Prod. 2011, 44, 697–706. [Google Scholar] [CrossRef]
  89. DSM. 2022. Available online: https://www.dsm.com/corporate/sustainability/our-purpose/minimizing-methane-from-cattle.html (accessed on 22 August 2022).
  90. Leng, R.A.; Preston, T.R.; Inthapanya, S. Biochar reduces enteric methane and improves growth and feed conversion in local “Yellow” cattle fed cassava root chips and fresh cassava foliage. Livest. Res. Rural. Dev. 2012, 24, 11. [Google Scholar]
  91. Rani, V.; Prasanna, R.; Kaushik, R. Prospecting the significance of methane-utilizing bacteria in agriculture. World J. Microbiol. Biotechnol. 2022, 38, 176. [Google Scholar] [CrossRef] [PubMed]
  92. Finn, D.; Ouwerkerk, D.; Klieve, A. Methanotrophs from Natural Ecosystems as Biocontrol Agents for Ruminant Methane Emissions; Meat & Livestock Australia Limited: North Sydney, Australia, 2012. [Google Scholar]
  93. Lackner, M.; Drew, D.; Bychkova, V.; Mustakhimov, I. Value-Added Products from Natural Gas Using Fermentation Processes: Products from Natural Gas Using Fermentation Processes, Part 2. In Natural Gas—New Perspectives and Future Developments; Ravanchi, M.T., Ed.; Intechopen: London, UK, 2022. [Google Scholar] [CrossRef]
  94. Oliver, J.P.; Schilling, J.S. Harnessing fungi to mitigate CH4 in natural and engineered systems. Appl. Microbiol. Biotechnol. 2018, 102, 7365–7375. [Google Scholar] [CrossRef] [PubMed]
  95. ZELP. ZELP—Reduce Methane Emissions while Improving Animal Welfare. 2022. Available online: https://www.zelp.co/ (accessed on 25 August 2022).
  96. Rachel Nowak. 25 September 2004. Available online: https://www.newscientist.com/article/dn6431-burp-vaccine-cuts-greenhouse-gas-emissions/ (accessed on 25 August 2022).
  97. DeFabrizio, S.; Glazener, W.; Hart, C.; Henderson, K.; Kar, J.; Katz, J.; Pratt, M.P.; Rogers, M.; Ulanov, A.; Tryggestad, C. Curbing Methane Emissions: How Five Industries Can Counter a Major Climate Threat, 23 September 2021 Report. Available online: https://www.mckinsey.com/business-functions/sustainability/our-insights/curbing-methane-emissions-how-five-industries-can-counter-a-major-climate-threat (accessed on 25 August 2022).
  98. FAOSTAT. Statistical Databases of the Food and Agriculture Organization of the United Nations. 2020. Available online: https://www.fao.org/faostat/en/#search/camel (accessed on 25 August 2022).
  99. Lerner, J.; Matthews, E.; Fung, I. Methane emission from animals: A Global High-Resolution Data Base. Glob. Biogeochem. Cycles 1988, 2, 139–156. [Google Scholar] [CrossRef]
  100. Febres, F.E.F.; Terrazas, L.A.; Vasquez, J.; Muñoz, J.E.M.; Howard, F.S.M.; Mariazza, E.F. Effects of chestnut bark (Castanea spp.) tannin extracts on selectivity, dry matter intake, weight gain, and enteric methane emission from llamas (Lama glama) under grazing conditions in the high Andean grasslands. Small Rumin. Res. 2021, 205, 106559. [Google Scholar] [CrossRef]
  101. Clauss, M.; Dittmann, M.T.; Vendl, C.; Hagen, K.B.; Frei, S.; Ortmann, S.; Müller, D.W.H.; Hammer, S.; Munn, A.J.; Schwarm, A.; et al. Review: Comparative methane production in mammalian herbivores. Animal 2020, 14, s113–s123. [Google Scholar] [CrossRef] [Green Version]
  102. Frei, S.; Dittmann, M.T.; Reutlinger, C.; Ortmann, S.; Hatt, J.; Kreuzer, M.; Clauss, M. Methane emission by adult ostriches (Struthio camelus). Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2015, 180, 1–5. [Google Scholar] [CrossRef]
  103. Palangi, V.; Macit, M. Indictable Mitigation of Methane Emission Using Some Organic Acids as Additives towards a Cleaner Ecosystem. Waste Biomass- Valorization 2021, 12, 4825–4834. [Google Scholar] [CrossRef]
Figure 1. Global GHG emissions from the livestock sector (%). Reproduced with permission from Rojas-Downing et al. [2].
Figure 1. Global GHG emissions from the livestock sector (%). Reproduced with permission from Rojas-Downing et al. [2].
Sustainability 14 13229 g001
Figure 2. Increasing atmospheric CH4 levels. Reproduced with permission from NOAA [18].
Figure 2. Increasing atmospheric CH4 levels. Reproduced with permission from NOAA [18].
Sustainability 14 13229 g002
Figure 3. Venn diagram of strategies for mitigation and adaptation in the livestock sector. Reproduced with permission from Zhang et al. [24].
Figure 3. Venn diagram of strategies for mitigation and adaptation in the livestock sector. Reproduced with permission from Zhang et al. [24].
Sustainability 14 13229 g003
Figure 4. Utilization of ruminant animal methane emissions according to patent# US 6982161. Right: ZELP “Zero emission livestock project”, EU-project from 2019 (ID: 877091) [95]; Exhaled CH4 (90% comes out of the mouth) is catalytically converted into CO2 in a special mask, which is said to come on the market in 2022.
Figure 4. Utilization of ruminant animal methane emissions according to patent# US 6982161. Right: ZELP “Zero emission livestock project”, EU-project from 2019 (ID: 877091) [95]; Exhaled CH4 (90% comes out of the mouth) is catalytically converted into CO2 in a special mask, which is said to come on the market in 2022.
Sustainability 14 13229 g004
Figure 5. Correlation between body mass (BM) and (a) absolute daily CH4 emissions for different mammalian herbivores. Reproduced with permission from ref. [101].
Figure 5. Correlation between body mass (BM) and (a) absolute daily CH4 emissions for different mammalian herbivores. Reproduced with permission from ref. [101].
Sustainability 14 13229 g005
Table 1. Typical tropical animal supplements for critical seasons.
Table 1. Typical tropical animal supplements for critical seasons.
Animal Nutrient NeedsSupplementCritical Season
EnergyGrains, molassesDry
ProteinUreaDry
RoughageSilage, hayDry and wet
MineralsPhosphorusWet
Data in the table is extracted from Suybeng et al. [31].
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Palangi, V.; Taghizadeh, A.; Abachi, S.; Lackner, M. Strategies to Mitigate Enteric Methane Emissions in Ruminants: A Review. Sustainability 2022, 14, 13229. https://doi.org/10.3390/su142013229

AMA Style

Palangi V, Taghizadeh A, Abachi S, Lackner M. Strategies to Mitigate Enteric Methane Emissions in Ruminants: A Review. Sustainability. 2022; 14(20):13229. https://doi.org/10.3390/su142013229

Chicago/Turabian Style

Palangi, Valiollah, Akbar Taghizadeh, Soheila Abachi, and Maximilian Lackner. 2022. "Strategies to Mitigate Enteric Methane Emissions in Ruminants: A Review" Sustainability 14, no. 20: 13229. https://doi.org/10.3390/su142013229

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop