The expanding global population, coupled with the escalating demand for food, is intensifying the pressure on food production systems(Reference Molotoks, Smith and Dawson1). Alarmingly, almost 12 % of the world’s population experiences food insecurity, leading to widespread nutrient deficiencies and severe health consequences such as anaemia and stunting(Reference Baspakova2). This widespread malnutrition poses significant health risks and creates a considerable economic burden on healthcare systems, with its severity varying across different regions(Reference Nugent, Levin and Hale3). In response to these pressing challenges, the One Health framework provides a holistic strategy that recognises the deep interconnections between human, animal, and environmental health, aiming to achieve a sustainable balance and long-term resilience(Reference Zinsstag, Kaiser-Grolimund and Heitz-Tokpa4). Within this approach, livestock plays a crucial and multifaceted role, not only as a source of nutrition but also in enhancing food security, supporting livelihoods and contributing to economic stability. By integrating livestock management with public health and environmental sustainability, the One Health framework fosters solutions that address global health risks while ensuring a more secure and equitable food system.
Ruminant meat and milk products are high in macro- and micronutrients, therefore providing a nutrient-dense food source for human consumption. Human nutritional impacts from ruminant production and consumption have been examined for years but have become even more important recently, given increasing demand driven by population growth, rise in affluent middle classes and environmental concerns(Reference Jebari, Pereyra-Goday and Kumar5–Reference van Oort, Daloz and Andrew8). While livestock production is recognised for its resource-intensive nature, it also plays a crucial role in the production of nutrient-rich foods, such as ruminant meat and dairy, which are important contributors to human health and well-being, as evidenced in most countries’ food-based dietary guidelines(Reference Beal, Gardner and Herrero9). However, while ruminant products are nutrient-dense food sources, overconsumption has been associated with increased dietary intake of SFA, which are documented to increase the risk of CVD, diabetes, and some cancers, such as colon cancer(Reference Kennedy, Alexander and Taillie10). Therefore, balancing their consumption within a diverse and nutrient-rich diet is essential to maximising their benefits while mitigating potential health risks. Likewise, while there is a need to ensure population dietary adequacy, this must be achieved while keeping within planetary boundaries, considering the contribution of ruminants to greenhouse gas (GHG) emissions. Indeed, ruminants are substantial contributors to methane (CH4) emissions globally, accounting for approx. 32 % of global anthropogenic CH4 emissions, 17 % of the global food system GHG emissions and 5 % of global GHG emissions(Reference Arndt, Hristov and Price11–Reference Ivanovich, Sun and Gordon13). Consequently, this review examines the challenges and opportunities of sustainable ruminant production systems through the lens of One Health principles. It examines the challenges related to (1) ruminant products and human health, (2) environmental concerns with a specific focus on methane and (3) the role of ruminants in the circular bioeconomy. Additionally, this review also explores the research and innovation landscape required for sustainable practices to support advances in sustainable ruminant production for the future.
Role of ruminants in human health
Red meat and dairy provide essential nutrients that support both population-level nutrition security and individual dietary needs(Reference Scollan, Price and Morgan14). Despite concerns about excessive intake of SFA found in ruminant products, ruminant products offer a valuable dietary source of macro- and micronutrients, including high biologically valuable protein, iron, zinc, iodine, B-complex vitamins, and polyunsaturated fatty acids (PUFAs) such as n-3 fatty acids(Reference Leroy, Abraini and Beal15,Reference Sheffield, Fiorotto and Davis16) . The nutritional composition of ruminant products varies based on factors such as species, animal diet, geographical location, cooking methods and processing techniques(Reference Scollan, Price and Morgan14,Reference Suleman, Wang and Aadil17) . Additionally, dietary requirements vary throughout the human life cycle. For example, early life stages will have different nutritional requirements relative to adults to maximise potential for optimal growth and repair of the skeleton, muscles, and organs. In later stages of life requirements for nutrients such as protein and calcium increase, which alongside a reduced energy intake requirement highlights the importance of nutrient density(Reference Dorrington, Fallaize and Hobbs18). Similarly, females of a reproductive age and those who are lactating have increased requirements, particularly for nutrients such as iron, vitamin B9 (folate) and magnesium(Reference Jouanne, Oddoux and Noël19,Reference Marshall, Abrams and Barbour20) . Therefore, responsible consumption of ruminant products can contribute to the intake of key nutrients for people at all life stages.
Meat
Globally, both per capita and absolute meat consumption have increased since the 1960s, driven by rapid economic development and rising household incomes(Reference Whitton, Bogueva and Marinova21). However, this trend has not been uniform across all geographical regions worldwide. Between 2008 and 2019, UK meat consumption per capita per day decreased by around 15 %. This shift was particularly evident in red meat consumption, which dropped by around 14 g per day, while white meat consumption showed an increase of approximately 3·2 g per day. Although UK meat consumption has declined over the past ∼15 years, 34 % of people are reported to consume above the Department of Health’s and World Cancer Research Fund’s recommendation to consume less than 70 g of red and processed meat per day(Reference Stewart, Piernas and Cook22). European countries consume the greatest amounts of animal products v. southeast Asia and Africa who consume lowest(Reference Henchion, Moloney and Hyland23).
Ruminant meat provides a rich source of high biological value protein, which is classified as ‘complete’ as it contains all the essential amino acids needed for maintenance requirements and muscle growth(Reference Williams24). In recent years, plant protein has increased in popularity due to perceived health benefits and reduced environmental impact(Reference Aschemann-Witzel, Gantriis and Fraga25). Nevertheless, many plant proteins are not considered ‘complete’ and require a greater dietary variety to ensure optimal amino acid intake(Reference Millward26,Reference Day, Cakebread and Loveday27) . Adequate consumption of high biological value protein is important for health and well-being and sub-optimal intake is associated with reduced skeletal muscle and impaired muscle function(Reference Williams24). In addition, ruminant meat such as beef and lamb are major contributors to dietary vitamin B12 intake (not synthesised by plants), which is essential for cognitive development and central nervous system function. Since vitamin B12 is found exclusively in animal-derived foods, such as meat, dairy and fish, individuals following plant-based diets rely on supplements or fortified foods to meet their requirements(Reference Niklewicz, Smith and Smith28). Similarly, ruminant meat is one of the richest sources of haem iron, which is essential for growth, development, and energy levels, with haem iron representing 95 % of functional iron in the body. While some plant-based products are fortified with non-haem iron, its bioavailability and absorption are lower than haem iron(Reference Hooda, Shah and Zhang29). This is an important factor to consider when evaluating iron intake from plant-based diets. Ruminant meat is a valuable source of fatty acids with SFA representing up to 50 % of total dietary fat(Reference Scollan, Price and Morgan14). Due to volume, meat is also recognised as an important source of n-3 PUFAs to human diets, however, levels vary considerably depending on animal diet. Optimal n-3 PUFA intake is associated with improved cognition, reduced severity of arthritis symptoms and reduced risk of non-communicable diseases such as CVD(Reference Scollan, Price and Morgan14,Reference Ponnampalam, Hopkins and Jacobs30–Reference Bassuk, Manson and Grp34) .
Dairy
Dairy products such as milk, yoghurt and cheeses derived from ruminants are also a valuable source of nutrients such as calcium, protein, vitamin D, phosphorus and iodine, in addition to being a key hydration tool due to high water content(Reference Scholz-Ahrens, Ahrens and Barth35,Reference Niero, Visentin and Censi36) . Adequate dairy consumption is positively associated with optimal bone density, with no reported effect on all-cause mortality(Reference Thorning, Raben and Tholstrup37). Dairy intake is particularly important for children and adults over 70 due to bone growth and structure development(Reference Geiker, Molgaard and Iuliano38,Reference Bristow, Bolland and Gamble39) . Dairy products also represent a valuable source of nutrients in developing countries where nutritional diversity is limited(Reference Dror and Allen40,Reference Grace, Wu and Havelaar41) .
Therefore, the consumption of ruminant products plays a crucial role in a balanced human diet providing a rich source of essential nutrients. However, it is important to promote responsible consumption, focusing on unprocessed, nutrient-dense options while being mindful of concern such as certain saturated and trans fatty acids. Additional dietary recommendations should align with One Health principles, considering environmental impacts, land use, water quality issues, climate factors and food distribution challenges.
Greenhouse gas challenges of ruminant production
Ruminants produce CH4 as a by-product of the fermentation of feedstuffs through the symbiotic relationship with the rumen microorganisms(Reference Piñeiro-Vázquez, Canul-Solís and Alayón-Gamboa42). The enteric production of CH4 results in a 6–12 % loss in feed energy and, consequently, production efficiency for the ruminant, while also contributing to global warming. Ruminant production is estimated to be responsible for 32 % of total global anthropogenic CH4 emissions, 17 % of the global food system GHG emissions, and 5 % of global GHG emissions due to the growth of livestock production for human consumption(Reference Arndt, Hristov and Price11). The GWP of CH4 over 100 years is quantified as approximately 27 and 30 times greater than that of CO2 (43), nonetheless its shelf life is short at approximately 12 years(Reference Lynch, Cain and Pierrehumbert44). Resultantly, the global mitigation targets in place for anthropogenic CH4 production are the most time sensitive of the GHGs, as reducing CH4 emissions will have the most immediate impact on slowing climate warming(45).
More notably for CH4 production and the ruminant sector, the 2015 Paris Agreement(46) set a maximum 1·5°C global warming target (above pre-industrial levels), with CH4 from ruminants having a reduction target of 11–30 % by 2030 and 24–47 % by 2050 compared to 2010 levels(Reference Arndt, Hristov and Price11). This has been reinforced by the creation of the Global Methane Pledge at COP26 in 2021 where currently 158 participating countries that represent over 50 % of global anthropogenic CH4 emissions are working towards a 30 % CH4 reduction from 2020 levels. This has resulted in country specific policies and individualised targets for CH4 reduction. For instance, Northern Ireland’s aims for 46 % reduction in CH4 by 2050 from 1990 levels(47), California has set a target of a 40 % reduction by 2030 compared to 2013 levels(48), while New Zealand aiming to reduce biogenic CH4 by 10 % below 2017 levels by 2030 and reducing net emissions by 50 % below gross 2005 levels(49). The predicted cumulative benefit of reducing global anthropogenic CH4 by up to 45 % by 2045 is projected to reduce global warming by 0·3°C(50).
Therefore, understanding how ruminants produce enteric CH4 is paramount in the development of reduction strategies. The rumen microbiome is the main influencer of enteric CH4 production levels in ruminants(Reference Henderson, Cox and Ganesh51). Essentially, dietary carbohydrates are broken down by the rumen microbes (Figure 1) and go through the biochemical process that results in the production of volatile fatty acids (VFAs), which serve as an energy source for the ruminant. This process results in the generation of hydrogen (H2), which is predominantly utilised by methanogenic archaea in the rumen to convert CO2 into CH4. The production of certain VFAs, such as propionate, utilises more H2 than others and can therefore help to redirect H2 away from CH4 production. Thus, the effect of diet on the rumen microbiome is likely to be the main influencer of CH4 emissions in ruminants(Reference Henderson, Cox and Ganesh51) via the downregulation of the methanogenic archaea community or by reducing substrate (H2) availability for methanogenesis(Reference Hook, Wright and McBride52).
Fig. 1. Ruminant gastrointestinal tract, illustrating the fermentative microbial ecosystem within the rumen compartment of the forestomach (created using BioRender).
Dietary interventions to reduce methane
Dietary interventions to manipulate the rumen microbiome activity to reduce enteric CH4 outputs can be broadly grouped into the following categories: plant-based strategies (e.g. forage management and feeding plants that are high in secondary bioactive compounds, such as tannins); targeted methanogenesis inhibitors (such as 3-NOP, which is commercially known as Bovaer®); oils and oilseeds (e.g. fish oil, algal oil, linseed oil, sunflower oil); and hydrogen sinks (e.g. either chemicals or microbes that utilise hydrogen so that there is less available for methanogenesis).
Plant and algae-based dietary interventions to reduce methane emissions from ruminants
Naturally occurring plants that contain bioactive compounds, such as tannins can be used as plant-based dietary interventions for ruminant feeding. One such example is the inclusion of multi-species and silvopastoral swards, which increase plant biodiversity and nitrogen fixation while improving quality(Reference Sharrow and Ismail53,Reference Poudel, Pent and Fike54) . These swards are also readily available and implementable, with no approval or registration required. Terrestrially found tannins consist of polyphenolic compounds with an affinity to bind to molecules including carbohydrates, polysaccharides, bacteria and enzymes, metal ions and proteins and can inhibit the activity of cellulolytic bacteria, subsequently the reducing their degradability(Reference Wang, Xu and Bach55,Reference Fagundes, Benetel and Welter56) . Tannin-containing plants (e.g. legumes) in ruminant feeding systems can reduce CH4 emissions by ∼18 % (g CH4/kg milk)(Reference Arndt, Hristov and Price11,Reference Enriquez-Hidalgo, Gilliland and Deighton57–Reference Beauchemin, Ungerfeld and Abdalla59) .
Brown seaweed species also contain phlorotannins, which are analogues to terrestrial tannins with a similar mode of action in terms of CH4 reduction(Reference Wang, Xu and Bach55). One such CH4 reducing brown seaweed is Ascophyllum nodosum, however trials involving feeding this species to ruminants in vivo have reported varying results, with reductions in CH4 emissions albeit small(Reference Bosnjakovic, Nedic and Arsic60–Reference Thorsteinsson, Weisbjerg and Lund62). Conversely, red seaweeds, including Asparagopsis taxiformis and A. armata, can induce reductions of enteric CH4 by up to 80 % in vivo (Reference Roque, Venegas and Kinley63). Bromoform, the bioactive halogenated compound found in these seaweeds, has been shown to inhibit methanogenesis(Reference Abbott, Aasen and Beauchemin64,Reference De Bhowmick and Hayes65) . Studies have demonstrated that delivering bromoform alone to ruminants can reduce CH4 emissions by 55·4 %(Reference George, Platts and Berry66). Additionally, a dose-dependent effect was observed, with CH4 yield reductions of 64 %, 98 %, and 99 % as the inclusion rate of Asparagopsis-derived bromoform increased from 17 to 51 mg per kg of DMI(Reference Cowley, Kinley and Mackenzie67).
Studies have also shown the benefits of feeding certain microalgae genera with respect to reducing CH4 emissions from ruminants, specifically those with high poly-unsaturated fatty acid (PUFA) contents. PUFA have been shown to have a toxic effect on the cellulolytic bacteria(Reference Nagaraja, Hobson and Stewart68) and protozoa(Reference Doreau and Ferlay69) leading to decreased CH4 production and a favourable shift towards propionate production(Reference Martin, Morgavi and Doreau70). The PUFA content of microalgae spp. ranges from 1–40 % DM(Reference Chacon-Lee and González-Mariño71,Reference Remize, Brunel and Silva72) . Gomaa et al.(Reference Gomaa, Kholif and Kholif73) investigated the CH4 reduction potential of Nannochloropsis and found that a supplementation of 5 % reduced CH4 production up to 23 % in vitro. The high PUFA content in microalgae are known to be beneficial to human health(Reference Díaz, Pérez and Sánchez74,Reference de Lima Valença, da Silva Sobrinho and Borghi75) . This illustrates the role that microalgae could play in terms of the ‘One Health’ framework by enhancing the human health characteristics of meat and milk products whilst minimising environmental impact and contributing to biodiversity and the circular bioeconomy.
Targeted CH4 inhibitors to reduce methane emissions from ruminants
The increased knowledge of the rumen microbiome and particularly methanogenesis has led to the development of chemically derived CH4 inhibitors with the most well studied being 3-nitrooxypropanol (3-NOP)(Reference Arndt, Hristov and Price11,Reference Beauchemin, Ungerfeld and Abdalla59,Reference Beauchemin, Ungerfeld and Eckard76) . In dairy cattle, 3-NOP has been reported to reduce enteric CH4 per unit of feed intake or milk production by 25–30 %(Reference Kebreab, Bannink and Pressman77). 3-NOP works through molecular docking at the methylcoenzyme M binding site, selectively interacting with the nickel enzyme methylcoenzyme M reductase, which facilitates the final step of CH4 – forming pathway in rumen archaea(Reference Duin, Wagner and Shima78,Reference van Gastelen, Burgers and Dijkstra79) . Van Gastelen et al.(Reference van Gastelen, Burgers and Dijkstra79) administered 3-NOP to dairy cattle throughout an entire lactation to evaluate its long-term effectiveness as a CH4 inhibitor. The CH4 mitigation potential was affected by the lactation stage and the dietary regimen. Reductions of 16 % of CH4 yield (g/kg DMI) were recorded for the dry and mid-lactation periods whereas 20 % and 26 % reductions were observed for the early and late-lactation periods. 3-NOP is deemed as a feed additive requiring regulatory approval to feed in many countries, thus discovery to implementation in a small number of dairy farms has taken over 10 years. It was first approved as a CH4 reducing feed additive in 2021 in Brazil and Chile and has since been approved in multiple geographies including Australia, the European Union, USA, Canada and UK.
Oils and oilseeds to reduce methane emissions from ruminants
Supplementary plant-derived lipids are often incorporated into dairy cow diets as a practical source of metabolisable energy (ME) that bypasses ruminal fermentation(Reference Klieml, Humphries and Kirton80). Lipids can impact CH4 production through providing alternative routes for hydrogen utilisation or by having direct toxic effects on cellulolytic microbes and thus fibre digestion, further shifting fermentation patterns towards propionate production(Reference Martin, Morgavi and Doreau70,Reference Vargas, Andrés and López-Ferreras81,Reference Villar, Hegarty and Nolan82) . However, adding oils to diets of ruminants with a total lipid level over 6 % (DM basis) may impact the ability of rumen microbes to degrade dietary fibre and protein, and consequently reduce feed intake and animal performance(Reference Patra83). A variety of plant-based lipids can be used in ruminant diets, with linseed and rapeseed oils being commonly used(Reference Halmemies-Beauchet-Filleau, Rinne and Lamminen84) and lipids can be included to levels of 5 % DM without causing adverse effects on ruminant health or production. The amount and type of lipid, particularly the fatty acid profile, significantly influences the CH4 production response(Reference Vargas, Andrés and López-Ferreras81). However, the observed CH4 reductions (∼20 %) in vivo may be partly attributed to a decrease in DMI resulting from the increased ME provision(Reference Bayat, Tapio and Vilkki85). Palangi et al.(Reference Palangi, Taghizadeh and Abachi86) concluded that oils and lipids might effectively be used, alone or in combination with other strategies for enteric CH4 mitigation.
Strategies for balancing metabolic hydrogen concentration to reduce methane emissions from ruminants
In the rumen, methane is the primary sink for metabolic hydrogen, produced as a byproduct of microbial fermentation(Reference Ungerfeld87). However, excessive CH4 emissions not only represent an energy loss for the animal but also contribute to environmental challenges. To address this, dietary interventions provide promising strategies for redirecting hydrogen away from the methanogenic pathway, both by reducing its production and by promoting its consumption through alternative pathways, such as propionate formation(Reference Ungerfeld87,Reference Wang, Xiong and Zhao88) . Chemical compounds like phloroglucinol and 3-NOP have shown potential in modulating microbial activity and redirecting hydrogen flux away from CH4 production(Reference Kebreab, Bannink and Pressman77,Reference Martinez-Fernandez, Denman and Cheung89–Reference Pitta, Indugu and Melgar92) . Additionally, DFM, often called probiotics, can enhance beneficial microbial populations that utilise hydrogen more efficiently, offering an alternative metabolic pathway that produces less CH4 (Reference Lan and Yang93).
Phloroglucinol, a naturally occurring phenolic compound, has been shown to influence hydrogen utilisation in the rumen. It is an intermediate metabolite formed during the microbial degradation in the rumen of flavonoids and other phenolic compounds in forage plants(Reference Martinez-Fernandez, Denman and Cheung89). Rumen bacteria can reduce phloroglucinol using hydrogen or formate as electron donors, yielding acetate as the terminal product(Reference Huang, Romero and Belanche94). This process provides a potential alternative sink for hydrogen, thus reducing the overall methane production in the rumen. The ability of phloroglucinol to support hydrogen capture in this manner may enhance microbial efficiency, particularly when methane production is inhibited through other means. A recent in vitro study by Huang et al.(Reference Huang, Romero and Belanche94) assessed the effects of phloroglucinol and found that it effectively reduced hydrogen accumulation while increasing the concentration of volatile fatty acids, particularly acetate. Moreover, the study revealed that phloroglucinol, in conjunction with methanogenesis inhibitors such as 2-bromoethanesulfonate (BES), exhibited a synergistic effect, further reducing methane production by and improving overall rumen fermentation.
In addition to chemical compounds, DFMs can also play a key role in hydrogen management(Reference Lan and Yang93,Reference Ban and Guan95) . Probiotics and other beneficial microbes introduced into the rumen can enhance microbial populations that utilise hydrogen more efficiently, either by increasing the production of SCFA or by supporting alternative fermentation pathways that produced less hydrogen as a byproduct, thereby reducing its availability for methanogenesis. For instance, Jeyanathan et al.(Reference Jeyanathan, Martin and Morgavi96) also screened 45 bacteria, including strains of LAB, Bifidobacteria and Propionibacteria, in vitro for their ability to reduce methanogenesis and then selected 3 strains for in vivo trials in sheep, with one strain, L. pentosus D31, resulting in a 13 % reduction in CH4 yield over four weeks following dosing with 6 × 1010 cfu/ animal/ day. However, studies feeding the bacterium Propionibacterium, which utilises lactate to produce propionate, when tested in vivo did not affect total VFA production or enteric methane production in beef heifers fed high-forage diets(Reference Vyas, McGeough and McGinn97) or finishing cattle fed high-concentrate diets(Reference Narvaez, Alazzeh and Wang98). These studies did not report a change in rumen propionate concentrations and hypothesised that this lack of change was caused by the moderate persistency of the strains and/or the pre-existing high level of propionate production from starch fermentation(Reference Vyas, McGeough and Mohammed99,Reference Vyas, Alazzeh and McGinn100) . Research on the topic has been limited, and much effort is now needed to develop DFMs. These beneficial microbes may not only help in reducing methane but can also improve overall rumen health and productivity by enhancing fermentation efficiency and promoting a more stable microbial ecosystem. These dietary interventions, whether through chemical compounds like phloroglucinol and 3-NOP or through the strategic use of DFMs, can effectively redirect hydrogen flow in the rumen, reducing methane emissions and improving the metabolic efficiency of ruminant livestock.
Breeding for ruminants with lower methane emissions
Whilst nutritional interventions can have the most immediate impact on CH4 output, genetic selection is an attractive solution to reduce enteric CH4 emissions due to its cumulative and permanent nature(Reference Lassen and Difford101). Correlations between animal phenotypes and CH4 emission output have been successfully identified, highlighting that animal genotypes and thus breeding programmes can be altered to actively select for low-emitting phenotypes(Reference de Haas, Pszczola and Soyeurt102). Residual methane emissions (RME) are defined as the gap between an animal’s observed CH4 output and the expected output based on its feed intake and body weight(Reference Bird-Gardiner, Arthur and Barchia103). Recently, RME has been promoted as an ideal trait for selecting cattle with lower CH4 emissions because it is phenotypically and genetically independent of productivity, yet it shows a strong correlation with daily methane emissions(Reference Bird-Gardiner, Arthur and Barchia103–Reference Smith, Kelly and Kenny107). Smith et al.(Reference Smith, Kelly and Kenny107) observed a comparable level of beef cattle productivity but a 30 % difference in CH4 output in cattle ranked low for RME. The investigation of the rumen microbiome of these animals highlighted potential microbial biomarkers of the methanogenic potential of beef cattle, identifying the abundance of bacterial genera associated with the synthesis of propionate via the acrylate pathway, as well as the methanogens Methanosphaera and members of the Methanobrevibacter RO clade(Reference Smith, Kelly and Kenny107). This supports earlier research by Kittelmann et al.(Reference Kittelmann, Pinares-Patiño and Seedorf108) who identified three ruminotype clusters (Q, S and H) in sheep. Low CH4-emitting sheep (ruminotypes Q and S) had a greater abundance of bacterial taxa associated with propionate production and a combination of lactate and succinate, respectively. Thus, selecting animals with low RME inherently favours a distinct rumen microbiome composition characterised by microbial taxa associated with reduced methanogenesis.
Ruminant diets and the circular bioeconomy
Ruminants play a key role in the circular bioeconomy by upcycling inedible agricultural by-products into nutritious food, using waste as feed, producing manure as fertiliser, and supporting ecosystem services(Reference Van Zanten, Van Ittersum and De Boer109). Additionally, specific feed ingredients can further minimise waste and reduce environmental impact. Indeed, the European Commission defines feed ingredients for circular bioeconomy: ‘where the value of products, materials and resources is maintained in the economy for as long as possible, and the generation of waste minimised’(110). Examples of feed ingredients for ruminants that may fall under this category include cellular agriculture products (e.g. bacterial proteins), alternative food sources including both macro- and microalgae, food waste, former foods and by products e.g. of brewing industry(Reference Pexas, Doherty and Kyriazakis111). A key priority of a system based upon circular bioeconomy principles is to prevent non-edible co- or by-products from becoming food waste.
Cellular agriculture and fermentation products
As noted, DFMs can mitigate rumen methanogenesis to various extents, but is should also be noted they are also a source of protein for the animal(Reference Jeyanathan, Martin and Morgavi96). The performance outcomes depend on factors such as the species and strains used, their format in which they are incorporated into feed (e.g. live culture or freeze-dried formats), the dosage included in the diet and the substrate forming the basis of the ration. As research continues to refine their efficacy and reliability, they have the potential to play a key role in improving animal performance, as well as reducing environmental impact, and enhancing the sustainability of livestock production systems.
Alternative algae-based dietary proteins as a renewable ruminant feed source
Algae including macroalgae (seaweed) and microalgae, have gained attention for their potential role in carbon sequestration and sustainable biomass production. Their cultivation exemplifies the circular economy providing renewable resources that minimise waste while delivering diverse environmental and social benefits. If macro and microalgae were broadly adopted in different sectors it would be a driving force to achieve circularity across feed/ food, energy, and material sectors. Firstly, the capacity of macro and microalgae to draw down carbon dioxide (CO2) and to fix it into organic matter, has been previously demonstrated(Reference Chung, Oak and Lee112,Reference Anyaoha, Krujatz and Hodgkinson113) . In addition to the natural process of sequestering carbon using macro and microalgae, the potential to cultivate harvest, and add them in the ocean is under investigation as well as growing them at scale away from the ocean. By sequestering carbon, micro and macroalgae can support carbon-offset initiatives, providing a renewable resource that helps reduce the carbon footprint(Reference Anyaoha, Krujatz and Hodgkinson113,Reference van den Burg, Koch and Poelman114) . Seaweeds accounted for 1·5 million tonnes of carbon sequestration each year. Additionally, commercial harvest seaweeds approximately 3·2 % of the carbon released to seawater yearly due to the emission of greenhouse gases(Reference Hossain, Sharifuzzaman and Nobi115). Conversely, by 2030, the global microalgae production would be expected to capture 171 000 tonnes of CO2 (0·171 Mt) annually. However, with the market expanding exponentially and scaling technologies being implemented, production densities are expected to increase, potentially enhancing carbon capture efficiency as a consequence(Reference de Souza, Meers and Mangini116). Additionally, the cultivation of micro and macroalgae also have positive biodiversity impacts through habitat formation and improves the fish populations(Reference Hasselström, Visch and Gröndahl117). Studies have shown that seaweed farms enhance the structural complexity of coastal habitats, drawing fish and fish larvae by providing them with shelter and feeding opportunities(Reference Underwood and Jeffs118).
There is a great variety of micro- and macroalgae-based products which have been developed and introduced to ruminant diets and alternative feedstocks. These feeding strategies promote environmental sustainability and offers a viable alternative to conventional feed ingredients (e.g. cereal grains, soybeans). This will reduce the competition among the food, feed, and biofuel industries as their cultivation requires fewer resources of freshwater and arable land(Reference Yong, Thien and Rupert119,Reference Jagtap, Meena, Jhariya, Meena, Banerjee and Meena120) . Protein production from alternative cultivation methods, such as micro and macroalgae may have close to zero requirements regarding land and water(Reference Parsons, Allen and Abeln121) and may require less fossil fuel inputs compared to conventional cereal and soya production, although this is currently disputed due to the high energy inputs for drying(Reference Koesling, Kvadsheim and Halfdanarson122). Such alternatives may also make minimal use of synthetic and chemical fertilisers, the production of and use of which accounts for up to 95 % of the environmental impact of conventional crop production.
Former foods
Contrary to assertions(Reference Pinotti, Luciano and Ottoboni123), inclusion of former foods seems to be of limited use as a feeding ingredient for ruminant diets. This is because former foods, including bakery by-products are usually high in energy sources, such as fats, sugars and starch, compared to conventional ingredients used in ruminant diets. These sources have the potential to affect rumen function (fermentation), including the potential for rumen acidosis. The interest of including such ingredients is mainly in high-yielding dairy cows(Reference Kaltenegger, Humer and Stauder124), aiming to increase their DM intake and affect milk yield. To the authors knowledge, Kaltenegger et al.(Reference Kaltenegger, Humer and Stauder124) is the only published study to suggest that inclusion of bakery byproducts in the diets of cows during mid-lactation decreased the risk of rumen acidosis, when included up to 30 % in the diet. The effects of inclusion of former foods in the ruminant diet on CH4 emissions, productivity and human health parameters of meat and milk still require investigation.
Future scoping research and innovations for sustainable ruminant production
Future ruminant productions systems will undoubtedly continue to focus on research and innovation in (1) Genetics and Breeding; (2) Animal nutrition and (3) Animal Health, to achieve food security and human health, whilst limiting environmental impact (Figure 2). Subsequent development of innovations will require several enablers, including investment, multi-actor partnerships, scaling, regulatory approval and importantly social acceptability. The rapid evolution of enabling or disruptive technologies, such as multi-omics, artificial intelligence, diagnostic tools etc. will also be critical to the speed of delivery of innovations to improve sustainable ruminant production. Below, we set out a framework and timelines whereby innovations are expected to be implemented, alongside current underlying investment, partnerships, and regulatory pathways, and their social acceptance (Figure 2). We also outline likely future enabling technologies, which will enhance our ability to improve ruminant production in a One Health framework.
Fig. 2. Scoping future research and innovation to support advances in sustainable ruminant production.
Ruminant genetics and breeding
Recent breeding advances have seen the introduction of sexed semen to enable farmers to have more control over the sex of calves, which will inevitably also reduce greenhouse gas emissions and food waste associated within the less profitable part of the herd(Reference Quelhas, Pinto-Pinho and Lopes125). Breeding for optimal production with regards to animal performance in addition to GHG output, nutrition and animal health has also been a focus in past few years(Reference Pulina, Francesconi and Stefanon126). Breeding programmes will see the exploitation of favourable genetics, such as reduced CH4 emissions in a reasonably short timeframe e.g. Irish Cattle Breeding Federation began a breeding programme approximately 5 years ago and have recently released estimated breeding values based on CH4 emissions of beef sires(127). Breeding goals are achieved using a combination of techniques such as genetic evaluation and selection, Artificial Insemination, appropriate storage and optimising longevity of genetic material. This is complimented by the use of advanced software for breeding goals, animal performance predictions and calculation of impact of breed strategy e.g. financial implications.
Animal nutrition
Dietary interventions will undoubtedly be fed increasingly in ruminant diets as they play a crucial role in ensuring ruminant production systems are sustainable(Reference Britten and Mahendran128). The likelihood that grazing systems will move substantially from monocultures systems to more mixed sward systems in the coming few years is high given the holistic benefits this may have, e.g. introducing legumes increases above and below-ground biodiversity, whilst increasing nitrogen fixation and improving soil quality(Reference Sharrow and Ismail53,Reference Poudel, Pent and Fike54) . Likewise, introduction of ‘the right tree’ in the ‘right place’ will also benefit ruminant production, whilst aiding nutrient-run off and ensuring enhanced water quality(Reference Bateman, Anderson and Argles129).
In addition, feed additives continue to be investigated primarily for mitigation strategies for improved environmental sustainability with enhanced productivity and product quality for human health being a significant added value, especially in terms of economic viability and enabling a unique selling point. Bovaer® is one of the most studied feed additives, with approval for use in many countries, and the next few years will undoubtedly see an increase in its application on-farm. Currently, it is being used by Arla in Denmark with the aim of implementation in the UK shortly. However, it should be noted that consumer concerns regarding the safety of drinking milk from cows fed Bovaer® have recently been expressed on social media. Whilst the data on Bovaer® from numerous countries shows no human health concerns as the product does not reach the milk, these concerns show the importance of social licence when moving from development to implementation. It should however be noted, that whilst safe to use, Bovaer® have few additional One Health benefits beyond reducing CH4.
Micro- and macroalgae also show great promise to reduce carbon footprint and improve feed efficiency as noted previously and as such is highly likely that we will see these being increasingly used in livestock diets; albeit they are at an earlier stage of development than Bovaer®(Reference Patel, Singhania and Awasthi130,Reference Ahmed, Elwakeel and El-Zarkouny131) . Nonetheless, scalability in an economically viable manner has been a challenge for the implementation of both micro and macroalgae. The tides are rapidly changing though, with many companies now upscaling production, for example, Corbion are now able to produce microalgae at scale(132). In terms of scalability of macroalgae production, numerous start-up companies are also exploring the cultivation possibilities of Asparagopsis spp. with Rumin8 (supported by $12 million investment from Bill Gates), Sea Forest, Volta GreenTech and Blue Ocean Barns being prominent. Other bolus technologies such as rumen bromoform boluses for grazing systems are being explored. The use of a rumen bolus allows the slow release of bromoform into the rumen to manipulate the microbial environment, and as previously mentioned reduce enteric methane production. However, bromoform is carcinogenic and studies that assess its safety regarding both animal and human health are paramount prior to adoption. Future of commercialisation and use of bromoform boluses coupled with other innovations on farm has the potential to significantly reduce CH4 emissions from cattle. However, it should be noted that once seaweeds are processed to extrude bromoform for dietary inclusion, it is labelled as an additive, which in many countries requires regulatory approval, which can often be time-consuming.
The application of DFM will also undoubtedly increase in the coming years. This is largely due to a new large strategic project (ACRONYM: RUMEN Gateway) which is funded by the Global Methane Hub(133), and the Foundation for Food and Agriculture Research Greener Growth Initiative(134). Combining the above nutritional strategies with the introduction of DFMs will also undoubtedly gain traction in the next few years, providing exciting opportunities to reduce methane by suppression of the methanogens as well as limiting their available of hydrogen and re-directing that hydrogen to produce VFAs and ultimately energy to the animal. Indeed, it has already been shown that supplementation of phloroglucinol with 3-NOP promotes the capture of excess hydrogen from methanogenesis and generates valuable metabolites for the host(Reference Martinez-Fernandez, Denman and Cheung89). Likewise, combining breeding strategies with innovative dietary interventions will also provide a potentially greater additive effect on ruminant production and environmental impact, resulting in enhanced sustainable ruminant production systems.
The development of anti-methanogen vaccines is also a pioneering avenue, which is currently being explored, and interest is growing, which is reflected in increased investment and funding, for example, the BEZOS Earth Fund(135). Methane vaccines triggering antibody production which target and inhibit methanogens in saliva(Reference Beauchemin, Ungerfeld and Eckard76). Although experiments have been conducted in the past, with varied success, the use of CH4 vaccines would be extremely beneficial in a pasture-based system(Reference Wedlock, Pedersen and Denis136,Reference Zhang, Huang and Xue137) . Future implementation will depend on consistency of results, effects on nutrition and productivity, monitoring of rumen adaptation and financial viability relative to the levels of reduction of enteric CH4.
Clearly the development, regulatory approval processes and underlying data requirements to label a product as being reduced in CH4 emissions during its production are complex and timely. In an attempt to provide clarity to aid the development of feed additives a recent series of publications driven by the Feed and Nutrition network underpinning the activities of the Global Methane Alliance have been published which outline requirements for in vitro testing protocols, in vivo study design, understanding their mode of action(Reference Belanche, Bannink and Dijkstra138), measuring CH4 outputs effectively at farm, national and supranational scales(Reference del Prado, Vibart and Bilotto139), modelling the effects of feed additives to inform local and national inventories, whilst outlining the importance of designing, conducting, and reporting scientific evaluations transparently, using validated standards and methods, and communicating with regulatory bodies to ensure compliance with regulations and evidence requirements(Reference Dijkstra, Bannink and Congio140–Reference Hristov, Bannink and Battelli142). This is a major undertaking and forms a solid foundation to expedite the future development, commercialisation and inventory accounting of feed additives with antimethanogenic properties.
Animal health
By definition, all livestock-associated emissions arise from production system inefficiency: any inputs, such as feed, not retained by the animal and its products, such as milk or meat, would lead to emissions, as they would be excreted into the environment, including as GHG emissions. System inefficiency also includes animals that die, are culled or whose products are condemned. The latter, ‘outputs’ can be seen as ‘waste’, in the sense they are not captured by the system and thus contribute to emissions. In addition, animal health has major consequences for how animals use their resources, including feed and water, and poor health will tend to increase inputs, including medication, and reduce outputs. For example, an animal challenged by a pathogen will have to divert some of its resources towards the damage caused by the pathogen and the mounting of the immune response, instead of towards production-related functions(Reference Sandberg, Emmans and Kyriazakis143).
Animal health improvements through the provision of interventions will also be an increasing, relatively easily implementable route to reduce ruminant GHG emissions, as such interventions are available here and now(Reference Kyriazakis, Arndt and Aubry144), e.g. biosecurity, vaccination, medication. Some of these interventions are consistent with dietary interventions, such as the provision of swards with phenolic compounds or supplements that have the potential to reduce digestive disorders, such as acidosis. In addition, emerging diagnostic and sensor technologies could also contribute more widely to the early detection and treatment of health issues, through, for example, the automated detection of behavioural changes associated with digestive disorders(Reference Matthews, Miller and Clapp145). In addition, novel technologies should enable extraction of relevant disease occurrence and animal, and system efficiency data from ruminant systems in a variety of conditions. All these technological advances would enable early intervention and thus enhance the likelihood of their success.
Enabling technologies
The next 15 years and beyond are also likely to see dramatic increases in the enabling technologies which will underpin the speed at which innovations can be developed. For example, wearable technologies enabling gaseous emission to be measured in a high-throughput manner are imminent, with substantial investment from the Global Methane hub underpinning the development of these technologies by the industrial partner, Zelp(Reference Hub146). This enhanced ability to measure methane in a high-throughput and cost-effective manner will undoubtedly speed up the process of genomic selection and breeding for low CH4 emitting ruminants, whilst also providing a transformative platform to measure the effects of animal nutrition and health measurements on CH4 emissions.
Likewise, ‘omic’ technologies allowing genotyping of ruminants and assessment of the rumen microbiome are becoming cheaper with higher throughput capacity. These ‘omics’ tools include metataxonomy, metatranscriptomics, metaproteomics and metabolomics amongst others(Reference Zhao, Tan and Fang147) and these allow mechanisms of action of dietary interventions to be understood and to also ensure that no detrimental effects can be seen on the rumen microbiome and its ability to ferment ingested feed.
The use of clustered regularly interspaced short palindromic repeats (CRISPR) for genome editing will also be a powerful tool for agriculture and ruminant livestock. Genetic improvement in plants using CRISPR will boost productivity, resilience, increase the supply of specific nutrients and see a reduction in chemical input during production(Reference Leahy, Kelly and Ronimus148,Reference Khan, Ali and Wu149) . From a ruminant perspective, multipurpose breeds will become more achievable using CRISPR and will allow selectivity of desirable traits, which can be used for breeding(Reference Menchaca150). Genes encoding for productivity traits can be selected for and therefore increases animal efficiency(Reference Lamas-Toranzo, Ramos-Ibeas and Pericuesta151). Animal welfare could also be improved, for example using CRISPR to breed polled cattle, reducing the common procedure of dehorning(Reference Schuster, Aldag and Frenzel152). Applications of CRISPR in ruminant production systems can also be beneficial to human health, for example, by producing dairy products without beta-lactoglobulin, which causes allergies and intolerances(Reference Zhao, Tan and Fang147,Reference Tara, Singh and Gautam153) . The science around CRISPR is continuing to evolve. Some of the challenges surrounding CRISPR in livestock production is cost, legality and ethical concerns(Reference Eriksson, Jonas and Rydhmer154). Bioethical impacts for the environment and biodiversity is another drawback of CRISPR technology. It is possible interspecies transfer of genes could occur which would pass a trait recognised as desirable in one species onto another species where the expression of the gene could be undesirable(Reference Ayanoglu, Elçin and Elçin155). In addition, while animal welfare may be improved, there are concerns that genome editing for certain productivity traits could lead to reduced welfare for individual populations as well as trans-generational. For example, selecting genes for increased muscle may cause health problems such as strain on organs, limbs and increase risk of dystocia(Reference Singh and Ali156). The ethical concerns surrounding CRISPR in livestock can be overcome with increased education and clear communication on product labels.
Artificial intelligence (AI) and machine learning (ML) methods are increasing integrated into the ruminant agriculture sector, harnessing the vast amounts of data already being collected to drive efficiency, sustainability, and animal welfare. The abundance of high-resolution time-series data, such as daily milk yields, feed intake records, and health monitoring metrics, provides a prime resource for training ML applications. These datasets enable the training of sophisticated models to identify patterns and make accurate predictions, enhancing decision-making processes in livestock management. The continuous monitoring of livestock behaviour through sensors and imaging technologies generates vast amounts of time-series data. ML models have successfully been applied to this data to recognise and interpret animal behaviours, enabling early detection of health issues and improving welfare management. A comprehensive review by Liakos et al.(Reference Liakos, Busato and Moshou157) highlights the transformative impact of ML in agriculture, emphasising its application in animal welfare and livestock management. The high temporal resolution of collected data allows ML models to capture subtle changes and trends over time, leading to more accurate predictions and preintervention. The integration of AI/ML in precision livestock farming will enable early disease detection and control, reducing the spread of infections and improving herd health management through predictive analytics. AI-driven genetic trait prediction will also enhance selective breeding programmes, optimising desirable traits such as disease resistance, milk yield, and feed efficiency and contribute to environmental sustainability by reducing methane emissions and resource wastage. As the volume and quality of agricultural data continue to grow, the application of AI and ML is positioned to direct significant advancements in ruminant agriculture. However, studies such as(Reference Hu and You158) have highlighted not only the benefits of integrating ML into the agriculture sector, but also the need to ensure the interpretability of the predictive models built. The risks associated with black-box models, those whose decision-making processes are not easily interpretable, especially when used to assess and guide climate change impact, must be carefully considered. While the vast amount of available data presents an invaluable resource for ML applications, potential pitfalls must be acknowledged and addressed. A common challenge arises from the differing priorities of domain scientists and ML engineers, which can result in predictive models that fail to fully meet the needs of either group. To maximise the effectiveness of ML in agriculture, clear and ongoing communication between scientists, engineers, and farmers is essential, ensuring that models are both scientifically robust and practically useful. Moreover, the training and use of ML models currently requires large infrastructure and electricity, which is at odds with the aims of ensuring food security while balancing economic and ecological sustainability within the One Health framework.
Conclusions
While ruminant products offer vital nutrients for human health and contribute to the circular bioeconomy, their environmental impacts, particularly CH4 emissions, pose significant challenges. While much of the current literature is centred on mitigating CH4 emissions alone, fewer studies have embraced a holistic ‘One Health’ framework that includes not only aiming to achieve CH4 reduction while enhancing animal health, productivity and human health attributes of the resultant ruminant products, which recognises the interconnectedness of human, animal, and environmental health. Enhancing sustainable ruminant production within the ‘One Health’ framework will require research and innovations to increasingly focus on (1) Genetics and Breeding; (2) Animal Nutrition and (3) Animal Health. In terms of nutritional approaches with multiple one-health benefits, mixed grazing and silvopastoral systems offer much potential, as does the use micro and macroalgae and DFMs. The use of microalgae also has further benefits in terms of enhancing the human health attributes of ruminant products through enrichment with n-3 fatty acids. Micro- and macroalgae, and DFMs also contribute to the circular bioeconomy, thus increasing their attractiveness for further development for on-farm use. Together with enhanced ruminant genetics and breeding, these precision nutrition approaches could also have a substantial advantage, with the merger of these research areas being transformative and imminent in the next few years. Expedited timeliness of delivery of all innovations will also require use of rapidly evolving enabling technologies and data innovation, for example use of AI. Subsequent implementation of resultant innovations within the agri-food sector will also require several enablers, including large-scale investment, multi-actor partnerships, scaling, regulatory approval and importantly social licence. This One Health approach will be critical for developing holistic sustainable livestock production systems that benefit both animal and human health, while also contributing to environmental sustainability.
Acknowledgements
We thank the Nutrition Society for the opportunity to publish this review.
Authorship
S.A.H. and L.S.P. coordinated and led on the writing of this review and all other authors contributed to sections and to the editing.
Financial support
The authors gratefully acknowledge funding from European Union (H2020-SFS-2018-1 project MASTER-818368; (Facilitating Innovations for Resilient Livestock Farming Systems-Re-Livestock-10159609) and Devenish Nutrition. We also acknowledge funding from FACCE JPI (Project Acronym: SeaSolutions) and the Department for Agriculture, Environment, and Rural Affairs for the underpinning funding.
Conflict of interest
There are no conflicts of interest to raise.
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