Animal Science

Rumen environmental and nutritional strategies to mitigate emissions from livestock^*

0000-0003-0828-4610Antonella Chiariotti^{1  *} 

¹CREA, Research Center for Animal Production and Acquaculture, Via Salaria 31, 00015 Monterotondo, Italy

ABSTRACT

Methane is the single largest greenhouse gas produced by ruminants, 28-times the warming effect of carbon dioxide. Methane is a by-product of the anaerobic fermentation of carbohydrates and amino acids in the rumen to a lesser extent. It is produced by archaea, and it is considered a loss of feed energy that could otherwise be used for productivity. Economic progress and the world’s growing population will increase meat and milk product demands; when ruminant livestock increase, methane production increases, accelerating global warming in the process inevitably. A massive worldwide research effort has investigated various mitigation strategies that can be grouped into three categories: animal and feed management, diet formulation, and rumen manipulation. These approaches affect directly or indirectly the rumen microbiome thereby reducing rumen methanogenesis. The strategy is to improve forage quality or change the forage type or proportion or add supplements such as probiotics, oils, and enzymes that either reduce methanogenesis or shift the metabolic pathways leading to the H₂ reduction as a useful substrate. Methanogens community composition rather than its size seems correlated to methane production and the diversity is influenced by H₂ availability and interactions within and between H₂-producing microbes in the rumen, so research needs to study the different mechanisms of methanogenesis according to dietary and environmental conditions in different ruminants’ species.

Key words: GHG mitigation strategies; methane; methanogenesis; rumen microbiome

Methane is a greenhouse gas (GHG) far less abundant than CO₂ but with a global warming potential 28-times more powerful on a 100-year scale (^{Jackson et al. 2020}). The more abundant methane sources include anthropogenic emissions from agriculture, waste management, fossil fuels, and natural emissions from wetlands, freshwater systems, and geological sources (^{Saunois et al. 2016}). Agriculture contributes with a percentage varying from 8 to 18 % of total anthropogenic GHG emissions and the ruminants account for about 81 % of GHG from the livestock which involves enteric fermentation (around 90 %) and manure management (^{Hristov et al. 2013}). Among ruminants-related direct emissions, cattle are responsible for 65 %, buffaloes for 8 %, and sheep and goats for 7 % (figure 1) (^{Steinfeld et al. 2019}). Based on 2010 GHG emissions, to limit global warming to 1.5 °C, agricultural emissions should be decreased by 11-30 % by 2030 and by 24-47 % by 2050 (^{Arndt et al. 2022}).

Figure 1 Global and livestock sector methane emissions 

Livestock sustains the livelihood of millions of people in the world (up to 12 %), both in developing and developed countries. The world’s population has been estimated to reach 9.7 billion in 2050 and 10.4 billion in 2100 (^{UN 2022}), particularly in Low- and Middle-income Countries (LMC) along with increasing production and demand for milk and meat products by 35 % (1168 Mt) and 44 % (373 Mt), respectively (^{IFCN 2018}).

There is a growing concern that the demand for animal products, associated with population growth, prolonged lifespan, and improved economic welfare in developing countries, will put an unsustainable call on the environment (^{Salter 2017}). Nevertheless, ruminants, especially when fed with feedstuff produced on land not suitable for primary cropping or by-products from agro-industrial, can be a net contributor to the global supply of human edible food, maintaining and enhancing the provision of protein and essential micronutrients (zinc, calcium, Vit.B₁₂, and riboflavin) (^{Scollan et al. 2011}).

A massive worldwide research effort has investigated various mitigation strategies that can be summarized into three categories: changes in animal and feed management, diet formulation, and rumen manipulation (^{Arndt et al. 2022}). All the strategies potentially involve changes in the rumen microbiome (^{Tapio et al. 2017}). Rumen methane production also represents a loss of energy (from 2 to 12 % of gross energy intake) for animal growth and production (^{Johnson and Johnson 1995}). Thus, lowering CH₄ emissions would benefit the environment and eventually the livestock production efficiency.

Rumen microbial community and methanogenesis. Ruminants live on plant matter using their specialized digestive system with a well-adapted symbiotic web of microorganisms (^{Cammack et al. 2018}) which includes ciliate protozoa, anaerobic fungi, bacteria, and archaea that have co-evolved with their host (^{Henderson et al. 2015}, ^{Sasson et al. 2017} and ^{Huws et al. 2018}). Protozoa can be up to half of the rumen biomass (^{Hungate 1966} and ^{Newbold et al. 2015}), fungi that may reach 20 % (i.e., sheep, ^{Rezaeian et al. 2004}), archaea between 0.3-4 % (^{Janssen and Kirs 2008}) and the bacteria as the largest group.

Microbial fermentations in the rumen play an essential role in the ability of ruminants to utilize lignocellulosic materials to produce volatile fatty acids (VFAs) and to convert non-protein nitrogen into microbial protein, which is an essential source of energy and protein for the host, while the rumen provides the microbes a suitable environment to thrive and grow (^{Cammack et al. 2018}). Nevertheless, microbes also have potential environmental detrimental effects through the emission of GHGs and excessive N excretions in feces and urine.

Rumen methanogenesis carried out by archaea follows two main pathways (^{Tapio et al. 2017}). The hydrogenotrophic route converts H₂ and CO₂ produced by protozoa, fungi, and bacteria in CH₄ thus reducing the metabolic (^{Kittelmann et al. 2013} and ^{Poulsen et al. 2013}). Formate, which can be used by all the most abundant archaea, is considered equivalent and is included in the hydrogenotrophic category (^{Janssen and Kirs 2008} and ^{Janssen 2010}). The second pathway uses methyl groups as substrates, such as those present in methylamines and methanol (^{Poulsen et al. 2013} and ^{De la Fuente et al. 2019}). If H₂ accumulates in the rumen NADH re-oxidation, microbial growth, forage digestion, and associated production of acetate, propionate, and butyrate are inhibited, so any mitigation strategy that reduces methanogens populations must include some pathway for H₂ removal from the rumen (^{Eckard et al. 2010}).

Propionate production is the second major H₂ sink in the rumen plus other minor such as nitrate/nitrite reduction, reductive acetogenesis, and unsaturated fatty acid biohydrogenation (^{Mitsumori and Sung 2008} and ^{Kobayashi 2010}). Therefore, for optimum rumen function, the methane reduction strategy must be paralleled by the enhancement of propionate production without compromising feed digestion, stimulating H₂ utilizing pathways, and inhibiting the population and activity of methanogens (^{Martin et al. 2010}).

So, methanogens in the gastrointestinal tract produce methane as a by-product of anaerobic fermentation (^{Tapio et al. 2017}). As the sole producer, it would be reasonable to consider the increase in number to be associated with the greater production of CH₄. Nonetheless, it would seem that methanogens community composition rather than its size is correlated to methane production and that this diversity is influenced by H₂ availability and interactions within and between H₂ producing microbes in the rumen (^{Tapio et al. 2017}, ^{Abbot et al. 2020} and ^{Pitta et al. 2021}).

Culture-independent next-generation sequencing together with “omics” approaches, developed in recent years, have become powerful tools to understand which microorganisms are in the rumen, which role they play in methanogenesis, and what is the effect of mitigation strategies. Reports from ^{Söllinger et al. (2018)} and ^{Söllinger and Urich (2019)} have found that less abundant methanogenic lineages may have a more significant role in CH₄ formation than the most represented rumen methanogens. Methanogens are less diverse than ruminal bacteria, and the type and abundance variation is due to host genetics as well as dietary, environmental, and ruminal factors (i.e., H₂ concentrations, pH, and interactions with other fermenting microbes). A deeper understanding of methanogens diversity under different environmental conditions and the mechanistic basis of methanogenesis are necessary to develop targeted and effective enteric methane mitigation strategies (^{Pitta et al. 2022}).

Mitigation strategies. Several reviews indicate the three main roads for mitigation are: animal and feed management, diet formulation, and rumen manipulation (^{Hristov et al. 2013}, ^{Veneman et al. 2016}, ^{Arndt et al. 2022} and ^{Tseten et al. 2022}). Nevertheless, according to ^{Arndt et al. (2022)} methane yield is not the only relevant measure, other CH₄ emissions and animal performance metrics should be considered to estimate the feasibility of mitigation strategies. In this paper, only the nutritional strategies (diet formulation and rumen manipulation) will be evaluated (figure 2).

Figure 2 Mitigation strategies diagram for the reduction of CH₄ in ruminants 

Diet formulation. Dietary manipulation by changing the feed composition and quality is a simple approach that may enhance animal productivity and reduces GHG emission (^{Khusro et al. 2021}). This strategy alone could obtain interesting results depending on the method or nature of the nutritional intervention (^{Mosier et al. 1998} and ^{Benchaar et al. 2001}). The predominant approach is to improve forage quality or change the forage type or proportion or add supplements such as probiotics, oils, and enzymes that either reduce methanogenesis or alter the metabolic pathways leading to the H₂ reduction as a useful substrate.

Forage quality. CH₄ production might be reduced by improving forage quality, feeding less-mature plants, switching from C₄ to C₃ grasses, or even grazing on less-mature pastures (^{Ulyatt et al. 2002} and ^{Beauchemin et al. 2008}). These forages contain higher amounts of easily fermentable carbohydrates and less NDF, leading to a higher digestibility and faster passage rate in the rumen. In contrast, more mature forage induces a higher CH₄ yield mainly due to an increased C:N ratio, which decreases the digestibility.

Methane production per unit of cellulose digested is three times that of hemicellulose (^{Moe and Tyrrell 1979}). Cellulose and hemicellulose ferment more slowly than non-structural carbohydrates, thus yielding more CH₄ per unit of the digested substrate (^{McAllister et al. 1996}). Consequently, the addition of grain to the diet increases starch and reduces fibre intake, reducing the rumen pH and favouring the production of propionate rather than acetate in the rumen (^{McAllister and Newbold 2008} and ^{Hills et al. 2015}). Improving forage quality also tends to increase the DM intake and reduce the retention time in the rumen, promoting energetically more efficient post-ruminal digestion and reducing the proportion of energy converted to CH₄ (^{Blaxter and Clapperton 1965}). Methane emissions are also commonly lower with higher proportions of forage legumes in the diet, partly because of the lower fibre content, the faster retention time, and in some cases, the presence of condensed tannins (^{Beauchemin et al. 2008}).

Improving forage quality can both improve animal performance and reduce CH₄ production, but it can also improve efficiency by reducing CH₄ emissions per unit of animal product (^{Beauchemin et al. 2009}). However, many of these strategies may also provide the farmer with an opportunity to increase the stocking rate, leading to a no net change or even a net increase in CH₄ production. Similarly, the addition of more grain to the diet will incur additional N₂O emissions and transport during the grain production processes.

Forage processing and preservation also affect methane emissions (^{Beauchemin et al. 2008}). Chopping or pelleting forages reduces the feed size and consequently less degradation in the rumen as well as CH₄ emissions per kg DM intake (^{Boadi et al. 2004}).

Therefore, further research and modelling are required to understand the likely relationships between improvements in diet quality and voluntary intake, stocking rates, and net CH₄ production in various production systems.

Lipids. The efficacy of fat supplementation depends on the fat source, quantity, fatty acid profile, the form in which the fat is added (refined oil/full-fat oilseeds), and the diet (^{Bauchemin et al. 2008}). Fats supplementation effect could be summarized as: reduction of fibre digestion (mainly in long-chain fatty acids); decreased DM intake (if total dietary fat exceeds 6-7 %); decreased organic matter fermentation; reduction of activities of different microbes including methanogens and hydrogen producing microorganisms; reduction of rumen protozoa number; and to a limited extent biohydrogenation of unsaturated fatty acids which serve as a hydrogen sink, although only 1-2 % of the metabolic hydrogen in the rumen is used for this purpose (^{Bauchemin et al. 2008},^{Eckard et al. 2010} and ^{Samal and Dash 2022}).

The addition of different vegetable oils (soybean, coconut, canola, rapeseed, sunflower, linseed) to ruminant diets has been shown to reduce CH₄production. Moreover, fats are not metabolized in the rumen and therefore do not contribute to methanogenesis (^{Johnson and Johnson 1995}). Seen the substantial body of literature, lipids addition to the diet is considered a promising technique.

Essential oils and plant metabolites. Supplements from biological sources have been investigated recently as feed ingredients and additives to mitigate emissions (^{Salem et al. 2014} and ^{Bayat et al. 2018}).

^{Tekippe et al. (2012)} tested 100 essential oils (EO) and plants for their ability to reduce methanogenesis. Essential oils are volatile and aromatic oily liquids extracted from plant materials such as flowers, seeds, buds, leaves, herbs, wood, fruits, twigs, and roots (^{Burt 2004}). They demonstrate broad-spectrum antimicrobial properties, inhibit rumen archaea, alter the rumen fermentation path by inhibiting fibrolytic bacteria (^{Cobellis et al. 2016}), and are generally considered safe for human and animal consumption (^{Davoodi et al. 2019}). Some inhibit the growth of protozoa indirectly or by biohydrogenation of unsaturated fatty acids limiting the hydrogen availability for methanogens (^{Iqbal et al. 2008} and ^{Toprak 2015}). Nevertheless, they produce a scarce effect in vivo, probably due to the rumen adaptation mechanism. Moreover, the reduction of fibre digestibility is another issue as it reduces animal performance (^{Benchaar and Greathead 2011}).

Numerous researches evaluated the efficacy of plant secondary metabolites as a mitigation strategy, (including saponins, flavonoids, tannins, and other terpenoids), mostly in vitro and with inconsistent results. Hydrolyzable tannins inhibit rumen methanogens bacteria, while condensed ones inhibit fibre digestion (^{Khusro et al. 2021}). Saponins decrease protein degradation and favour microbial and biomass synthesis (^{Makkar and Beker 1996}), two processes that reduce hydrogen availability (^{Dijkstra et al. 2007}). However, the saponins effect seems related to their anti-protozoal effect (^{Newbold and Rode 2006}).

Additional Organic Additives Biochar has also been tested in the last decade because of its effect on growth, egg yield, blood profiles, inhibitory effects against the growth of rumen pathogens, and the reduction of enteric methane emission (^{Leng et al. 2012} and ^{Man et al. 2021}).

Seaweeds. Seaweeds known as macroalgae, including brown (Phaeophyta), red (Rhodophyta), and green (Chlorophyta) seaweeds are rich in bioactive compounds including proteins, carbohydrates, and to a lesser extent, lipids, saponins, alkaloids, and peptides. These bioactive could also play a role as feed ingredients to decrease enteric CH₄ (^{Abbott et al. 2020}). The reduction is largely attributed to the compound bromoform which is found in several seaweed species especially red seaweeds like Asparagopsis spp. and is known to inhibit the CH₄ biosynthetic pathway within methanogens (^{Machado et al. 2015}).

Several in vitro studies of seaweed supplements have been carried out, but gaps remain in current knowledge regarding the efficacy of seaweeds to tackle climate change both as a diet supplement and feed for livestock. The potential positive and negative environmental and economic impacts of seaweed farming on a large scale are still to clarify (^{Abbott et al. 2020}).

Additives. Several additives consisting of either inorganic or organic compounds or direct-fed probiotics have been added to feed to reduce methane emissions in ruminants. These additives either directly inhibit methanogens or alter the metabolic pathways leading to a reduction of the substrate for it (^{Halmemies-Beauchet-Filleau et al. 2018} and ^{Haque 2018}).

Exogenous enzymes. Cellulase, xylanase, and hemicellulase have been used in ruminant diets as feed additives. These enzymes can improve fibre digestibility and animal productivity (^{Beauchemin et al. 2003}). They also decrease the acetate/propionate ratio in the rumen, thus reducing CH₄ production (^{Eun and Beauchemin 2007}). However, the supplementation of exogenous enzymes at the farm level is very limited (^{Khusro et al. 2021}).

Ionophores. Commercially available ionophores such as monensin, lasalocid, salinomycin, and laidlomycin are widely applied as feed additives to dairy cows’ diets in many countries and have been used to increase milk production, improve feed efficiency and prevent metabolic disorders (^{McGuffey et al.2001}). They benefit animal metabolism by enhancing the efficiency of energy metabolism, improving ruminal nitrogen metabolism while modulating intake, optimizing fermentation routes, and reducing the rates of digestive disorders (^{Duffield et al. 2012}). Ionophores also act as antimicrobials, preferentially inhibiting gram-positive bacteria that produce lactate, acetate, butyrate, formate, and hydrogen as end products, resulting in a propionate increased and an acetate-reduced concentration (^{Marques and Cooke 2021}). They also affect protozoa (^{Guan et al. 2006}).

The pressure to reduce the use of antimicrobials in livestock production suggests that is not a long-term solution. Furthermore, this family of additives is not permitted in many countries, Europe included.

Organic acids. The addition of organic acids like fumarate, malate, and acrylate, precursors to propionate production in the rumen, can be an alternative H₂ sink, reducing methanogenesis. ^{McAllister and Newbold (2008)} reviewed studies that showed 0 % - 75 % reductions in CH₄ achieved by feeding fumaric acid. Organic acid supplementation has mostly been tested for CH₄ production in vitro, producing inconsistent results. Moreover, at the relatively high doses required, dicarboxylic acids are prohibitively expensive as an abatement strategy.

Rumen manipulation. Manipulating microbial populations in the rumen either by chemical means or by introducing competitive or predatory microbes, or with vaccination approaches, can reduce CH₄ production. Biological control strategies, such as bacteriophages or bacteriocins, could prove effective in directly inhibiting methanogens and redirecting H₂ to other reductive rumen bacteria, such as propionate producers or acetogens (^{McAllister and Newbold 2008}). However, they still require significant research for a prolonged period to deliver commercially viable vaccines or biological control options that might be useful in different production systems and areas.

Vaccination. Methane reduction in ruminants could be obtained by vaccination and the strategy has been considered promising by many authors. Numerous trials are reported to reduce methane emissions by vaccination with extremely variable results (from a 20 % increase to a 69 % reduction in methane production, ^{Baca-Gonzalez et al. 2020}). Some of the causes of vaccination failures in reducing methane output are methanogens diversity, different animal-rearing conditions, and rumen adaptation (^{Williams et al. 2009}). Nevertheless, it is complicated to evaluate the real effectiveness of this strategy as few studies have directly assessed the complete approach, i.e., from vaccination to enteric animal CH₄ emission measurement. Therefore, for successful vaccination against methanogens, a much more broad-spectrum approach is required with a greater understanding rumen methanogen population (^{Mir and Begun 2022}).

Defaunation. Defaunation is the protozoa removal from the rumen. It has been reported to reduce methane emissions by as high as 50 % depending on the diet (^{Hegarty 1999}). The protozoa are associated with methanogens and are large producers of H₂ in the rumen so favouring the process of methane production by methanogens.

In defaunated animals, the lower methane production was sustained for more than two years which indicates a stable change induced by defaunating agents (^{Morgavi et al. 2008}). However, in some cases, this reduction in methane production is not consistent (^{Hegarty et al. 2008}). Moreover, it may negatively affect the normal rumen functions and in turn the animals’ performance (^{Mir and Begun 2022}).

Direct-fed microbials. Direct-fed microbials (DFM) is defined as a single or mixed culture of live organisms, which promotes desirable rumen microflora and provide beneficial effects when fed to animals (^{Krehbiel et al. 2003}). Various rumen bacteria are thought to compete with methanogens for the hydrogen supply by promoting propionogenesis, acetogenesis, and nitrate/nitrite or sulfate reduction which can serve as an alternative H₂ sink. This redirects the metabolic flow of rumen hydrogen toward VFAs production which could otherwise be used for methanogenesis (^{Ungerfeld 2015}).

Since H₂ is a limiting substrate for methane production, the addition of propionate-forming bacteria might help in lowering methane production (^{Jeyanathan et al. 2014}). However in vivo, Propionibacteria spp. do not last in the rumen of cattle when a starch-rich diet is administered. High starch fermentation results in an increased molar proportion of propionate reducing their efficacy (^{Jeyanathan et al. 2019}).

Acetogens. Homoacetogens are a group of bacteria producing acetate (^{Drake et al. 2008}). In vitro studies have also suggested that acetogenesis could serve as an alternative to methanogenesis in eliminating H₂ from the rumen (^{Morvan et al. 1996}). Nevertheless, ^{Lopez et al. (1999)} reported that high concentrations of acetogenic bacteria cannot compete against methanogens for H₂ disposal, making it unclear whether homoacetogens could play a pivotal role in the ruminal ecosystem (^{Henderson et al. 2010}).

Methane Oxidizing Bacteria (MOB) is a class of bacteria that can grow on methane as a sole carbon and energy source. However, in vivo studies using MOB as probiotics are scarce and need to expand to verify its probiotic potential.

Conclusions

As the demand for meat and milk products rise, methane emissions and global temperature increase. So, developing an efficient and effective methane mitigation strategy while improving animal performance is critical in achieving agricultural sustainability.

Even if a huge effort has been put into the study of the composition and function of the rumen microbiome, it becomes clear that there is a long way to go to truly understand the relationship between microbial community and methanogenesis. A deeper knowledge of methanogens diversity under different environmental conditions and the mechanistic basis of methanogenesis are necessary to develop targeted and effective enteric methane mitigation strategies.

Currently, the under-representation of certain strategies, geographic regions, and long-term studies are the main limitations in providing an accurate quantitative estimation of the mitigation potential of each strategy under diverse animal production systems. So future research needs to focus on: developing new mitigation strategies, particularly for pasture-based livestock rearing systems; deepening the comprehension of the combined effect of various mitigation strategies; investigating the effect on growing and non-lactating animals; identifying the obstacle to large-scale adoption of effective strategies, especially in high- and low-income countries. A multidisciplinary approach that considers the environment, livestock management, diet and rumen microbiome seem to be the best approach to finding a long-term solution to reduce enteric methane production by ruminants.

Note

*Conference presented in the Convención Producción Animal y Agrodesarrollo 2022 celebrated on October 11-14, 2022 in Plaza America Convention Center, Varadero, Cuba.

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Received: March 20, 2023; Accepted: May 27, 2023

^*E-mail: [e-mail]

Conflict of interest: The author declare that there was not conflict among them.