Harnessing plant bioactivity for enteric methane mitigation in Australia

Keywords: methane, mitigation, rumen, forages, plant-based feed additives, plant bioactive compounds.

Ruminants can consume and digest large amounts of plant material and convert it into high-quality products such as meat, milk and wool, by virtue of microbial fermentation in their gut, where volatile fatty acids (VFA) and methane (CH₄) are produced as end products of the fermentation. While VFA present a major energy source for the animal, the CH₄ serves as the main pathway of eliminating hydrogen in the rumen (Beijer 1952). In the past century, enteric CH₄ has been regarded simply as a loss of energy from ingested feed, but in more recent times, it has become of concern as a major greenhouse gas (GHG; Johnson and Johnson 1995). About 70% of the CH₄ produced on Earth is generated from anthropogenic sources, and ruminant livestock is the single most significant contributor (Moss et al. 2000). Each ruminant animal produces and eructates 5–130 kg of CH₄ year, depending on its size and the amount of fibrous material consumed in the diet (Johnson and Johnson 1995). Enteric CH₄ has been estimated to contribute half of the total GHG emissions from the agricultural sector (Swainson et al. 2018; Dong et al. 2019).

Methane is a highly potent GHG, being more effective than carbon dioxide (80 times over 10–20 years, or 28 times over 100 years from release), but has a shorter atmospheric lifetime of 12 years from release, compared with either carbon dioxide at 50–200 years from release, or nitrous oxide at 120 years from release (EPA 2003). Thus, enteric CH₄ is an attractive target for reducing overall GHG production. A reduction of 10% in enteric CH₄ production could be sufficient to prevent further accumulation of CH₄ in the atmosphere (Moss et al. 2000). In Australia, CH₄ emissions from livestock account for 60–70% of total GHG emissions from the agricultural sector (Cottle et al. 2011; Taylor et al. 2016). The size of this contribution is partly due to the large number of ruminants; Australia is a significant player in global food supply, accounting for ~4% of global beef production (Suybeng et al. 2019). Australian CH₄ emissions from livestock are also significant because most ruminants are managed under extensive conditions where the animals usually graze low-quality, fibrous diets that promote relatively high CH₄ production in the rumen compared with feedlot or dairy cattle offered high-grain diets (Charmley et al. 2008).

Early CH₄ mitigation strategies focussed on removal of protozoa from the rumen, because a portion of the methanogenic archaea in the rumen live in close association with them (Blaxter and Czerkawski 1966; Whitelaw et al. 1984). Subsequently, concepts and approaches broadened in the recognition that enteric CH₄ is a significant contributor to atmospheric pollution and global warming. The outcome was global development of solutions, including manipulation of animal physiology, genetics and management of the rumen microbiome by manipulation of diet composition and the use of feed additives (reviews: Moss et al. 2000; Busquet et al. 2006; Calsamiglia et al. 2007; McAllister and Newbold 2008; Hristov et al. 2013; Patra et al. 2017; Beauchemin et al. 2020; Min et al. 2020).

Early attempts to reduce enteric CH₄ emissions frequently relied on synthetic chemicals and antibiotics, but often with only modest benefits (reduction by only 10% in vivo), that were also variable (Johnson and Johnson 1995) and mostly ineffective in grazing animals (Grainger et al. 2010). Emerging concerns over the impact of antibiotics in feed on human, animal and environmental health led to legislation of restrictions on their use. The result was a worldwide search for natural, safe and sustainable alternatives, with a particular focus on plants and plant products.

The primary constituents of forage plants, including soluble and insoluble carbohydrates and oils, can drive the ‘methanogenic potential’, namely, amount of CH₄ produced when consumed and fermented by rumen microbes, but many plant secondary compounds (PSC) can also affect methanogenesis by acting directly and specifically on methanogens, or by acting indirectly on the overall processes of fermentation in the rumen (Bodas et al. 2012). The aim of a CH₄ mitigation strategy is to reduce CH₄ emissions, while not reducing overall digestibility/fermentability of the feed consumed. In that respect, a reduction in the concentration of VFA in the rumen can be used as an approximation for assessing negative effects of a strategy on overall feed digestibility/fermentability.

The present paper reviews current developments and strategies for the use of plant bioactivity to reduce enteric CH₄ emissions in Australia. We focussed on mitigation approaches based on the grazing of low methanogenic forages, the feeding of plant by-products as supplements, the use of whole plant extracts, essential oils and pure PSC, and also considered some commercially available plant-based products. We first illustrated each of these mitigation strategies with some of the work done globally, and then focussed on work in Australia, critically evaluating the prospects for local success. We compared the strategies in terms of national potential for CH₄ mitigation, agronomic and animal production benefits, and barriers and limitations to their use. This structured approach allowed us to finally analyse the options and prospects for practical applications in Australia.

Enteric CH₄ emissions from grazing animals can be targeted by manipulating the forage they consume, because there is significant variation among plant species in their methanogenic potential. There is worldwide interest in commonly used forages, but also in region-specific and novel grazing plants. Among the mainstream forages, the most prominent candidates with low-to-moderate methanogenic potential are lotus (Lotus corniculatus, L. pedunculatus), sulla (Hedysarum coronarium), lucerne (Medicago sativa), chicory (Cichorium intybus), white clover (Trifolium repens) and red clover (Trifolium pratense; Tavendale et al. 2005; Navarro-Villa et al. 2011; Hammond et al. 2013). Tropical forages have been found to be particularly effective at reducing rumen CH₄ production, in vitro and in vivo, with a wide variety of effective fodders from diverse plant families being reported (Hariadi and Santoso 2010; Silivong et al. 2013; Pal et al. 2015). The reduction in CH₄ production in these forages was generally attributed to the presence of PSC, particularly tannins, with reductions by up to 25% (kJ/MJ gross energy intake) seen with tannin-rich shrubs and trees (Soliva et al. 2008; Tiemann et al. 2008).

Work on low-methanogenic forages has been particularly strong in Australia, because feeding systems rely so heavily on pasture-based grazing, with minimal grain supplementation. In that respect, native woody perennial plants (trees and shrubs) seem able to play an important role, especially in low-rainfall areas, while tropical forages are utilised in the tropical and subtropical regions. There is also emerging evidence that grazing ruminants in Australia have a high methanogen diversity and harbour some unique methanogen populations (Wright et al. 2004; Rea et al. 2007; McSweeney and Tomkins 2015).

The search for variability in methanogenic properties in grazing plants in Australia began with an investigation of forage shrubs when 128 Australian native forage shrubs were assessed using in vitro 24-h batch culture (Durmic et al. 2010). Several highly potent candidates were revealed, with almost half of the species tested producing less CH₄ than with oaten chaff, a common supplementary feed. One plant in particular, commonly known as tar bush (Eremophila glabra), reduced CH₄ production by 81%. This CH₄ mitigation effect was subsequently confirmed using a continuous in vitro system (Li et al. 2014) and in vivo using sheep (Li 2013, K. Lund, pers. comm.). Eremophila species produce abundant terpenes and flavones that are potent CH₄ inhibitors (Oskoueian et al. 2013), and the effect in E. glabra was linked to direct inhibition of methanogenic populations (Li et al. 2014). However, E. glabra had a general inhibitory effect on fermentation, with a 15% reduction in VFA concentrations when it is used as the sole substrate in vitro (Durmic et al. 2010). However, the anti-methanogenic effect of E. glabra is sufficiently potent so that it can be used in a mix with other forages, thus moderating negative effects while still significantly reducing CH₄ (Li et al. 2014). E. glabra is well adapted to drought and infertile soils, two critical issues in our grazing systems, and it has an advantageous mineral profile, but it may be constrained by relatively low biomass production and poor palatability compared with some mainstream pastures (Revell et al. 2013). Such problems are likely to respond to plant improvement, or by just ensuring it is integrated as part of a mixed forage base in grazing systems; however, further research is needed for E. glabra to be widely adopted in grazing systems.

Research has been conducted on the plants from the Australian tropics and subtropics. These species are particularly important because that region is home to half of Australia’s beef cattle, so it is responsible for the majority of the nation’s enteric CH₄ emissions (AGEIS 2017). Among those with low-to-moderate methanogenic potential are both grasses (Andropogon gayanus, Brachiaria ruziziensis, Bothriochloa decipiens, Sorghum plumosum, Urochloa mosambicensis) and leguminous forages (Calliandra calothyrsus, Desmanthus leptophyllus, Gliricidia sepium, Stylosanthes scabra, Leucaena leucocephala; Meale et al. 2012; Durmic et al. 2017; Suybeng et al. 2019). These species often contain tannins that can directly reduce the amount of CH₄ produced (Piñeiro-Vázquez et al. 2018), but these forages can also reduce CH₄ emission intensity because they improve growth rates and thus animal productivity (Taylor et al. 2016). There are some potential limitations, including eco-geographical constraints and some anti-nutritive or toxic PSC that impede feed intake or affect animal health (Dalzell et al. 2012), but as with all novel feedstuffs, it is important to complete a duty of care assessment (Revell and Revell 2006).

Concurrent with the investigations into tropical and subtropical forages was research focussed on temperate herbaceous forages. In our initial screening of 13 mainstream and alternative pasture species of southern Australia, using fermentation in vitro, we discovered that a legume biserrula (Biserrula pelecinus) produced 73% less CH₄ than did lucerne, and 90% less CH₄ than did the highest CH₄-producing species, bladder clover (Trifolium spumosum; Banik et al. 2013). Subsequently, other mainstream pasture species were investigated, and it was shown that when subterranean clover (Trifolium subterraneum) was fed to sheep, CH₄ production was reduced by 30% compared with feeding ryegrass (Muir et al. 2020). Moreover, the methanogenic potential of subterranean clover is found to be a heritable trait, so it can be manipulated by plant breeding (Kaur et al. 2017). Birds-foot trefoil (lotus) was also explored for its potential, and theoretical estimates suggest that it can reduce the CH₄ emission intensity for wool and prime lamb by increasing liveweight gain and fecundity (Doran-Browne et al. 2015). For some of the temperate forage species, the mitigation effect may be linked to their primary chemical composition and to enhancing productivity, thus reducing CH₄ emission intensity, whereas in others, such as biserrula, the effect may be linked to the presence of specific anti-methanogenic PSCs (Banik et al. 2016).

In addition to the mainstream species, some alternative forages that are aimed at filling seasonal feed gaps in temperate parts of Australia were also investigated. Local varieties of turnip (Brassica rapa), chicory or plantain (Plantago lanceolata) were found to produce ~25% less CH₄ (mL/g dry matter incubated) in vitro than did lucerne (Durmic et al. 2016). Feeding forage brassicas to cattle was found to reduce CH₄ yield (g CH₄/kg dry-matter intake) by 5%, and CH₄ emission intensity (g/kg energy-corrected milk) by 10% (Williams et al. 2016). The mechanism of these effects is largely unknown, but it is likely to be a combination of primary chemical constituents and their PSC.

During this period of exploration of plant bioactivity, it became evident that, while some variation in methanogenic potential was related to plant species, there was also within-species variation. Often due to environmental factors, the same species can differ in primary chemicals, PSC composition, or simply, in moisture, consequently resulting in differences in methanogenic potential (Durmic et al. 2017). As we examined a core collection of biserrula, we also demonstrated variation among cultivars, growth stages and cutting treatments that were not influenced by environmental factors (Banik et al. 2019).

In addition to reducing CH₄, most of the forages mentioned above presented fermentation profiles (as described by production of VFA and the acetate:propionate ratio) that were comparable or better than the respective controls (standard forages), implying that it is possible to target CH₄ without impeding microbial fermentation and thus compromising animal productivity. Figure 1 presents examples of low-methanogenic forages in Australia and their effect on CH₄, and outlines candidates that markedly reduce CH₄ production, while maintaining or even promoting VFA production.

Fig. 1.  The VFA and CH₄ values with different sources of plant bioactive compounds when fermented in vitro or in vivo (marked with *) by rumen microbes and compared with a control forage or diet used in the system. Data generated from: Durmic et al. (2010) (native shrubs); Durmic et al. (2017) (tropical forages); Banik et al. (2013), Durmic et al. (2016) and Williams et al. (2016) (temperate forages); Durmic et al. (2014), Shakeri et al. (2017), Moate et al. (2011), Russo et al. (2017) and Hixson et al. (2018) (by-products); and Grainger et al. (2009), Durmic et al. (2014), Banik et al. (2016) and Shakeri et al. (2017) (plant extracts and essential oils).

Horticulture generates huge amounts of organic waste (prunings, leaves, seeds, fruits, peels, pulp, stones) that is a loss of valuable biomass and is an environmental burden. There is a need for cost-effective, sustainable and environmentally friendly processes for the utilisation of these products. This issue is particularly important in developing countries where livestock industries are constrained by fodder shortages and the high costs of conventional feeds. Horticultural by-products often retain a high nutrient content, so they are attractive as a supplementary feed in animal production. They can also be rich in PSC (Sagar et al. 2018), so many of these materials have been investigated globally for their potential to modulate rumen fermentation and mitigate enteric CH₄ production (McGinn et al. 2009; Benchaar et al. 2013; Castillo-Lopez et al. 2017). The effects are mainly ascribed to increased intakes of fat and high-quality protein (Moate et al. 2011), or in some cases tannins or other PSC.

This concept is also relevant to Australia, where ~1500 kT of fruit and vegetable biomass is wasted each year during production, processing and packing stages, or is simply lost as food waste (ARCADIS 2019). The wine industry generates a by-product, grape marc, that is high in protein, fat, fibre and other nutrients and has been used as a feed supplement for cattle. It contains condensed tannins, which, in turn, can reduce enteric CH₄ production when fed to ruminants (Goel and Makkar 2012).

By-products can contain a substantial amount of crude protein, increasing the excretion of ammonia, or products such grape marc have a high-water content, diluting out the bioactivity, causing product spoilage and increasing the cost of transport. Despite these issues, grape marc, in particular, continues to be a topic of interest because, as a major producer of wine, Australia generates ~200 kT of the by-product annually. However, there has been some inconsistencies in its mitigation potential, because only a limited reduction in CH₄ production was seen when extracts of grape marc were tested in vitro (Hixson et al. 2018), whereas it reduced CH₄ emissions by 20% when fed to lactating cows (Moate et al. 2014). This disagreement could be explained by the difference between in vitro and in vivo methodologies, or by variations in the chemical profiles of various types of grape marc (Russo et al. 2017). The high fibre content and low digestibility of grape marc reduces milk yield when fed to dairy cattle, when used to replace high energy supplements (Moate et al. 2020). However, when grape marc is substituted for feed with a similar energy value, CH₄ emissions are reduced, with little change in productivity (Black et al. 2021).

Feeding ruminants plant oils is another effective way of reducing enteric CH₄ production, while utilising oil-rich waste products generated during the oil-extraction process. Olive cake, cashew nut shell, hazelnut pericarps, and the seeds from sunflower, flax and canola have been identified as CH₄ mitigators (Beauchemin et al. 2009; Watanabe et al. 2010; Niderkorn et al. 2020). The anti-methanogenic action in these involves direct removal of hydrogen during fermentation (Eugène et al. 2008; Rasmussen and Harrison 2011). The products considered in Australia for CH₄ mitigation include brewers’ grains, cold-pressed canola, hominy meal, pequi oil, almond hulls and cottonseed (Moate et al. 2011; Durmic et al. 2014, Duarte et al. 2017; Williams et al. 2018). Among these, almond hulls have been shown to reduce CH₄ production by 25% (Durmic et al. 2014), while preliminary investigations into olive leaves and fruits suggested a 50% reduction in CH₄ production in vitro (Shakeri et al. 2017), and a recent study linked the effect to polyphenol content and shift in bacterial populations (Lee et al. 2021).

The exploration of CH₄ mitigation strategies extended from feeding whole plants or plant products, to a quest for specific bioactive molecules of plant origin. Early reports from Europe showed that extracts from flavouring oils, particularly garlic, reduced CH₄ emissions (Busquet et al. 2005a, 2005b; Chaves et al. 2008).

In Australia, extracts from two native forage plants (i.e. Tar Bush or Kennedia prorepens, as well as biserrula), significantly reduced CH₄ production in vitro (Durmic et al. 2014; Banik et al. 2016). In biserrula, selected fractions were tested against methanogens in pure culture and found to inhibit some key ones, including those found in Australian grazing sheep (Banik et al. 2016). More research is needed to identify specific anti-methanogenic compounds from a variety of candidate plants that can be tested in vivo.

Significant research has been dedicated to studying the anti-methanogenic effects of essential oils, and, globally, those from clove, white thyme, citronella, peppermint, anise and cinnamon have been reported to reduce CH₄ emissions (Patra and Yu 2012; Benchaar 2016; Günal et al. 2017). Essential oils from Australian plants gained attention in the late 1990s as potent antimicrobials for human pathogens (Hammer et al. 1999), leading to assessment of their value for CH₄ mitigation. Essential oils from swamp paperbark (Melaleuca ericifolia), honey myrtle (M. teretifolia) and lemon-scented teatree (Leptospermum petersonii) were found to be very potent and inhibiting CH₄ production by up to 75% (in vitro), although they also inhibited microbial fermentation (VFA) at the doses tested (Durmic et al. 2014). Subsequently, we identified optimal doses that did not affect overall rumen fermentation, but were still effective at reducing CH₄ production (Jahani-Azizabadi et al. 2019). In vitro work is continuing to identify the mechanisms that explain the effect and to optimise the doses of pure active ingredient, after which we will move to in vivo testing.

Tannins and saponins are often abundant in plants of low methanogenic potential, with condensed tannins becoming a major focus for anti-methanogenic compound research (Waghorn 2008; Patra and Saxena 2011; Rira et al. 2013). In vivo studies confirmed the potency of condensed tannins, with emission reductions of more than 50% having been reported (Carulla et al. 2005; Lima et al. 2019). Tannins can act directly, affecting methanogens and protozoa, and preventing methanogens from attaching to protozoa, or act indirectly by inhibiting overall rumen microbial activity, with the subsequent consequence of reducing animal productivity (Kumar and Vaithiyanathan 1990; Ku-Vera et al. 2020).

Saponins have been also considered for CH₄ mitigation because they can control ruminal protozoa and thus reduce the number of methanogens that are directly associated with them (Patra and Saxena 2009; Jayanegara et al. 2012). However, the results with saponin-rich plant sources have been variable, with effects ranging from no CH₄ reduction to moderate reduction in vitro and in vivo (Goel and Makkar 2012; Liu et al. 2019; Molina-Botero et al. 2019). These disagreements could be explained by variation in the saponin source. The most promising candidates reported around the world appear to be Yucca schidigera, Saponaria officinalis, Medicago sativa, Camellia sinensis, Enterolobium cyclocarpum and Quillaja Saponaria, inhibiting CH₄ production by up to 40% (Rodríguez and Fondevila 2012; Patra et al. 2017).

In Australia, Ramírez-Restrepo et al. (2016) reported an 18% reduction in total daily CH₄ emissions (g/day) and a 22% reduction in yield (g/kg dry-matter intake) after feeding steers with tea-seed saponins in combination with Rhodes grass and grain concentrate

Investigation of the active components of essential oils has progressed, also leading to the discovery of some potent pure compounds from these that inhibit CH₄ production in vitro and in vivo, including thymol, carvacrol, cinnamaldehyde, garlic organosulfur compounds, citral, limonene, linalool, α- and β-pinene (Busquet et al. 2005a; Cardozo et al. 2006; Macheboeuf et al. 2008; Joch et al. 2016; Ma et al. 2016). Similar work is currently being conducted on compounds found in Australian plant essential oils.

There are advantages in working with pure compounds. The structure is well known and the effects on CH₄ production can be attributed specifically to the compound itself, presenting opportunities to investigate mechanisms of action. They are more attractive than mixed compounds or whole plants from a commercialisation perspective, because purity can be verified for drug acceptability and efficacy. Once identified, they can be obtained from natural sources, using scaled-up extraction processes, or even synthesised. However, anti-methanogenic effects might be less efficient with a single compound than with a combination of compounds, some of which may not even be identified (Patra et al. 2017).

Plant bioactivity has been explored globally, with a view to the development of commercial products. One of the first, based on essential oil compounds, was Crina^® Ruminant (Akzo Nobel Ltd, Netherlands) that had positive effects on animal production, but with limited effects on CH₄ mitigation (Beauchemin and McGinn 2006; Tomkins et al. 2015; Patra et al. 2017). Another essential oil product, Agolin^® Ruminant (Agolin SA, Switzerland), was more effective and became the first feed additive certified for CH₄ mitigation in ruminants (Carbon Trust Assurance Ltd, https://agolin.ch/certifications/). It contains compounds from coriander seed, eugenol, geranyl acetate and geraniol. In vitro, Agolin^® Ruminant reduced CH₄ production by 30% (Durmic et al. 2014), and when fed to dairy cattle at a rate of 1 g/head daily, it decreased CH₄ production by more than 10% without affecting animal productivity (Belanche et al. 2020). A recently emerged product that is showing promise, Mootral^TM (Mootral, Switzerland), a combination of extracts from garlic and bitter orange, persistently reduced CH₄ production in vitro by 70% (Eger et al. 2018). Activo^® Premium (EW Nutrition, Germany), a mix of microencapsulated PSC, has been reported to reduce enteric CH₄ production in sheep by 26%, while improving rumen fermentation, digestibility and protein synthesis (Soltan et al. 2018). All of these products are commercially available as feed additives in Australia, but, in parallel, the work is progressing towards developing local products.

There are some obvious advantages when using a commercial product for CH₄ mitigation, including the following: it is backed up by extensive research and development; it has passed regulatory requirements; and it is easy to adopt and apply. However, these products do come at a cost, so their use is often limited to intensive industries that can reliably incorporate such additives in the feedlots.

Plant-based approaches to CH₄ mitigation in ruminants may offer several benefits and advantages. Many of the plant sources under consideration are already a major part of ruminant diets, so there is little imposition on the animal and they qualify as ‘natural’. The anti-methanogenic PSC are present, abundant and diverse in some of these plants. In addition to reducing CH₄ production, some bioactive plants and plant-based products have other beneficial properties. They can improve animal feed intake and utilisation, enhance fermentability and digestibility, reduce protein degradability, and increase animal productivity (Aerts et al. 1999; Akanmu and Hassen 2018). A wide variety of these plants and PSC are also effective in managing animal digestive disorders, such as lactic acidosis, controlling animal diseases (i.e. worms), or enhancing animal reproduction (Kotze et al. 2009; Hutton et al. 2010; Durmic and Blache 2012). Many of the bioactive plants that have been investigated in Australia are native (unbred) plants, grown locally; so, they contribute to the preservation of biodiversity and thus a more ‘ecologically friendly’ animal production system. Adding these native forages to the production system has also been reported to add value to the feed-base (Vercoe et al. 2009; Revell et al. 2013) and improve overall farm profitability (Monjardino et al. 2010). Further, if plant-based bioactive compounds are derived from organic waste that would otherwise end up as landfill, then the CH₄ mitigation achieved by feeding them to livestock is accompanied by a reduction in environmental pollution and gas emissions from the secondary fermentation.

Plant-based CH₄ mitigation strategies, while having many advantages, also have certain limitations and present challenges. Propagation and utilisation of low methanogenic forages may be restricted to a single geographical location, climate or season, with constraints in their nutritional profile, supply, biomass, or because the strategy to incorporate them is not feasible for all animal production systems. Tannin- and saponin-rich browse and extracts are too often restricted in their application due to the depression of feed intake, fermentation and milk yield (Busquet et al. 2005b; Hess et al. 2006; Tan et al. 2011; Castro-Montoya et al. 2012). The use of industry by-products is often limited because their high water content can lead to spoilage, as well as increased cost of transport and processing. High content of protein, tannin, sugar or lignin may also affect the animal directly, by inhibiting rumen function, or lead to increased GHG emissions from manure of animals fed these by-products (Hünerberg et al. 2014). Vegetable oils and fats that remain in oil by-products can also have negative effects on milk production (Martin et al. 2008), whereas tannins and terpenes may leave residues and taint the animal products (Mason et al. 2017). Although essential oils are considered natural, with a history of use in traditional medicine, some toxic effects have been recorded in livestock (Horky et al. 2019).

However, the main problems of progressing plant-based approaches for CH₄ mitigation are confirmation of effectiveness in vivo and finding the optimal dose and mode of delivery. Many reports have failed to demonstrate in vivo efficacy of promising candidates that have emerged from in vitro screening (Meale et al. 2014; Benchaar 2016). For those that are shown to be effective in vivo, doses are often too high, so there are adverse effects on rumen microbes, or the feeding requirements are simply impractical (Benchaar et al. 2008; Macheboeuf et al. 2008; Grainger et al. 2009). There is also the effect of the interactions among host species, genotype, rumen conditions and animal diet, limiting extrapolation to specific production systems and situations (Calsamiglia et al. 2007; Patra and Saxena 2009; Castro-Montoya et al. 2012). For example, some plant-based feed additives are most effective when combined with a high-fibre diet (Shakeri et al. 2017), whereas others are better suited to combination with concentrate rations (Calsamiglia et al. 2007). Furthermore, most in vivo data in the literature are derived from short-term trials. As a result, extrapolation to production systems becomes difficult because the rumen microbes can adapt to the PSC (Moss et al. 2000; Busquet et al. 2005a; Pellikaan et al. 2011), or degrade them into metabolites with less bioactivity (Malecky et al. 2012; Ghaffari et al. 2015). These adaptations can explain reduced efficacity over time of candidate PSC in vivo (Benchaar et al. 2008). We also need to take testing beyond laboratory-based or animal house-type in vivo studies and assess candidates and plant-based strategies under commercial conditions. This issue becomes evident when we consider extensive grazing systems in which the amount of bioactive compound that an animal ingests is unpredictable. Moreover, in some production systems, the application of plant bioactivity may not be practical or cost-effective.

Table 1 and Figs 1 and 2 present an overview of benefits and limitations of plant-based mitigation strategies for Australian ruminant industries, summarised from information provided by Black et al. (2015, 2021) and other literature cited in the present review. Briefly, in Fig. 1, we have summarised the information on the level of CH₄ reduction, as well as the effect on rumen fermentation (VFA production) gathered in Australia and for different sources of plant bioactivity. In Table 1, we have then summarised the extent (moderate–high) and the type (specific–nonspecific) of effect on CH₄ for each category. In there, we have also evaluated the other benefits to animal production, such as good agronomic properties and nutritive value of the plant material fed, effect on fermentation and animal health, and, consequently, on animal productivity and welfare. We have also considered the barriers and limitations to adoption for each practice. Finally, we sourced information from Black et al. (2021) to plot these mitigation categories according the predicted time to practical application, barrier/cost to implement, and the national CH₄ mitigation potential in Australia based on 25% reduction in CH₄ emissions across all Australian ruminants and 10% adoption. We then used the information on the barriers and limitations, whether the methodology is something that producers are familiar with, whether the plant used in the strategy has good agronomic properties, biomass and NV, so as to estimate and present ‘likelihood of adoption’ (low–high).

Table 1.  Summary of potential benefits and limitations for Australian ruminant industries from mitigation strategies involving plant bioactive compounds
Values for CH₄ mitigation potential (Mt/year) are national estimates

Fig. 2.  Distribution of plant-based strategies for enteric CH₄ mitigation according to predicted time to practical application (years), barrier/cost to implement (relative score: 1 (low) to 20 (high)). The bubble size illustrates the predicted national CH₄ mitigation potential from each strategy in Australia, based on 25% reduction in CH₄ emissions across all Australian ruminants and 10% adoption, while the shade of the bubble (white (low) to dark (high)) illustrates predicted likely level of adoption. Information from modified from Black et al. (2021).

Given the Australian focus on grazing livestock, changing forage species available for consumption seems the obvious first option. The wide range of eco-climatic zones, from tropical to temperate, to hostile, dry environments, will also dictate the strategies that are most applicable. The natural, sustainable, cost-effective solutions for CH₄ mitigation in grazing ruminants are therefore likely to be low-methanogenic browse, i.e. native forage shrubs in low- to medium-rainfall zones; mainstream/alternative herbaceous plants for temperate climates; tropical or rangeland plants for the northern regions of Australia.

Temperate forages such as subterranean clover and lucerne are highly ranked in terms of national mitigation potential and practicality; they achieve only a moderate reduction in CH₄ production, but they offer a significant reduction in CH₄ emission intensity due to their high nutritive value and positive effect on other fermentation pathways. They are familiar to producers, and despite requiring high inputs for sourcing, establishment, cultivation and maintenance, they are likely to have a high adoption rate, and as such can contribute significantly to national CH₄ mitigation overall (Fig. 2). By contrast, the current estimates for Australian native forage shrubs predict that these have a smaller role in national mitigation, as they are geographically contained and need to be grazed in a mix to offset any deficiencies in nutritive profile or negative effects on the rumen, animal health and productivity. Greater implementation is also limited by our incomplete agronomic knowledge of the species and insufficient analysis of the anti-methanogenic properties in a wider range of native plants that are naturally present in the feedbase. These limitations extend the timeline of more widespread adoption, which is currently limited to areas of marginal land and as a drought reserve (Fig. 2). Research is required to overcome these knowledge gaps, so the shrubs are contributing more to the feedbase in a variety of regions. As some of them have a strong, direct anti-methanogenic effect, and many are found to be naturally present and already grazed in Australian rangelands, predictions of ruminant emissions from Australian rangelands, and the value of our native plants, may need to be revisited and altered when more information becomes available.

Tropical forages (e.g. Leucaena) generally elicit moderate reductions in enteric CH₄ production, but have the potential to increase animal productivity by 20% and therefore significantly reduce CH₄ emission intensity, when compared with the standard practice of grazing Rhodes grass pastures (Harrison et al. 2015). Despite barriers due to high establishment costs, complex management, and issues with anti-nutritive factors and toxicity (Table 1), they have the advantage of providing good biomass and nutritive profiles (Taylor et al. 2016), resulting in moderate prospects for practical application.

Industry by-products are already valued as a feed supplement in Australia, and some of these also bring a desired reduction in CH₄ production (Table 1). However, the distribution and use of the by-products is limited to farms that are in relatively close proximity to the site of generation, resulting in a relatively low likelihood of adoption (Fig. 2). As a high-energy supplement, their most obvious application is intensive systems (feedlot) and high-performance animals (dairy cattle). Moreover, the anti-methanogenic effect is often non-specific and some of the by-products may have negative effects on the animal; so, further research is needed to find the optimal inclusion levels that balance these positive and negative effects. In this category, by-products of oil extraction processes or brewing industries have been reported to have some potential for practical application in intensive farming systems and have been shown to reduce CH₄ emission by 15–20% (Moate et al. 2011). Other by-products should be assessed further for their benefits and their potential to address feed shortages and contribute to agricultural waste management in Australia.

While we already have access to some of the imported commercial plant-based products, our products are yet to be developed, and are yet to be investigated for our conditions and systems. Also, we do not know how much they could realistically reduce CH₄ and what the cost of this strategy would be.

The outcomes from the research undertaken have moved us closer towards practical solutions to mitigating methane. While some strategies for enteric CH₄ mitigation in Australia exist, more are yet to be researched and established. Focusing on plant bioactivity is clearly an option worthy of further investigation and investment. Australia is well positioned to explore and exploit its own plant resources as a means of balancing out the environmental effects of its livestock. While doing so, it may also address some other issues, including animal productivity, farm profitability, animal health, the security of plant biodiversity and the management of organic waste. While there seems to be an enormous potential for Australian plants and PSC, most of the exciting candidates are yet to be investigated in detail in vivo and under commercial settings; so, their potential for commercialisation is not clear. Also, the long-term impacts on palatability, intake, performance, and the quality of animal products, need to be investigated. Moreover, they need to be carefully assessed with regards to seasonal availability, total CH₄ emission and to rule out any toxicity to the animals and humans needs. Balancing these issues will almost universally depend on finding optimal doses and delivery methods, and then developing and adopting plant-based mitigation strategies for whole-farm enterprises. Clearly, Australia must align with global efforts to find effective mitigation strategies, and start developing locally relevant approaches tailored to our animals, climate, national profile, capacities and needs.

Data sharing is not applicable as no new data were generated or analysed during this study.

Zoey Durmic was Associate Editors of Animal Production Science at the time of submission, but was blinded from the peer-review process for this paper.

This research did not receive any specific funding, but we have drawn on data that was generated through the projects funded through the Reducing Emissions from Livestock Research Program (Department of Agriculture, Fisheries and Forestry, Australia) and the National Livestock Methane Program (Meat and Livestock Australia).