AGRONOMIC AND ENVIRONMENTAL BENEFITS OF REINTRODUCING HERB- AND LEGUME-RICH MULTISPECIES LEYS INTO ARABLE ROTATIONS: A REVIEW

Emily C. COOLEDGE, David R. CHADWICK, Lydia M. J. SMITH, Jonathan R. LEAKE, Davey L. JONES

Front. Agr. Sci. Eng. ›› 2022, Vol. 9 ›› Issue (2) : 245-271.

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Front. Agr. Sci. Eng. ›› 2022, Vol. 9 ›› Issue (2) : 245-271. DOI: 10.15302/J-FASE-2021439
REVIEW
REVIEW

AGRONOMIC AND ENVIRONMENTAL BENEFITS OF REINTRODUCING HERB- AND LEGUME-RICH MULTISPECIES LEYS INTO ARABLE ROTATIONS: A REVIEW

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Highlights

● Arable-ley rotations can alleviate soil degradation and erosion.

● Multispecies leys can improve livestock health and reduce greenhouse gas emissions.

● Ley botanical composition is crucial for determining benefits.

● Lack of livestock infrastructure in arable areas may prevent arable-ley uptake.

● Long-term (10–25 years) research is needed to facilitate evidence-based decisions.

Abstract

Agricultural intensification and the subsequent decline of mixed farming systems has led to an increase in continuous cropping with only a few fallow or break years, undermining global soil health. Arable-ley rotations incorporating temporary pastures (leys) lasting 1–4 years may alleviate soil degradation by building soil fertility and improving soil structure. However, the majority of previous research on arable-ley rotations has utilized either grass or grass-clover leys within ungrazed systems. Multispecies leys, containing a mix of grasses, legumes, and herbs, are rapidly gaining popularity due to their promotion in agri-environment schemes and potential to deliver greater ecosystem services than conventional grass or grass-clover leys. Livestock grazing in arable-ley rotations may increase the economic resilience of these systems, despite limited research of the effects of multispecies leys on ruminant health and greenhouse gas emissions. This review aims to evaluate previous research on multispecies leys, highlighting areas for future research and the potential benefits and disbenefits on soil quality and livestock productivity. The botanical composition of multispecies leys is crucial, as legumes, deep rooted perennial plants (e.g., Onobrychis viciifolia and Cichorium intybus) and herbs (e.g., Plantago lanceolata) can increase soil carbon, improve soil structure, reduce nitrogen fertilizer requirements, and promote the recovery of soil fauna (e.g., earthworms) in degraded arable soils while delivering additional environmental benefits (e.g., biological nitrification inhibition and enteric methane reduction). Multispecies leys have the potential to deliver biologically driven regenerative agriculture, but more long-term research is needed to underpin evidence-based policy and farmer guidance.

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Keywords

bioactive forages / integrated crop-livestock systems / nitrogen cycling / plant secondary metabolites / soil carbon / soil quality

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Emily C. COOLEDGE, David R. CHADWICK, Lydia M. J. SMITH, Jonathan R. LEAKE, Davey L. JONES. AGRONOMIC AND ENVIRONMENTAL BENEFITS OF REINTRODUCING HERB- AND LEGUME-RICH MULTISPECIES LEYS INTO ARABLE ROTATIONS: A REVIEW. Front. Agr. Sci. Eng., 2022, 9(2): 245‒271 https://doi.org/10.15302/J-FASE-2021439

1 INTRODUCTION

With the global population expected to reach 10.9 billion by 2100, sustainable agricultural intensification is required to increase food production by 48.6% to meet the projected demand[1,2]. However, current agricultural practices are unsustainable and have contributed to a global decline in soil quality, risking future crop and livestock production, especially with intensifying climate change[3]. Reliance on agrochemicals and mineral fertilizers to increase productivity has led to increases in greenhouse gas (GHG) emissions[4,5], pest and herbicide resistance[6,7], loss of biodiversity[8], and soil degradation[9,10].
Soil degradation is widely recognized as a key threat to soils and the ecosystem services they provide[11]. Due to their slow rate of formation, ca. 0.3–1.4 t·ha−1·yr−1 for Europe, soils are regarded as a non-renewable resource that need careful protection and management to preserve them for future use[12]. Soils can provide multiple ecosystem services, such as carbon sequestration, food and fiber production, disease control, water quality management, and flood and climate regulation[11,13]. Arable land management and cultivation practices, for example, deep tillage and removal of crop residue, can contribute to progressive soil degradation through damage to soil structure, loss of soil organic matter (SOM), increased compaction and an increased risk of erosion, especially in hilly regions. Poor soil structure also leads to more diffuse pollution; especially excessive nitrogen and increasingly phosphate leaching[9]. Although it is difficult to accurately quantify the full economic impact of the loss of ecosystem services, soil degradation has a significant impact on the global economy. The 2006 Thematic Soil Strategy for the EU estimated the annual cost of soil degradation to be 38 billion EUR for the EU25 member states, with soil erosion and loss of soil organic matter costing 0.7–14.0 billion and 3.4–5.6 billion EUR·yr−1, respectively[14]. In a wider perspective, the global economic cost of land degradation has been estimated at 231 billion USD·yr−1, equivalent to ~0.41% of the global GDP[15].
Technological advancements in farm machinery, introduction of high-yielding crop varieties, increased consumer demand and affluence, and government policies, subsidies and grants have improved farm efficiency and productivity per unit of labor but inadvertently accelerated the degradation of agricultural soils in many European nations[16]. This has encouraged agricultural intensification and specialization, leading to the decline of mixed farming and the infrastructure to support this. Consequently, there has been an increase in monoculture farming and continuous cropping with no fallow or break years, which formerly involved rotations with grazed grass-clover leys, and subsequently decreasing the heterogeneity of the landscape and creating regional areas of soil degradation and environmental pollution[17,18]. In the UK, for example, increases in specialization were initiated in 1947 by the introduction of the Agriculture Act following World War II to improve self-sufficiency[17]. This resulted in a decline in mixed farming and a progressive geographical separation of land use with livestock-grazed grasslands becoming dominant in the wetter west of the country and arable farming becoming dominant in the drier east of the country[16,19].
In many regions of the world, integrated crop-livestock systems, also referred to as mixed farming systems, have been reintroduced to promote more climate-resilient, sustainable and economically viable agricultural systems, compared to specialized and intensive systems[20]. However, coupled crop-livestock farming systems maintain on-farm specialization but utilize neighboring farms to manage system inputs effectively (e.g., muck-for-straw deals), integrated crop-livestock systems utilize systems more efficiently and can produce higher economic returns than coupled crop-livestock farms[21]. Integrated crop-livestock systems employ arable-ley rotations to alleviate soil degradation, improve soil quality for future use, build soil fertility via symbiotic nitrogen fixation in legumes, and increase resilience by diversifying the farm enterprise[22,23]. Incorporating leys, temporary grasslands lasting up to 5 years, and integrating livestock into arable rotations can help to better manage arable weeds, pests, improve soil structure, enhance nitrogen fixation and recycle nutrients from livestock excreta back into the soil[24]. However, the effect of integrated crop-livestock systems on soil quality and productivity can vary significantly depending on grazing management regime, soil type and ley species sown, for example, perennial ryegrass, grass-legume, or a multispecies mix containing grasses, herbs and legumes[2527]. Ryegrass-based leys are often used due to their wide tolerance of different conditions, versatility of use for silage, hay, haylage and grazing, and high digestibility for livestock[28], however, ryegrass monocultures provide limited ecosystem service benefits[29,30]. By comparison, grass-legume leys have the benefit of reducing the need for mineral N fertilizers in the subsequent crop due to their N fixing abilities[31]. It should be noted, however, that plowing in leys in preparation for the following crop can lead to increased N leaching into watercourses and thus indirect GHG emissions[32]. Based on the study of natural ecosystems, however, it is clear that resilience and ecosystem delivery increases with plant diversity[33]. Pasture management for increased plant species diversity, however, is not simply a case of mixing and planting as many forage species as possible. It is clear that the kinds and amounts of different forage species along with their arrangement within and among pastures at the farm scale are critical features that must be considered[34].
Although research often focuses on the effect of multispecies leys (also known as herbal leys) on livestock health and productivity[35], grass yield[27] and GHG emissions[36], there is currently limited information available on the combined effects of these leys on restoring soil quality in degraded arable soils over and above simple mixtures of two to three species. This review focuses on the potential benefits and implications of reintroducing multispecies leys and livestock grazing in arable rotations for (1) ecosystem services, (2) soil structure, (3) soil carbon and nitrogen cycling, (4) livestock GHG emissions, (5) livestock productivity, and (6) sustainable agriculture. Finally, we highlight areas that require further research.

2 REINTRODUCING LEYS INTO ARABLE ROTATIONS

2.1 Ecosystem services delivered by leys

Policy, land use and management regime heavily influence the ecosystem services that modern agriculture can provide. The decline in mixed farming, and subsequently the intensification of arable agriculture, has contributed to the generation of an unbalanced agroecosystem and the poor delivery of some ecosystem services. Such services are split into four core categories; provisioning (e.g., food and fiber production), regulating (e.g., climate and flood regulation), cultural (e.g., heritage and recreation), and supporting (e.g., nutrient cycling and biodiversity)[37]. The drive to increase provisioning services to meet consumer demand often comes at the cost of long-term regulating, supporting and cultural services[38]. Disservices, for example, eutrophication from excessive nutrient use or species loss from agrochemical use, caused by intensive agriculture are not always experienced just at the local scale but can apply at a range of spatial scales impacting the wider ecosystem[39]. These disservices are often described as trade-offs, where certain regulating or supporting services are reduced as a result of maintaining or increasing current food, fiber and bioenergy production[39].
Although some agri-environment schemes (AES) encourage the use of amelioration measures to reduce disservices from agriculture, for example, promoting extensification or introduction of buffer strips, they have attracted criticism for increasing production pressure elsewhere to account for a reduction in provisioning services[40,41]. In the UK, for example, the Higher Level Stewardship scheme in England, and the Tir Gofal and Glastir agri-environment schemes in Wales, promoted conversion of arable land to species-rich permanent pastures as an extensification measure[42,43]. However, it is important to discriminate between the aims of restoring and establishing species-rich permanent pastures compared to the desired ecosystem services of establishing multispecies leys. Species-rich permanent pastures, such as described in the GS6 and GS7 scheme in England, aim to restore, maintain and protect important habitats such as lowland meadows and rush pastures[44,45]. In contrast, schemes promoting the introduction of multispecies leys in arable rotations (e.g., GS4 scheme in England) aim to restore soil quality and provide new habitats (e.g., for pollinators and soil invertebrates)[42]. However, as with other AES, farmer willingness and the voluntary nature of schemes is recognized as a key limitation to uptake[46]. Further, assessment of the benefits of these schemes indicated that they provided little tangible improvement in key indicators such as biodiversity, carbon storage, greenhouse gas reduction, and water quality[46,47]. Alternative strategies are therefore needed to promote current and future AES, particularly those that can be adopted at the landscape scale. In Ireland, an ongoing Results-Based Environment Agri Pilot Programme (REAP) is testing a results-based payment system to reward farmers for maintaining or improving their farm environment[48]. Payments within this 2-year trial scheme are dependent on the results of an environmental scorecard, assessing ecological integrity (e.g., species richness), field margins (e.g., width) and the field boundary (e.g., hedgerow condition and density)[48]. Farmers that establish multispecies leys within their grassland system can receive payments up to 275 EUR·ha−1 if achieving the maximum scorecard result[48]. However, currently REAP does not include tilled fields or multispecies leys sown within a crop rotation[48]. This may be an avenue that future AES explore to encourage uptake of multispecies leys to deliver multiple ecosystem services at a landscape level.
Although the establishment of species-rich pastures encourages improvements in biodiversity, it often fails to account for the persistent effects of previous intensive management on soil properties[37,49]. This can limit the potential ecosystem services that the conversion of arable land to multispecies leys can offer. Incorporating leys and livestock into arable rotations offers the potential to increase provisioning services and ameliorate the disservices created by intensive arable agriculture. These potential services and disservices are illustrated in Fig.1.
Fig.1 Comparison of the ecosystem services and disservices produced by arable farming, livestock farming and arable-ley rotations.

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In Sweden, a system including a one-year grass ley in rotation did not encounter disservices between provisioning services and supporting or regulating soil services from the agroecosystem, but instead maximized the delivery of soil-focused ecosystem services[50]. Under the zero N fertilizer regime, the grass ley system produced a greater yield than the conventional continuous commodity crop system, which produced the least ecosystem services delivery overall[50]. If a multispecies ley is introduced into cropping systems, it may provide a greater abundance of ecosystem services than a basic grass ley through increased resilience and complementarity of species[41,51,52]. This was demonstrated in a 3-year, 31-site study across Europe where a four-species mixture consisting of two grasses and two legumes consistently outperformed the respective monoculture comparison of each plant species[53]. This was attributed to the synergistic interactions between the plant types delivering transgressive overyielding and a greater resistance to weed invasion in the multispecies mixture than in the grass monoculture[53]. During the 3-year study, only 4% of the total yield was weed biomass in the multispecies ley whereas the weed biomass of the monoculture mixtures increased from 15% to 32% over 3 years[53]. The beneficial yield effects were also highlighted in Switzerland, where a temporary 3-year four-species mixture consisting of two grasses and two legumes receiving 50 kg·ha−1 N delivered multifunctional ecosystem services at the same level as grass or legume monocultures receiving 450 kg·ha−1 N[54]. The greater delivery of ecosystem services such as N cycling, forage quality and production in the four-species mixture at a low N rate was mainly attributed to the symbiotic nitrogen fixation in legumes[54]. Similar findings were reported in Ireland under rainfed conditions, where the annual yield of a 2-year six-species mixture receiving 150 kg·ha−1 N outperformed the 2-year perennial ryegrass (Lolium perenne) monoculture receiving 300 kg·ha−1 N by 1.3 t·ha−1[55].
In addition to the inclusion of nitrogen fixation from legumes in multispecies leys, attributes such as deep rooting of plant species including cocksfoot (Dactylis glomerata), Festulolium, chicory (Cichorium intybus), lucerne (Medicago sativa), sainfoin (Onobrychis), and sweet clover (Melilotus officinalis) can increase regulating and supporting services such as C storage, nitrogen fixation, soil structure and biodiversity[5659]. The deep rooting capabilities of these species enable access to water in deeper soil horizons to increase herbage production during dry periods compared to ryegrass leys, thus improving provisioning services[50,60]. The benefits of species diversity under drought conditions were shown in Ireland by Grange et al.[55], where a 2-year six-species mixture receiving 150 kg·ha−1 N under drought conditions produced a similar yield (10.7 t·ha−1) to a rainfed 2-year perennial ryegrass monoculture receiving 300 kg·ha−1 N (10.5 t·ha−1). The deep rooting capabilities of multispecies leys may also recover both macro- and micronutrients from depth which would have otherwise been lost. Although leys can be used for silage, hay or haylage production, grazing livestock on multispecies leys may increase farm productivity to address the economic gap that removing land from cultivation can cause. The supporting and regulating services that grazed multispecies leys in arable rotations can provide is explored in detail in the following sections. Although there has been extensive research into the delivery of ecosystem services in species-rich permanent grasslands, there is a lack of research into the ecosystem services delivered by temporary multispecies leys introduced to degraded arable land. Further research is needed to evaluate the potential benefits and disservices delivered by multispecies leys, with an emphasis on how these services can be maintained in the following crop.

3 IMPACT OF REINTRODUCING LEYS ON SOIL QUALITY

3.1 Soil quality under cropping systems

Application of agrochemicals for crop protection, use of mineral fertilizers, tillage regime, high temperature and increased rainfall intensity are all factors that contribute to the loss of soil structure and soil fertility[10,61,62]. Tillage is frequently used in arable agriculture to provide an effective seedbed, aid the decomposition of plant residues, and reduce crop pests, pathogens and weeds[63]. However, continuous cultivation and intensive tillage practices such as moldboard plowing and harrowing frequently deplete SOC through enhanced oxidation, and also damage the soil crumb structure; reducing the macroporosity and contributing to greater compaction and erosion, which drive further soil degradation[911]. The increased use of heavy farm machinery and the decline of mixed farming systems has increased reliance on mineral fertilizer inputs to maximize yield. The intensification of growing crop species that deliver only small amounts of organic matter that is stabilized in the soil has contributed to long-term depletion of SOM from arable soils, undermining soil stability that cannot be alleviated by normal tillage alone[64]. Fine-textured arable soils with reduced SOM content are vulnerable to structural collapse when wet, and especially under compaction and prone to losses from water and wind erosion[10]. Soils with poor aggregate stability suffer from increased susceptibility to water erosion that can lead to on-site and off-site environmental and economic impacts, such as reduced water holding capacity, loss of valuable nutrients such as N, P and K, reduced water quality, eutrophication, increased flood risk, and erosion leading to the siltation of watercourses and estuaries[62]. Under current practices, it is estimated 112 Mha (12%) of European land area is under threat from water erosion, with a further 42 Mha affected by wind erosion[14].
Maintaining a healthy soil structure is crucial in arable agriculture, as soil structure determines seedling establishment and root development, and thus nutrient use efficiency and yield[62]. Tillage disrupts key biological processes responsible for soil structure formation and crop productivity. Arbuscular mycorrhizal fungal (AMF) hyphae, polysaccharides produced by microbial communities and mucilage excreted in earthworm casts act as an adhesive between soil particles and humus, forming micro- and macroaggregates and increasing soil stability and macropores that control infiltration rates[65,66]. However, tillage can alter the composition and distribution of microbial communities in the soil profile, reduce earthworm populations and disrupt AMF hyphal networks, reducing their symbiotic ability to increase crop P uptake[63,6769]. The effects of tillage on earthworms is seen immediately after compaction events, where earthworm populations experience a 70% decline in total biomass due to animal death from crushing and lateral escape of the remaining population[69]. Effects of compaction on soil porosity can be seen for up to 2 years after the initial compaction event[69]. This has consequences for the restoration of soil structure and porosity of arable soils, as earthworm burrows aid the mechanical working of the soil and create interconnected macro- transmission pores and channels that allow plant roots rapid access to nutrients at depth and influence water and air infiltration[70,71]. Additionally, reduced soil porosity and inadequate drainage from compaction can create anaerobic conditions ideal for denitrifying bacteria, also favoring increased nitrous oxide (N2O) production[72].
Although some farmers attempt to ameliorate compaction and remove the plow pan through subsoiling, also referred to as deep tillage or subsoil ripping, this is fuel and labor intensive and creates a new soil structure inferior to that of uncompacted soil under grassland or reduced tillage management[73]. Numerous studies and intergovernmental bodies have recognized the damaging impact excessive tillage has for soil degradation and encourage the adoption of alternative tillage methods, for example, minimum tillage (min-till) and no-tillage (no-till), to alleviate environmental issues[74]. However, adoption of no-till methods remain slow in some areas due to concerns about soil compaction, reduction in pathogen inoculum, pest control (e.g., slugs), and perceived losses of crop productivity from herbicide resistant arable weeds, for example, black-grass (Alopecurus myosuroides), which would be buried deeper in the soil under an intensive tillage system reducing germination[75,76]. Repeated herbicide and pesticide applications to control arable weeds and pests in no-till systems have contributed to a greater increase in herbicide resistant weeds, and herbicide and pesticide runoff into watercourses than multi-pass tillage systems[77,78]. In the UK, common herbicide resistant weeds such as black-grass, wild oats (Avena spp.), Italian ryegrass (Lolium multiflorum), common poppy (Papaver rhoeas), common chickweed (Stellaria media), scentless mayweed (Tripleurospermum inodorum) and sterile brome (Bromus sterilis) threaten crop yield and farm productivity in arable systems[78,79]. Development of herbicide resistant weeds, and recently the discovery of glyphosate-resistant Italian ryegrass[80] and sterile brome[79], has resulted in some no-till farmers returning to more intensive tillage[81]. This has increased pressure to develop alternative pest management regimes for no-till systems. Incorporating leys and livestock, such as sheep and goats, into no-till and min-till systems can provide biocontrol for arable weeds, preventing seed set and thereby depleting seed banks over consecutive years, and pests without sacrificing the ecosystem services and improved soil structure of no-till[82].

3.2 Improving soil quality using arable-ley rotations

Integrated crop-livestock systems have long utilized cover-crops, leys and livestock in arable rotations to ameliorate soil degradation without excessive chemical and mechanical inputs[21]. Due to their ease of establishment and diversity of use, grass or grass-clover leys are used to improve arable soil structure, increase soil fertility, improve yield, and disrupt pest and pathogen life cycles[8385]. Most commonly, these leys are used for conservation, grazing or forage (e.g., hay or silage) production and are plowed into the topsoil after 1–4 years of use, losing some of the newly developed soil structure and accumulated SOC, and leaving soil and soil nutrients vulnerable to losses[86]. Despite requiring increased herbicide inputs to remove competition from unwanted plant species, no-till management can help to preserve the improved soil structure and biological activity post-ley[87].
Improvement of arable soil quality under ley is dependent on several key factors: ley duration, botanical composition, soil type, grazing density of livestock and agronomic management[86]. It can take between 5 and 10 years for coarse sandy soils under an ungrazed grass ley to return to permanent pasture conditions and to up to 50 years for clay soils[88]. Perennial ryegrass leys lack deep rooting capabilities, limiting their potential to bioturbate the soil and remove subsoil compaction. Perennial legumes and herbs, for example, chicory and lucerne, with deep primary roots (i.e., taproots) in the ley can influence soil microbial community composition, nutrient cycling, and increase soil porosity and infiltration through the generation of large pores (> 2 mm diameter) in the subsoil[25,89,90]. Perennial plant taproots generate large continuous pores from the topsoil to the subsoil through root compression of soil particles and mucilage excretion from the root tip. Once decayed, this produces large pores, encouraging earthworm activity and root growth for the following crop and offering opportunities for subsoil C deposition and storage[89,91,92]. However, it should be noted that short-term leys (< 3 years) may be insufficient to realize the synergies between deep rooted crops and deep burrowing earthworms[89].
Inclusion of legumes in the ley composition can have persistent effects on soil, often observed to affect the following crop[84]. Legumes can further encourage additional symbiotic relationships between N fixing bacteria in their root nodules and AMF, which enhances P sequestration in return for nitrogen fixation and plant assimilated C[93,94]. This can increase the abundance of AMF hyphae and improve aggregate stability of arable soils under ley, encouraging an improvement in soil structure[95]. Unlike arable soils where the AMF network is regularly disrupted by frequent tillage, leys allow AMF to establish a new permanent network that can be preserved by no-till management during the establishment of the following crop[87,93]. In Argentina, arable soils under a temporary grass-clover ley experienced a rapid restoration of soil properties (i.e., SOC and microbial biomass N) to original values within 3−4 years[96]. Similarly, in New Zealand, microaggregates (< 0.25 mm) in arable soil under a temporary grass or grass-clover ley became highly water-stable macroaggregates (> 1 mm) after 5 years, attributed to the enmeshing of soil particles by grass roots and AMF hyphae[95]. Introduction of leys into arable rotations allows the development of a denser root system that encourages increases in microbial biomass, earthworm and mesofauna activity, and subsequently the production of binding agents (e.g., mucilage and exopolysaccharides) which enable soil aggregate stability[82].
Increases in earthworm populations in soils under leys can accelerate the restoration of degraded arable soils[97]. Recovery of earthworm populations is relatively quick and increases with the duration of the ley[89,98]. Leys encourage the restoration of earthworm populations by no-till management for the duration of the ley, increased C inputs from roots compared to an arable crop, and increased humus and detritus from ley litter, providing food and habitat[65,75]. Under herb and grass leys, populations of the anecic earthworm Lumbricus terrestris in degraded soils in Germany experienced a rapid increase over 1−2 years, but did not increase further when the duration of ley cropping was extended to 2−3 years[89]. Prendergast-Miller et al.[98] corroborate this; earthworm recovery and abundance in a degraded arable soil in England was found to improve under a 2-year grass-clover ley (732 ± 244 earthworms m−2) and this was four times higher than the arable control (185 ± 132 earthworms m−2) which could potentially exceed the permanent grassland earthworm populations (619 ± 355 earthworms m−2·yr−1) in field margin soils. Similarly, within a 6-year arable-ley rotation, earthworm biomass under a 3-year simple grass ley reached 187 g·m−2 compared to 62 g·m−2 and 30 g·m−2 under temporary and permanent arable crop, respectively[99]. This was estimated as an increase of 40−45 g·m−2·yr−1 under ley, indicating that within 4−5 years the earthworm biomass could reach that of a permanent grassland, although sometimes this recovery can happen sooner[99]. Earthworms are crucial engineers of soil structure, improving soil porosity through burrows, reducing bulk density, increasing SOM and redistributing AMF spores and mycelium through grazing[93,100]. Similarly, within 1 year of establishment of a grass-clover ley, Hallam et al.[97] reported a decrease in soil bulk density of 6% and an increase in SOM by 9% due to increased earthworm populations.
Although the influence of livestock on soil quality has been well explored in pasture systems (e.g., Abdalla et al.[101], Stavi et al.[102]), there is relatively limited information available for the influence of grazed leys on soil structure and key biological indicators of soil quality when incorporated into arable rotations, for example, microbial and fungal community composition or earthworm activity. This is important as arable soils depleted of SOM may be structurally weak, so could be less resilient to the effects of poaching and trampling by livestock when soils are moist. Studies on arable-ley rotations instead focus on soil C and N cycling of ungrazed or cattle grazed leys, discussed in detail in the next section; with limited attention given to the role of sheep grazed leys on soil structure in comparison to those grazed by cattle. The previously discussed studies in this section detailing the influence of ungrazed leys on earthworms, AMF and aggregate stability fail to consider the potential of compaction and excreta returns from grazing livestock. Inclusion of livestock on leys can stimulate increases in earthworm population, soil macrofauna (e.g., dung beetles), microbial and fungal biomass, and above- and below-ground plant biomass, but risk increased topsoil compaction[71,103].
Partial improvements in soil physical properties have been observed in cattle-grazed integrated crop-livestock systems within the first annual crop cycle after the overwinter ley or cover crop has been reverted back to arable[104]. Integrated crop-livestock systems typically utilize winter cover-crop grazing by cattle in arable rotations to provide green manure to the soil, control arable weeds and stimulate bioturbation of the soil[83,105,106]. These winter cover-crops are often plowed into the soil in spring to prepare for the following crop. However, cattle-grazed integrated crop-livestock systems often suffer from increased topsoil (0−5 cm) compaction from livestock trampling of the already weakened arable soil structure[104]. Static pressure exerted from sheep and cattle hooves averages 66 and 138 kPa, respectively, whereas nominal tire pressures of farm machinery range from 74 to 81 kPa[107]. This can collapse macropores in the soil surface, reduce soil porosity and hydraulic connectivity, thus reducing water infiltration and promoting surface runoff and flooding[71]. Soils with high moisture content are vulnerable to collapse and deformation under livestock trampling, leading to soil poaching and erosion[107,108]. Farmers reintroducing livestock into arable rotations need to avoid overstocking and grazing livestock on weakly structured and fine-textured soils, especially when saturated, to preserve soil structure. An increase in compaction and penetration resistance can have persistent effects on the following crop, reducing root growth and thus yield[71]. It has therefore been suggested that preference when grazing should be given to sheep over cattle due to lower static pressures and smaller hoof sizes. In an integrated crop-livestock system in New Zealand, Laurenson and Houlbrooke[108] found that the soil bulk density under sheep grazing of overwinter forage crops was 1.26 Mg·m−3 (0–5 cm) compared to 1.35 Mg·m−3 (0–5 cm) for cattle grazing.
In arable-ley rotations, sheep grazing of a 3–4-year grass-clover ley resulted in increased bulk density in the 0–35 cm layer, reduced air permeability and macropore continuity compared to ungrazed undersown oats[109]. However, since grass-clover leys have a particularly dense root system, macroporosity (pores > 100 µm) was greater in the 0–10 cm layer than in the undersown oats[109]. Conversely, Riley et al.[92] examined soil physical properties within a 15-year mixed dairy-arable field trial under different grazing intensities and management (e.g., organic vs conventional, and different durations of grass-clover ley) on a loam soil in Norway. They found that soil bulk density increased by 0.14 Mg·m−3 for the continuous arable, but in the cattle-grazed grass-clover ley undersown with cereals in a 4-year rotation, bulk density decreased by 0.03 Mg·m−3 for a 2-year ley in a standard dairy production rotation and by 0.02 Mg·m−3 for an organic rotation with a 3-year ley. This was a relatively small reduction in bulk density for both systems with a ley, but may be attributed to post-ley reversion (e.g., plowing) and duration of ley within the 15-year trial. Similar findings were also found for soil porosity and aggregate stability of cattle grazed leys. Soil porosity within continuous arable rotations decreased by 4.3%, but increased by 1.4% for the conventional dairy system with a 2-year ley in rotation and by 0.2% in the organic dairy system with a 3-year ley in rotation[92]. Notably, continuous arable soils under reduced tillage management had the same aggregate stability as the rotation with a 3-year ley, highlighting the importance of preserving aggregate stability through reduced tillage and reduced compaction[92,109].
Currently, there are no reported studies that have compared continuous arable cultivation with mown, cattle or sheep grazed leys in rotation under the same soil type, sown botanical composition or different tillage management regimes. However, maintaining the same botanical composition under different sward management in future research may be difficult due to differences in grazing pressure and selective grazing between sheep and cattle; this may impact the persistence of certain plant species in the mixture and thus affect subsequent ley species composition. The influence of both sheep grazing, and in particular, complex multispecies leys, on soil structure and associated biological functions requires further research to critically evaluate the potential benefits and disbenefits sheep grazed arable-ley rotations can provide.

4 CARBON AND NITROGEN CYCLING IN ARABLE-LEY ROTATIONS

4.1 Changes in microbial communities

Arable-ley rotations can alter the microbial community composition, biomass, and activity of agricultural soils and the subsequent cycling of C and N[110]. Soil temperature, soil properties (e.g., pH), climate, botanical composition of the ley, nutrient and cultivation management can influence the soil microbial community and conversely C sequestration of arable soils[99,110112]. Formation of SOC stocks is regulated by the decomposition of SOM and root exudates by Gram-positive and Gram-negative bacteria and saprotrophic fungi[113]. However, microbial communities responsible for the decomposition of SOC in arable soils are sensitive to temperature changes. With global temperature increases projected to exceed 2 °C under different climate scenarios, this could affect the breakdown of SOC stocks and undermine efforts for C sequestration[114]. Microbial carbon use efficiency (CUE) determines the allocation of C for biomass growth, respiration (CO2 emissions), and ultimately necromass[115]. In a study by Bölscher et al.[115], sensitivity of CUE to increases in temperature reduced SOC stocks in Swedish grassland soils by 0.1–0.18 kg·m−2 C, 4% of their current stocks. Unlike grassland, forest or ley farming soils, microbial CUE in continuously cropped soils was not sensitive to temperature changes between 5−20 °C[115].
Although there has been extensive research on the effects of grassland[116,117] or arable farming[118] on soil microbial communities and functioning, there have been few attempts to measure this in arable-ley rotations[119]. Limited studies, however, have revealed that ley farming can increase the soil microbial biomass[50,120]. Long-term research on a sandy loam soil in a temperate climate at the Rothamsted Woburn Arable-Ley field trial in England also found that microbial biomass C and N pool was significantly larger in the arable-ley soil (964 kg·ha−1 C and 122 kg·ha−1 N) than the continuous arable control (518 kg·ha−1 C and 92 kg·ha−1 N) following an 8-year fertilized grass ley[112]. Under different conditions, results from a 25-year arable-ley cropping system experiment in Norway on a silty-sand loam soil in a humid continental climate indicated that there was no increase in microbial species richness or diversity, despite increasing microbial biomass[121]. The leys in both these studies used either grass or grass-clover leys, with low species diversity. Inclusion of herbal plants, such as plantain (Plantago lanceolata) or caraway (Carum carvi), into grass-clover mixtures were found to increase the ratio of fungi to bacteria but decrease Gram-positive bacteria, indicating a faster growing and more active microbial community[25]. However, as far as it known, there have been no studies on microbial community composition, biomass or diversity within multispecies leys under field conditions.

4.2 Carbon sequestration using arable leys

The 4-per-mille initiative aims to increase global SOM content by 0.4% per year to compensate for increases in atmospheric GHG emissions[122]. In particular, the initiative has promoted arable-ley rotations to increase global SOC stocks. In the UK, uptake of arable-ley rotations is projected to increase UK net SOC stocks by 1.6 t·ha−1·yr−1 C, with England in particular accumulating 0.20 t·ha−1 C annually in the 0–23 cm layer[122,123]. However, the 4-per-mille initiative has attracted criticism as being impractical and uneconomical in practice for land managers[124]. This largely depends on the payments system and AES employed on-farm, as under certain schemes, such as the Environmental Land Management scheme in England, this may become economically viable[125]. The use of arable-ley rotations to increase SOC is highly dependent on soil conditions and management; the limited evidence from long-term replicated trials and measurements of SOC post-ley conversion back to arable requires SOC results to be interpreted with caution. In addition, most studies have focused on a single ley rotation, rather than repeated cycles of multispecies leys and arable cropping. Tab.1 presents changes in SOC content reported from previous global field trials utilizing arable-ley rotations; studies relying solely on modeling changes in SOC were not considered.
Tab.1 Changes in soil organic carbon (SOC) content in arable-ley rotations, adapted from Schut et al.[21]
Publication Country Average annual rainfall (mm) Soil type Arable-ley rotation Ley composition Ley management Soil depth measured (cm) Annual C input to soil Change in SOC Comments
Börjesson et al.[126] Sweden 569 (Lönnstorp), 558 (Lanna) Loam (Lönnstorp), clay (Lanna) 4-year rotation: 3 years ley, 1-year cereal crop Grass-clover (meadow fescue, timothy, and red clover) Mown with biomass removed. Four N fertilizer treatments: 0, 50, 100, and 150 kg·ha−1·yr−1 N 0–20 1.7–2.5 t·ha−1 C in leys, 0.25– 1 t·ha−1 C in cereals + 0.28 (– N) + 0.35 (+ N) t·ha−1 C at Lönnstorp.+ 0.07 (– N) and + 0.17 (+ N) t·ha−1 C at Lanna No significant effect of N fertilizer on SOC stocks in the ley rotations
Johnston et al.[22] UK 640 Sandy loam Alternating rotation lengths followed by 8-year ley rotation. All leys followed by 2-year arable crop Grass or grass-clover (ley composition not given) Grazed by sheep or mown with biomass removed 0–25 n.d. + 0.01 t·ha−1 C for 3-year grass ley. + 0.16 t·ha−1 C for 3-year grass-clover ley. + 0.36 t·ha−1 C for 8-year grass ley. + 0.28 t·ha−1 C for 8-year grass-clover ley Long-term field trial started in 1938. Changes in SOC data are measured from 1965−1974 to 2000–2009
Krauss et al.[127] Switzerland 1303 (2012), 1112 (2013), 966 (2014) Calcareous clay 6-year rotation: 2-year ley, 4-year arable crop Grass-clover (ley composition not given) Mown with biomass removed. Cattle slurry applied after each cut 0–50 n.d. + 8.1 t·ha−1 C for arable-ley soils under reduced tillage and manure application compared to conventional tillage Increased stratification in soils under no-till management with manure applications, with highest SOC content in the surface soil. SOC did not increase in lower layers
Albizua et al.[50] Sweden 655 Sandy loam, sandy clay loam, and coarse-loamy soil 4-year rotation: 1-year ley, 3-year crop Grass (ley composition not given) Mineral N fertilizer addition: 0– 150 kg·ha−1 N. 20– 30 t·ha−1 of manure applied following wheat harvest at the end of the 4th year in rotation 0–20 n.d. + 0.39% SOC in 0 kg·ha−1 N ley system + 0.1% SOC in 150 kg·ha−1 N ley system Leys in rotation with additional mineral N fertilizer inputs results in positive effect on SOC content
Chan et al.[128] Australia 544 Clay loam 3- or 6-year rotation: see paper for more details Grass-legume (reed canary grass, cocksfoot, lucerne, and subterranean clover) or grass-clover (annual ryegrass and subterranean clover) Grazed by sheep or mown with biomass removed 0–30 n.d. + 500–700 kg·ha−1·yr−1 C Long-term field trials ranging 13–25 years. Increased SOC stocks following ley are quickly depleted by tillage and crop residue management
Bolinder et al.[129] Sweden 567 (Offer), 490 (Ås), and 566 (Röbäcksdalen) Silty clay loam 6-year rotation: 1–5 years of ley and arable crop Grass-clover (meadow fescue, timothy, and red clover) Ungrazed. Manure applied to ley in autumn (20 t·ha−1) 0–25 n.d. + 12 g·m−2·yr−1 C for rotation A (5 years ley, 1-year crop) 60-year field-trial of leys in organic dairy cropping systems
Chirinda et al.[130] Denmark 704 Sandy loam 4-year rotation: 1-year ley, 3-year arable with catch crops undersown in the barley crop Grass-clover (white clover and perennial ryegrass or red clover and perennial ryegrass) Mown with biomass removed. Anaerobically digested pig slurry used as N fertilizer 0–30 3.95 ± 0.06 t·ha−1 C between 1997 and 2007 −1 g·kg−1 C between 1996 and 2008 10-year field trial. Increased C inputs resulted in increased microbial activity but not C storage
Christensen et al.[86] Denmark 862 Sandy loam 6-year rotation: 1−6-year ley in rotation with barley undersown with grass Grass (perennial ryegrass, meadow fescue, timothy, smooth meadow grass) Mown with biomass removed. 225 kg·ha-1·yr−1 N of mineral fertilizer applied. 75 kg·ha−1 N after the first and 50 kg·ha−1 N second cut 0–20 n.d. + 1100 kg·ha−1·yr−1 C in soils under ley Lack of residual effect highlights need for legumes in the ley composition
van Eekeren et al.[99] Germany n.d. Sandy loam 6-year rotation: 3-year grass-clover ley, 3-years arable crop Grass-clover (perennial ryegrass and white clover) Grazed by dairy heifers from 1966 to 1989. Mineral N fertilizer: either 0 or 354 kg·ha−1·yr−1 N 0–10 n.d. + 7.5 g SOC kg−1 dry soil Long-term field trial established in 1966 (* SOC content of permanent arable minus average SOC of temporary grassland and temporary arable)
Studdert et al.[96] Argentina 870 Loam 7-year rotation: 2-year or 4−5-year ley with respective crops in rotation Grass-legume (cocksfoot, bulbous canary grass, tall fescue, perennial ryegrass, white clover and alfalfa) Mown with biomass removed 0–15 n.d. Returned to original SOC content 3−4 years under ley (37.2 g SOC per kg) Long-term field trial established in 1976−1993
Clement and Williams[131] UK n.d. n.d. 4-year ley Grass-clover (see paper for details) Grazed and mown for hay, with the post-mown ley grazed 0–15 n.d. + 0.23% SOC for grazed ley. + 0.17% SOC for cut and then grazed ley Increases in SOC was limited to 2–3 cm of the topsoil

Note: n.d., not determined; SOC, soil organic carbon; +, increases in SOC; –, decreases in SOC; and +N or –N with or without mineral N fertilizer.Plant species scientific names: Bulbous canary-grass (Phalaris aquatica), cocksfoot (Dactylis glomerata), lucerne or alfalfa (Medicago sativa), meadow fescue (Festuca pratensis), meadow grass (Poa annua), red clover (Trifolium pratense), reed canary grass (Phalaris arundinacea), ryegrass (Lolium perenne), subterranean clover (Trifolium subterraneum), timothy (Phleum pratense), white clover (Trifolium repens).

The information summarized in Tab.1 highlights the lack of homogeneity in reporting changes in SOC in arable-ley rotations in the literature. These studies report SOC content to different depths, different units (e.g., weight vs volume basis), and often without reporting the annual C input from the ley in rotation. Further, the lack of bulk density information prevents changes being expressed on a land area basis. Where livestock are used, such as in Clement and Williams[131], van Eekeren et al.[99], Chan et al.[128] and Johnston et al.[22], the authors did not estimate nutrient recycling from grazing livestock to allow comparison between studies.
Studies on arable-ley rotations (Tab.1) have mainly utilized grass or grass-clover leys, with limited attention given to multispecies leys with deep rooted plants that can provide other desirable traits (e.g., pollinator potential and biological nitrification inhibitor production). Botanical composition of the leys is crucial, as inclusion of legumes in grass-clover mixtures provide greater SOC increases than grass-only leys[86,132]. Diverse multispecies leys can sequester more C than simple grass or grass-clover leys due to the greater root mass and rooting depth. In New Zealand, diverse swards including herbs such as chicory, plantain and lucerne increased root mass by 5.32–9.35 t·ha−1 compared to 3.81–5.70 t·ha−1 root mass of a ryegrass-clover pasture, thus increasing C inputs into the topsoil (0−30 cm) by 1.20 t·ha−1·yr−1 C[56]. In comparison, annual soil C inputs from wheat (Triticum aestivum) roots were estimated to be only 0.40 t·ha−1·yr−1 C[133]. Although topsoil SOC is recognized as the most important functionally, the grass only and grass-legume leys listed in Tab.1 were reported to suffer from C stratification and limited subsoil SOC increases, attributed to the shallower root depths in common grass-clover leys[127,131].
Management of leys is also an important factor in C sequestration. Unsurprisingly, SOC content in the topsoil increased with the duration of the ley and the proportion of pasture in the crop rotation[128]. Grazed leys were found to sequester more C than mowing and removal of biomass as livestock return about a quarter of the OM they consume to the soil increasing SOM content[86,131]. Livestock excreta inputs and trampling of OM (e.g., plant litter and fecal matter) into the topsoil can increase SOC content by 0.23% compared to 0.17% for mown swards[131]. This was also seen in Johnston et al.[22], where SOC content within a 28-year sheep grazed ley rotation increased by 0.33 t·ha−1·yr−1 SOC, equivalent to an increase of 0.9% per year, exceeding the 0.4% increase encouraged by the 4-per-mille initiative.
The Highfield arable-ley experiment established in 1949 at Rothamsted Research Harpenden, UK, revealed that conversion of grassland to arable decreased SOC stocks by 30%, whereas arable to grassland conversion only increased SOC stocks by 8%[134]. These changes progressively slowed and tended toward new equilibria, indicating that rates of SOC loss and gain are greatest in the early years of management change. Evidence from long-term field trials, such as those held at Rothamsted Research, provides a warning that SOC content of soils under arable-ley rotations will eventually reach a new equilibrium or quasi-equilibrium where the total SOC will not change but the proportion of SOC in each pool will shift[22]. Once the new equilibrium is reached, tillage practices such as subsoil ripping may be useful to mix C rich topsoil with the subsoil as a form of occasional tillage where mixing from soil biota and fauna (e.g., earthworms) is not sufficient, allowing for C burial in the subsoil and establishment of a new equilibrium. Concerns over economic losses from the uptake of arable-ley rotations can be mitigated by utilizing livestock on the ley[135]. However, this would require significant changes in policy, governance and stewardship schemes to encourage arable farmers to diversify their enterprise or engage with partnerships at a community level and establish grazing agreements with livestock farmers.

4.3 Biological N fixation and nitrification inhibitors

In most arable agriculture, mineral N fertilizers have largely replaced the use of legumes for increasing N content of soils[136]. However, restrictions on fertilizer usage to constrain water and air pollution, consumer demand for organically grown produce, and increases in mineral fertilizer costs has returned attention to legumes in cropping rotations[136]. The symbiotic relationship between legumes and rhizobacteria (such as Rhizobium or Bradyrhizobium) within root nodules allows for atmospheric N2 fixation in return for plant generated carbohydrates[59]. This can also encourage the growth of grasses, leading to greater SOC inputs. For a 16-species diverse plant species mix, soil C and N increased by 70 ± 9 g·m−2·yr−1 C and 3.5 ± 0.53 g·m−2·yr−1 N, respectively, compared to monocultures of the same species (14 ± 10 g·m−2·yr−1 C and 0.59 ± 0.57 g·m−2·yr−1 N)[137]. Due to their N fixing abilities, legumes in leys can be used as a partial or full replacement for mineral fertilizers. Depending on abiotic conditions in the year of establishment, grass-clover leys plowed into the arable rotation saved 50%–83% or 77%–92% of fertilizer N typically applied during the arable phase of the rotation[31]. However, while grass-clover leys can reduce mineral fertilizer N inputs, plowing risks N leaching and subsequent eutrophication and nitrate (NO3) pollution of watercourses[61], as well as release of the potent greenhouse gas N2O. Under min-till management, these N losses may be greatly reduced.
Nitrification inhibitors (NIs) are used in agriculture to improve nitrogen use efficiency (NUE) by inhibiting the bacterial oxidation of ammonium (NH4+) to NO3, thus reducing N losses through leaching, runoff and denitrification[138]. Synthetic NIs such as DMPP (3,4-dimethylpyrazole phosphate) and DCD (dicyandiamide) are often used, however, these have varying levels of effectiveness and risk leaching into the environment and the contamination of water sources[139,140], and in the case of DCD, potential contamination of the food-chain[141]. Effectiveness of NIs is highly dependent on soil properties (e.g., pH and texture), crop type (e.g., cereals vs forage crops) and management factors (e.g., N fertilizer rate, and irrigation vs rainfed crops)[142]. When applied to cattle urine, DCD was effective at reducing N2O emissions by 70% but not NO3 leaching or ammonia (NH3) emissions[143] whereas DMPP was ineffective at reducing N2O emissions from cattle and sheep urine patches[143,144].
Naturally occurring NIs, or biological nitrification inhibitors (BNIs), are excreted from root exudates by herbs such as plantain to inhibit nitrification in the surrounding soil in N limited environments[145]. Plantain contains high levels of plant secondary metabolites such as aucubin, acteoside and catapol that act as BNIs of enzymes and nitrifying bacteria responsible for nitrification, Nitrosomonas and Nitrobacter[146148]. A laboratory incubation study by Dietz et al.[146] reported that the addition of plantain leaves resulted in reduced soil NO3 content for the 56 days in incubation. However, these plant secondary metabolites vary with growing season and climate. Aucubin concentrations in plantain increased from 3.8 to 6.9 mg·g−1 DM in the first and second growing season[149]. This can have implications for its efficacy as a BNI and the potential effect on NUE and N partitioning in livestock. Livestock grazing leys containing plantain can excrete plant secondary metabolites such as aucubin into the soil in urine, suppressing microbial activity within the urine patch[147]. The effect of plant secondary metabolites on livestock is explored in detail in the following section.

4.4 Enteric CH4 emissions

Ruminants, such as cattle and sheep, represent significant sources of CH4 emissions in livestock production. In 2017, cattle and sheep in the UK produced 16.8 and 4.0 Mt CO2e of CH4 by enteric fermentation[150]. CH4 is a powerful GHG, with a lifetime of 12.4 years and 100-year global warming potential (GWP) 28–36 times that of CO2[151] and a 20-year GWP 86 times that of CO2[152]. Recent revisions to GWP calculations have led to the development of GWP*, which accurately accounts for the reduced radiative forcing of short-lived climate pollutants such as CH4 compared to long-lived climate pollutants such as N2O and CO2[153]. GWP* is currently used to increase the modeling accuracy assessing mitigation measures to reduce the future impacts of ruminant production, helping countries identify feasible methods to achieve the coveted Net Zero C emissions[152]. In ruminants, CH4 production can vary with diet, animal, rumen microbiome composition and health. Currently, the IPCC default tier 1 emission factor estimates enteric fermentation emissions from sheep in developed countries as 8 kg CH4 per head per year and requires refining[154].
The use of plant secondary metabolites for enteric CH4 mitigation in ruminants has been extensively reviewed in the literature[155158]. Key herbs used in multispecies leys such as chicory, plantain, sainfoin and birdsfoot trefoil (Lotus corniculatus) contain plant secondary metabolites such as tannins, saponins and essential oils that can moderate the microbial production of CH4 in the rumen[159]. Saponins can suppress dihydrogen producing rumen protozoa, essential for the production of CH4[160]. Similarly, condensed or hydrolyzable tannins can reduce CH4 production by preventing fiber degradation in the rumen by complexing with proteins that are released for degradation in the low pH of the abomasum[158,161]. Addition of tannins and saponins as a feed supplement, however, should be used with caution, as hydrolyzable tannins and saponins in the rumen can be toxic to the host animal as well as to methanogens[157,160,162].
Naturally occurring tannins in chicory and sainfoin vary in concentration according to genotype, season, and management. Consequently, making measurements of tannin content within the forage is crucial for studies when investigating changes in rumen CH4 production. Addition of tanniniferous crop species to ensiled or dried forages (e.g., hay) has recently been found to decrease CH4 emissions[163]. In contrast, tannin addition to beef cattle fed a basal diet of lucerne and barley (Hordeum vulgare) silage reduced rumen ammonia concentration but not daily CH4 production[162]. Similarly, no differences in daily CH4 emissions were found for cattle fed sainfoin and birdsfoot trefoil hay[164]. This was attributed to the drying of plants inactivating the bioactive tannins in the forage[164]. However, enteric CH4 emissions were reduced from sheep fed either ensiled mixes of timothy (Phleum pratense) with either sainfoin (29.7 g CH4 kg−1 DM intake) or red clover (Trifolium pratense) (30.5 g CH4 kg−1 DM intake) containing high levels of condensed tannins and polyphenol oxidase respectively, compared to pure ensiled timothy (35.7 g CH4 kg−1 DM intake)[165]. In fresh forage, no differences in daily CH4 production was observed in sheep fed fresh chicory or ryegrass, with 24.1 and 21.4 g CH4 kg−1 DM, respectively[166]. For sheep fed ryegrass or a multispecies mix containing clover and herbs (herb composition was unspecified), CH4 production was lower in the multispecies mix (16.1 g·d−1 ryegrass vs 12.9 g·d−1 multispecies)[167].
The variable reports in the literature of plant secondary metabolites reducing CH4 emissions within livestock systems indicates that much more work needs to be undertaken to explore the complex relationships between diet and CH4 production. The effect of grazing ruminants on multispecies leys with herbs containing plant secondary metabolites is relatively understudied but is thought to affect other aspects of the ruminant, such as N excretion and parasite burden[168]. This indicates that a single focus on CH4 and live weight gain also needs to be coupled with studies of other aspects of rumen functioning.

4.5 Urine-patch N2O emissions

Increasing the available grazing area in the UK by reintroducing grazed leys into arable rotations risks increasing livestock N2O emissions. As ruminants are relatively inefficient at N assimilation, only 5%–10% of the N consumed is utilized in meat, milk and wool production, with the remainder excreted in urine and dung[169]. Urine deposited to pasture contains 70%–75% and 45%–60% of N excreted by sheep and cattle, respectively, and represent significant sources of livestock N2O emissions[170]. N2O is a potent GHG, with a GWP 298 times that of CO2 that requires careful monitoring[171]. Between 1961 and 2014, 54% of global annual N2O emissions from grasslands were attributed to livestock excreta deposits, with only 13% and 7% attributed to manure N and mineral N respectively[172]. Urine in particular contains readily available C and N that produce hotspots of N2O emissions within the grazing pasture, whereas dung contains more insoluble forms of N thus is more inert and slower to breakdown into N2O[171,173,174].
Sheep urine composition and N content is heavily dependent on diet and animal health, and ranges from 1.2 to 13.0 g·L−1 N[175]. 25%–90% of N in urine consists of urea, followed by purine derivatives and non-urea compounds: hippuric acid, allantoin, creatine, creatinine, uric acid, xanthine and hypoxanthine as well as any plant secondary metabolites such as the aucubin derivative aucubigenin[169,176178]. Diet manipulation, for example, by introducing plants with particular secondary metabolites into the pasture, can have a diuretic effect, reducing the proportion of urea in the urine and increasing the content of less labile non-urea compounds[178]. This has potential for use in swards containing high clover content to increase productivity and milk production, but exceeds the animal’s requirement for N resulting in increased N excretion to pasture[176]. Plant secondary metabolites, such as tannins, can also increase the proportion of N in dung, which is less vulnerable to N2O and NH3 losses than urine[173,179]. However, the effect of plant secondary metabolite containing plants in temperate multispecies leys on ruminant urine composition and subsequent N2O emissions is relatively understudied. A recent meta-analysis found that the relationship between animal diet and urine composition were under-reported in the literature[170]. Currently, the literature available for urine-patch N2O emissions, and subsequent emission factors, is dominated by grass or grass-clover pastures with almost no information available for multispecies leys.
In 2019, the IPCC announced the refinement of the 2006 Guidelines for National Greenhouse Gas Inventories, including refinements for the N2O emission factor for livestock urine and dung on pasture, range and paddock (EF3PRP) for sheep and cattle[180]. This reduced the 2006 EF3PRP from 1% to 0.3% of the N applied to the soil in urine and dung emitted as N2O[154,180]. There are currently no studies used by the IPCC to refine the EF3PRP that use emissions reported from grazed herbs such as chicory. Although some studies did not report sward composition[181183], calculations were made from predominantly grass swards[184192], grass-clover[144,186,193198] or forage crops (e.g., barley, lucerne, or brassicas such as rape, Brassica napus, or kale, Brassica oleracea var. sabellica)[186,194,199]. Currently, no estimates of direct livestock excreta N2O emissions from grazed multispecies pastures or leys are included in the IPCC calculations.
Although diet can alter the ratio of N in urine and dung, key soil properties such as pH, moisture, porosity, temperature, texture and microbial activity can affect N cycling in the urine patch[4,148,170,200]. Microbial activity responsible for N2O emissions by the processes of nitrification (NH4+ to NO2 then to N2O and NO3) and denitrification (NO3 and NO2 to N2O, NOX and N2) can be altered by plant secondary metabolites within a multispecies ley[178,201]. Urine-derived plant secondary metabolites such as acteoside, aucubin and isothiocyanates can act as natural NIs within the urine patch, suppressing the microbial activity of nitrate-oxidizing bacteria, ammonia-oxidizing archaea and ammonia-oxidizing bacteria[149,178,202]. However, as with urine composition, the plant secondary metabolite content of urine and longevity in the soil is also inadequately studied. It is unclear what form plant secondary metabolites exist as when broken down in urine or how much is excreted. For a dairy system, Gardiner et al.[147] estimated a potential aucubin urine excretion rate of 0.49−3.40 t·ha−1 for cattle grazing pastures with variable proportions of plantain in the sward composition. Further, the persistence of these plant secondary metabolites in the subsequent crop remains unknown.
Several recent studies have investigated the effect of multispecies swards on N2O losses, particularly in dairy production systems. Di et al.[194] reported a reduction of ~30% in cattle urine N2O emissions from lysimeters from lucerne grazed pasture compared to a ryegrass-white clover pasture, 7.1 and 10.9 kg·ha−1 N2O-N, respectively. In pastures containing 45% plantain, cattle urine-patch N2O emissions were observed to decrease from 6.9 to 1.8 mg·m−2·h−1 N[169]. This was observed to be a result of reductions in urine-N content from grazing key plants containing high levels of secondary metabolites. Cattle urine-N content was also observed to decrease from 6.1 g·L−1 N for a simple pasture to 4.9 g·L−1 N for a multispecies pasture containing chicory, plantain and lucerne[203]. Currently, there are no reports on sheep urine-patch N2O emissions from grazed multispecies leys under field conditions. Focus in the literature is predominantly on dairy production systems, as multispecies pastures can increase the proportion of N used in milk production in cattle[204]. This was observed in an indoor feeding trial; dairy cattle fed a multispecies mix containing perennial ryegrass, prairie grass (Sporobolus cryptandrus), white clover, chicory, plantain, and lucerne, had a higher milk yield (12.5 vs 11.3 kg·d−1 per cow) and higher percentage of N allocated to milk production (23% vs 15%) compared to cows fed a grass-clover mixture[205]. Alongside the numerous ecosystem benefits multispecies leys provide, plants containing high levels of secondary metabolites within a multispecies ley may offer a potential mitigation option for livestock agriculture by reducing excreta patch N2O emissions. However, it is important to note that the sward composition of multispecies leys is crucial, as high proportions of grasses and clovers as well as other herbs with low levels of plant secondary metabolites may dilute the effects of plants with high levels of secondary metabolites and weaken potential benefits. Importantly, the presence of these plants within a multispecies ley does not necessarily mean they are grazed by livestock. The astringency of plants such as chicory often reduces feed intake until livestock adjust to the taste difference or grazing management is changed to encourage consumption, for example, increased stocking density or rotational grazing.

5 LIVESTOCK HEALTH AND PRODUCTIVITY

In addition to reducing livestock GHG emissions, multispecies leys have the potential to improve livestock productivity, particularly in grazing lambs. Due to the implications for soil structure, preference in arable-ley rotations should be given to sheep grazing over cattle. Arable-ley rotations offer the potential for healthier grazing as newly established leys in arable rotations have reduced gastrointestinal nematode burdens than previously grazed permanent pasture[206]. Gastrointestinal nematodes in livestock systems have significant economic impacts, costing the UK sheep industry 84 million GBP·yr–1[207]. Since the introduction of the first anthelminthic, phenothiazine, in the 1950s gastrointestinal nematodes in livestock have developed resistance to commonly used anthelminthics[208,209]. In the UK, increasing resistance to commonly used anthelminthics, such as benzimidazoles, levamisole and macrocyclic lactones, has pushed the UK livestock industry to consider alternative methods of gastrointestinal nematode management[210]. Gastrointestinal nematodes can pass between untreated animals grazing the same pasture and survive outside the host in the sward[206]. Livestock productivity is affected by common gastrointestinal nematodes, such as Nematodirus and Hemonchus contortus, and results in livestock suffering from anemia, edema, weakness, reduced meat, milk and wool production[211,212].
Plant secondary metabolites within multispecies pastures are promoted as natural anthelminthics and can reduce parasite burden in livestock[211]. Studies including plantain, chicory, birdsfoot trefoil and lucerne in multispecies pastures found lower fecal egg counts in infected lambs than comparator grass or grass-clover pastures[213]. Tannins in multispecies pastures can decrease motor activity of gastrointestinal nematodes, inhibit the transformation of eggs to larvae, and inhibit the energy metabolism of gastrointestinal nematodes[214]. A study investigating plantain, chicory and grass swards versus permanent grass pasture found no differences in final fecal egg counts[215]. However, sparse and upright stems within the sward architecture in the plantain-chicory pasture was attributed to reduced adult (L3 parasite stage) parasite populations[215]. It is important to note that including plants with high levels of plant secondary metabolites in swards may not alleviate preexisting high-level gastrointestinal nematode burdens and should not replace effective pharmaceutical anthelminthic treatment on farms, but may reduce the frequency of anthelminthic use and increase the time between treatments. This was demonstrated by Grace et al.[35], where lambs grazing a nine-species multispecies sward required their second anthelminthic dose 59 days after the first treatment compared to lambs grazing a perennial ryegrass sward which needed another dose after 36 days.
As well as reducing parasite burdens, multispecies pastures can also increase live weight gains in livestock. Increased crude protein content in multispecies pastures can increase muscle mass and milk production, increasing livestock performance[216,217]. In New Zealand, lambs grazing a herb-clover pasture experienced weight gains of 0.4 kg·d–1[218]. Similarly, lambs grazing a grass-clover sward had a slower live weight gain and lighter carcass weight per ha over three years (1.27 t·ha−1) compared lambs grazing a multispecies mix of either red and white clover with plantain (1.71 t·ha−1) or chicory and plantain mixture (1.73 t·ha−1)[219]. Reducing the time it takes to reach slaughter weight has, having implications for the carbon footprint and life cycle assessment of lowland meat production. In Ireland, lambs grazing a six- or nine-species pasture containing grasses, legumes and herbs were found to take 168 days to reach slaughter weight compared to lambs grazing pure grass pastures, which took 181 days[35]. Currently, the majority of published studies investigate the impact of an individual herb or legume species, e.g., chicory or sainfoin, on livestock productivity or livestock health. However, there is minimal evidence available for the benefits of multispecies leys on livestock productivity. Future studies should carefully consider sward composition in their experimental design, as multispecies ley mixtures vary between seed companies, ranging from four plant species selected from each plant group (grasses, legumes and herbs) to 16 plant species. Mixtures containing a higher diversity could potentially dilute the effect of plants containing high levels of secondary metabolites within the sward, negating their full potential and resulting in variable results across studies.

6 SUSTAINABLE AGRICULTURAL INTENSIFICATION AND RESILIENCE

Achieving sustainable agricultural intensification is a key cornerstone of environmental research. Arable-ley rotations have long been recognized for their potential for sustainable intensification, with evidence of increases in biodiversity[50]. yield[220], soil nutrients (e.g., N) and organic matter[119], improvements in soil structure[97] and in ungrazed rotations, subsequent crop performance including under drought and flood stresses[65]. The recycling of nutrients and organic matter from livestock grazing has been observed to increase crop yields in integrated crop-livestock systems, but there is minimal data available for crop yields after the reversion of livestock-grazed leys back to arable. In a cattle grazed integrated crop-livestock system, dung inputs increased the availability of soil K and P by 122% and 38%, respectively, subsequently increasing the yield and number of pods per plant of the following soybean crop by 23% and 20% relative to the ungrazed control[83]. However, Taylor et al.[220] found that following a 3-year grass-clover ley grazed by sheep in Scotland, cereal crop yield was highest in the first year following ley reversion back to arable than the second year, producing in the first year and the second year 5.06 and 3.45 t·ha−1 of grain and 3.60 t·ha−1 and 2.26 t·ha−1 of straw, respectively, demonstrating that potential increases in yield are relatively short-lived.
Due to the N fixing capacity of legume containing leys, arable-ley rotations have the potential to reduce the N requirement of the following crop. In the UK, use of mineral N fertilizer has increased by 7.4% between 2008 and 2018, from 0.96 to 1.03 Mt, respectively[221]. By 2030, global demand for mineral N fertilizer to maintain production is predicted to reach 135 Mt[4]. The BNF ability of legumes within a multispecies ley could help to reduce the mineral N fertilizer demand of conventional farms. However, there is limited information available on the effect of leys in rotation on the nitrogen fertilizer replacement value (NFRV) of plowed out leys on crop nitrogen requirements. In Belgium, after a 2-year grass-clover ley was plowed and reverted back to a forage maize (Zea mays) crop, the NFRV was highest in the first year at 177 kg·ha−1N but declined successively over the 3-year period, averaging 79 kg·ha−1 N in the second year and 31 kg·ha−1 N in the third[222]. However, while a reduction in required fertilizer N was observed, Cougnon et al.[222] noted that ley management (i.e., grazing or mowing) did not affect the NFRV. Currently, there is no estimate of the NFRV potential of multispecies leys in rotation.
As well as their ability to reduce mineral N inputs and increase yield, multispecies leys have greater resilience to environmental stresses and extreme weather events than their grass or grass-clover counterparts. The deep rooting capabilities of key species, for example, chicory, yarrow (Achillea millefolium), lucerne and sainfoin, can allow plants greater access to water during drought conditions and maintain biomass production[217]. This could help to maintain productivity and resilience of the farm enterprise, as most countries are expected to experience more extreme weather events due to climate change; however, little is known about the effect of drought and flood events on multispecies leys under field conditions. At the time of this review, there was no available literature on the effect on microbial activity, yield and C and N cycling on multispecies leys under environmental stresses.
Deep rooted species may have the potential to access micronutrients in the subsoil and bring them to the surface to be made available to grazing livestock and cereal crops for human consumption. Micronutrient deficiencies in arable agriculture is often termed the ‘hidden hunger’, as deficiencies in iodine, iron and zinc content in cereal crops have implications for human health[223225]. This is also seen in livestock, as micronutrient deficiencies in the sward composition of grazing pastures can affect the reproductive system in livestock and subsequent meat and milk production, quality, and micronutrient content[224,226]. Compared to grass pastures, herb-rich pastures containing chicory, plantain, white and red clover were found to have greater micronutrient content concentrations of cobalt, copper, zinc and iron but not molybdenum[227]. The grass species cocksfoot was found to have the greatest concentration of manganese[227], however, this response is expected to be highly soil type specific. Pirhofer-Walzl et al.[228] identified that herbs such as chicory, plantain, caraway and salad burnet (Sanguisorba minor) in the multispecies mix had higher levels of sward macro- and micronutrients (e.g., zinc) than grasses and legumes. However, little is known of the effect of these multispecies leys on the micronutrient content of meat and milk production. If herb-rich leys can increase the micronutrient content of livestock products, it may help to address the hidden hunger in modern food production.
Despite the benefits multispecies leys can provide, it cannot be considered a magic bullet for many of the problems facing arable agriculture today. Under an organic farming scenario, if the UK, for example, was to shift to utilizing arable-ley rotations, GHG emissions and crop yield would reduce as production pressure is shifted overseas[229]. If arable-ley rotations were used in conventional agriculture as well this may be avoided. However, arable-ley rotations also face socioeconomic barriers to uptake. A scoping study found that commonly cited reasons against utilizing leys were: (1) short-term economic losses, (2) lack of existing partnerships between arable and livestock farmers, (3) lack of skilled workers with animal husbandry skills, and (4) limited evidence of proven benefits for livestock and arable farmers[135]. A recent review by Schut et al.[21] highlighted that the socioeconomic limitations to reintroducing arable-ley rotations, and thus the recoupling of integrated crop-livestock system, in the EU was mainly driven by the lack of suitable infrastructure, for example, abattoirs and grazing agreements, to support arable-ley rotations. For farmers to overcome these barriers, a change in infrastructure, increased financial support, and improved evidence base evaluating the potential benefits and consequences of arable-ley rotations are needed to help farmers make informed decisions.

7 SUMMARY

The use of ungrazed leys in arable-ley rotations is shown to increase ecosystem service delivery in agriculture through increasing C sequestration, symbiotic nitrogen fixation, water infiltration, biodiversity in soil fauna and microbial communities. However, currently there is insufficient literature available for arable soil improvement under grazed leys, particularly multispecies leys. The majority of previous research has been conducted on grass or grass-clover leys in arable rotations, resulting in a limited evidence base to support and justify the use of multispecies leys in cropping rotations. This review has highlighted that due to their complexity and complementarity of species, multispecies leys can potentially deliver greater ecosystem services than comparator grass or grass-clover ley. Increasing species diversity by utilizing a four- to eight-species multispecies ley can offer greater multifunctionality and opportunities to improve soil quality than a monoculture grass or low diversity (e.g., two- to four-species) grass clover ley. This review has examined the available literature and identified key knowledge gaps in the current understanding of grazed arable-ley rotations. These are as follows:
(1) There is a lack of evidence available on the effect of grazed multispecies leys on AMF, soil biodiversity, soil microbial communities and functioning in degraded arable soils.
(2) Further research is needed on the effect of plant secondary metabolites in fresh and ensiled multispecies leys on rumen microbiome functioning, livestock enteric CH4 emissions, livestock NUE, and gastrointestinal parasite burden.
(3) Lack of information for the biological nitrification inhibitor potential of multispecies leys in urine patches and after mineral N fertilizer applications.
(4) There is a need to assess if a different N2O EF3PRP for excreta deposited by livestock grazing multispecies leys is needed for national and international greenhouse gas inventories, as this is lacking in the IPCC calculations and in the available literature. Without an accurate N2O EF3PRP and enteric methane measurement this reduces the resolution of future carbon footprints and life cycle assessments.
(5) No information is available for micronutrient sward content of multispecies leys and the subsequent micronutrient content of meat and milk from grazed livestock.
(6) There is minimal information available on the tolerance and resilience of multispecies leys to extreme weather events (e.g., drought or flood) with respect to species persistence, pasture yield and quality, and ecosystem services.
(7) Although there is ongoing research across the EU, there is a lack of published data on the effect of reversion from multispecies leys to arable crop as part of the arable-ley rotation with regards to long-term SOC stocks, soil microbial community functioning, and soil N and C cycling.
(8) Further research is needed to provide replicated long-term trials (10-25 years) to evaluate greater ecosystem services (e.g., flood reduction) and identify the best method of ley management (i.e., mowing vs grazing, and sheep vs cattle).
(9) Socioeconomic research is needed to identify cultural barriers and evaluate the economic impacts of multispecies leys and the reintegration of arable-ley rotations to provide an evidence base for on-farm and country-specific economic assessments.
Further research is required to support the development of new policies and legislation to encourage the use of livestock and multispecies leys in arable rotations. Following new research, governments should support provide additional infrastructure (e.g., abattoirs) in predominately arable regions (e.g., eastern Europe) in addition to establishing national grazing networks linking arable and livestock farmers through grazing agreements. This may help overcome the socioeconomic barriers (e.g., skill gaps) that may be limiting the uptake of livestock and leys in arable rotations. Future agri-environment payment schemes should also consider payments for grazing livestock on arable land to encourage a reduction in mineral fertilizer use while improving soil quality. This may help to reduce short-term economic losses often incurred while adopting mixed farming methods. To enable farmers to make informed decisions for what is best for their land, research needs to fill these knowledge gaps and produce evidence-based recommendations.

References

[1]
United Nations. World Population Prospects 2019 Highlights. United Nations, 2019. Available at United Nations website on February 21, 2021
[2]
Food and Agriculture Organization of the United Nations (FAO). The future of food and agriculture: Trends and challenges. FAO, 2017. Available at FAO website on February 24, 2020
[3]
Committee on Climate Change (CCC). Land use: reducing emissions and preparing for climate change. CCC, 2018. Available at the CCC website on February 24, 2020
[4]
Bell M J, Hinton N, Cloy J M, Topp C F E, Rees R M, Cardenas L, Scott T, Webster C, Ashton R W, Whitmore A P, Williams J R, Balshaw H, Paine F, Goulding K W T, Chadwick D R. Nitrous oxide emissions from fertilised UK arable soils: fluxes, emission factors and mitigation. Agriculture, Ecosystems & Environment, 2015, 212 : 134–147
CrossRef Google scholar
[5]
Bouwman A F, Boumans L J M, Batjes N H. Emissions of N2O and NO from fertilized fields: summary of available measurement data. Global Biogeochemical Cycles, 2002, 16(4): 6–1−6–1
[6]
Hicks H L, Comont D, Coutts S R, Crook L, Hull R, Norris K, Neve P, Childs D Z, Freckleton R P. The factors driving evolved herbicide resistance at a national scale. Nature Ecology & Evolution, 2018, 2( 3): 529–536
CrossRef Google scholar
[7]
Ramsden M W, Kendall S L, Ellis S A, Berry P M. A review of economic thresholds for invertebrate pests in UK arable crops. Crop Protection, 2017, 96 : 30–43
CrossRef Google scholar
[8]
Donal P F, Green R E, Heath M F. Agricultural intensification and the collapse of Europe’s farmland bird populations. Proceedings of the Royal Society B: Biological Sciences, 2001, 268( 1462): 25–29
CrossRef Google scholar
[9]
Graves A R, Morris J, Deeks L K, Rickson R J, Kibblewhite M G, Harris J A, Farewell T S, Truckle I. The total costs of soil degradation in England and Wales. Ecological Economics, 2015, 119 : 399–413
CrossRef Google scholar
[10]
Gregory A S, Ritz K, McGrath S P, Quinton J N, Goulding K W T, Jones R J A, Harris J A, Bol R, Wallace P, Pilgrim E S, Whitmore A P. A review of the impacts of degradation threats on soil properties in the UK. Soil Use and Management, 2015, 31(Suppl 1): 1–15
[11]
Panagos P, Standardi G, Borrelli P, Lugato E, Montanarella L, Bosello F. Cost of agricultural productivity loss due to soil erosion in the European Union: from direct cost evaluation approaches to the use of macroeconomic models. Land Degradation & Development, 2018, 29( 3): 471–484
CrossRef Google scholar
[12]
Verheijen F G A, Jones R J A, Rickson R J, Smith C J. Tolerable versus actual soil erosion rates in Europe. Earth-Science Reviews, 2009, 94( 1-4): 23–38
CrossRef Google scholar
[13]
Kibblewhite M G, Ritz K, Swift M J. Soil health in agricultural systems. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 2008, 363( 1492): 685–701
CrossRef Google scholar
[14]
European Commission. Thematic strategy for soil protection. European Commission, 2006. Available at European Commission website on October 20, 2021
[15]
Nkonya E, Anderson W, Kato E, Mirzabaev A, von Braun J, Meyer S. Global Cost of Land Degradation. In: Nkonya E, Mirzabaev A, von Braun J, eds. Economics of Land Degradation and Improvement—A Global Assessment for Sustainable Development. Springer, 2016, 117–165
[16]
Robinson R A, Sutherland W J. Post-war changes in arable farming and biodiversity in Great Britain. Journal of Applied Ecology, 2002, 39( 1): 157–176
CrossRef Google scholar
[17]
Knox O G G, Leake A R, Walker R L, Edwards A C, Watson C A. Revisiting the multiple benefits of historical crop rotations within contemporary UK agricultural systems. Journal of Sustainable Agriculture, 2011, 35( 2): 163–179
CrossRef Google scholar
[18]
Posthumus H, Deeks L K, Rickson R J, Quinton J N. Costs and benefits of erosion control measures in the UK. Soil Use and Management, 2015, 31( S1): 16–33
CrossRef Google scholar
[19]
Department for Environment, Food & Rural Affairs of United Kingdom (DEFRAUK). Agriculture in the United Kingdom 2019. DEFRAUK, 2019. Available at UK Government website on February 11, 2020
[20]
Sekaran U, Lai L, Ussiri D A N, Kumar S, Clay S. Role of integrated crop-livestock systems in improving agriculture production and addressing food security—a review. Journal of Agriculture and Food Research, 2021, 5 : 100190
CrossRef Google scholar
[21]
Schut A G T, Cooledge E C, Moraine M, De Ven G W J V, Jones D L, Chadwick D R. Reintegration of crop-livestock systems in europe: an overview. Frontiers of Agricultural Science and Engineering, 2021, 8( 1): 111–129
CrossRef Google scholar
[22]
Johnston A E, Poulton P R, Coleman K, Macdonald A J, White R P. Changes in soil organic matter over 70 years in continuous arable and ley-arable rotations on a sandy loam soil in England. European Journal of Soil Science, 2017, 68( 3): 305–316
CrossRef Google scholar
[23]
Lemaire G, Franzluebbers A, Carvalho P C de F, Dedieu B. Integrated crop-livestock systems: strategies to achieve synergy between agricultural production and environmental quality. Agriculture, Ecosystems & Environment, 2014, 190 : 4–8
CrossRef Google scholar
[24]
Kumar S, Sieverding H, Lai L, Thandiwe N, Wienhold B, Redfearn D, Archer D, Ussiri D, Faust D, Landblom D, Grings E, Stone J J, Jacquet J, Pokharel K, Liebig M, Schmer M, Sexton P, Mitchell R, Smalley S, Osborne S, Ali S, Şentürklü S, Sehgal S, Owens V, Jin V. Facilitating crop–livestock reintegration in the northern great plains. Agronomy Journal, 2019, 111( 5): 2141–2156
CrossRef Google scholar
[25]
Cong W F, Eriksen J. Forbs differentially affect soil microbial community composition and functions in unfertilized ryegrass-red clover leys. Soil Biology & Biochemistry, 2018, 121 : 87–94
CrossRef Google scholar
[26]
Jing J, Søegaard K, Cong W F, Eriksen J. Species diversity effects on productivity, persistence and quality of multispecies swards in a four-year experiment. PLoS One, 2017, 12( 1): e0169208
CrossRef Google scholar
[27]
Moloney T, Sheridan H, Grant J, O’Riordan E G, O’Kiely P. Yield of binary- and multi-species swards relative to single-species swards in intensive silage systems. Irish Journal of Agricultural and Food Research, 2020, 59( 1): 12–26
CrossRef Google scholar
[28]
Kingston-Smith A H, Marshall A H, Moorby J M. Breeding for genetic improvement of forage plants in relation to increasing animal production with reduced environmental footprint. Animal, 2013, 7(Suppl 1): 79–88
[29]
Pembleton K G, Tozer K N, Edwards G R, Jacobs J L, Turner L R. Simple versus diverse pastures: opportunities and challenges in dairy systems. Animal Production Science, 2015, 55( 7): 893–901
CrossRef Google scholar
[30]
Pembleton K G, Hills J L, Freeman M J, McLaren D K, French M, Rawnsley R P. More milk from forage: milk production, blood metabolites, and forage intake of dairy cows grazing pasture mixtures and spatially adjacent monocultures. Journal of Dairy Science, 2016, 99( 5): 3512–3528
CrossRef Google scholar
[31]
Ten Berge H F M, Pikula D, Goedhart P W, Schröder J J. Apparent nitrogen fertilizer replacement value of grass-clover leys and of farmyard manure in an arable rotation. Part I: grass-clover leys. Soil Use and Management, 2016, 32( S1): 9–19
CrossRef Google scholar
[32]
Hansen E M, Eriksen J. Nitrate leaching in maize after cultivation of differently managed grass-clover leys on coarse sand in Denmark. Agriculture, Ecosystems & Environment, 2016, 216 : 309–313
CrossRef Google scholar
[33]
Quijas S, Schmid B, Balvanera P. Plant diversity enhances provision of ecosystem services: a new synthesis. Basic and Applied Ecology, 2010, 11( 7): 582–593
CrossRef Google scholar
[34]
Sanderson M A, Goslee S C, Soder K J, Skinner R H, Tracy B F, Deak A. Plant species diversity, ecosystem function, and pasture management—a perspective. Canadian Journal of Plant Science, 2007, 87( 3): 479–487
CrossRef Google scholar
[35]
Grace C, Lynch M B, Sheridan H, Lott S, Fritch R, Boland T M. Grazing multispecies swards improves ewe and lamb performance. Animal, 2018, 13( 8): 1–9
[36]
Bracken C J, Lanigan G J, Richards K G, Müller C, Tracy S R, Grant J, Krol D J, Sheridan H, Lynch M B, Grace C, Fritch R, Murphy P N C. Sward composition and soil moisture conditions affect nitrous oxide emissions and soil nitrogen dynamics following urea-nitrogen application. Science of the Total Environment, 2020, 722 : 137780
CrossRef Google scholar
[37]
Millennium Ecosystem Assessment. MA Conceptual Framework. Millennium Ecosystem Assessment, 2005. Available at Millennium Ecosystem Assessment website on February 21, 2021
[38]
Foley J A, Defries R, Asner G P, Barford C, Bonan G, Carpenter S R, Chapin F S, Coe M T, Daily G C, Gibbs H K, Helkowski J H, Holloway T, Howard E A, Kucharik C J, Monfreda C, Patz J A, Prentice I C, Ramankutty N, Snyder P K. Global consequences of land use. Science, 2005, 309( 5734): 570–574
CrossRef Google scholar
[39]
Power A G. Ecosystem services and agriculture: tradeoffs and synergies. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 2010, 365( 1554): 2959–2971
CrossRef Google scholar
[40]
Ekroos J, Olsson O, Rundlöf M, Wätzold F, Smith H G. Optimizing agri-environment schemes for biodiversity, ecosystem services or both. Biological Conservation, 2014, 172 : 65–71
CrossRef Google scholar
[41]
Horrocks C A, Dungait J A J, Cardenas L M, Heal K V. Does extensification lead to enhanced provision of ecosystems services from soils in UK agriculture. Land Use Policy, 2014, 38 : 123–128
CrossRef Google scholar
[42]
UK Government. GS4: Legume and herb-rich swards. UK Government, 2020. Available at UK government website on February 12, 2020
[43]
Welsh Audit Office. Tir Gofal. Welsh Audit Office, 2007. Available at Welsh Audit Office website on February 21, 2020
[44]
UK Government. GS7: restoration towards species-rich grassland. UK Government, 2020. Available at UK government website on January 27, 2022
[45]
UK Government. GS6: management of species-rich grassland. UK Government, 2021. Available at UK government website on January 27, 2022
[46]
Arnott D, Chadwick D R, Harris I, Koj A, Jones D L. What can management option uptake tell us about ecosystem services delivery through agri-environment schemes. Land Use Policy, 2019, 81 : 194–208
CrossRef Google scholar
[47]
Jones J I, Murphy J F, Anthony S G, Arnold A, Blackburn J H, Duerdoth C P, Hawczak A, Hughes G O, Pretty J L, Scarlett P M, Gooday R D, Zhang Y S, Fawcett L E, Simpson D, Turner A W B, Naden P S, Skates J. Do agri-environment schemes result in improved water quality. Journal of Applied Ecology, 2017, 54( 2): 537–546
CrossRef Google scholar
[48]
Teagasc. Results-based Environment-Agri Pilot Project (REAP). Teagasc, 2021. Available at Teagasc website on March 16, 2022
[49]
Horrocks C A, Heal K V, Harvie B, Tallowin J B, Cardenas L M, Dungait J A J. Can species-rich grasslands be established on former intensively managed arable soils. Agriculture, Ecosystems & Environment, 2016, 217 : 59–67
CrossRef Google scholar
[50]
Albizua A, Williams A, Hedlund K, Pascual U. Crop rotations including ley and manure can promote ecosystem services in conventional farming systems. Applied Soil Ecology, 2015, 95 : 54–61
CrossRef Google scholar
[51]
Lemaire G, Gastal F, Franzluebbers A, Chabbi A. Grassland-cropping rotations: an avenue for agricultural diversification to reconcile high production with environmental quality. Environmental Management, 2015, 56( 5): 1065–1077
CrossRef Google scholar
[52]
Malézieux E, Crozat Y, Dupraz C, Laurans M, Makowski D, Ozier-Lafontaine H, Rapidel B, De Tourdonnet S, de Tourdonnet S, Valantin-Morison M. Mixing plant species in cropping systems: concepts, tools and models. A review. Agronomy for Sustainable Development, 2009, 29( 1): 43–62
CrossRef Google scholar
[53]
Finn J A, Kirwan L, Connolly J, Sebastià M T, Helgadottir A, Baadshaug O H, Bélanger G, Black A, Brophy C, Collins R P, Čop J, Dalmannsdóttir S, Delgado I, Elgersma A, Fothergill M, Frankow-Lindberg B E, Ghesquiere A, Golinska B, Golinski P, Grieu P, Gustavsson A M, Höglind M, Huguenin-Elie O, Jørgensen M, Kadziuliene Z, Kurki P, Llurba R, Lunnan T, Porqueddu C, Suter M, Thumm U, Lüscher A. Ecosystem function enhanced by combining four functional types of plant species in intensively managed grassland mixtures: a 3-year continental-scale field experiment. Journal of Applied Ecology, 2013, 50( 2): 365–375
CrossRef Google scholar
[54]
Suter M, Huguenin-Elie O, Lüscher A. Multispecies for multifunctions: combining four complementary species enhances multifunctionality of sown grassland. Scientific Reports, 2021, 11( 1): 3835
CrossRef Google scholar
[55]
Grange G, Finn J A, Brophy C. Plant diversity enhanced yield and mitigated drought impacts in intensively managed grassland communities. Journal of Applied Ecology, 2021, 58( 9): 1864–1875
CrossRef Google scholar
[56]
McNally S R, Laughlin D C, Rutledge S, Dodd M B, Six J, Schipper L A. Root carbon inputs under moderately diverse sward and conventional ryegrass-clover pasture: implications for soil carbon sequestration. Plant and Soil, 2015, 392( 1−2): 289–299
CrossRef Google scholar
[57]
Modernel P, Dogliotti S, Alvarez S, Corbeels M, Picasso V, Tittonell P, Rossing W A H. Identification of beef production farms in the Pampas and Campos area that stand out in economic and environmental performance. Ecological Indicators, 2018, 89 : 755–770
CrossRef Google scholar
[58]
Nicholls C I, Altieri M A. Plant biodiversity enhances bees and other insect pollinators in agroecosystems. A review. Agronomy for Sustainable Development, 2013, 33( 2): 257–274
CrossRef Google scholar
[59]
Wagner S C. Biological nitrogen fixation. Nature Education Knowledge., 2011, 3( 10): 15
[60]
Mueller K E, Tilman D, Fornara D A, Hobbie S E. Root depth distribution and the diversity-productivity relationship in a long-term grassland experiment. Ecology, 2013, 94( 4): 787–793
CrossRef Google scholar
[61]
Nevens F, Reheul D. The nitrogen- and non-nitrogen-contribution effect of ploughed grass leys on the following arable forage crops: Determination and optimum use. European Journal of Agronomy, 2002, 16( 1): 57–74
CrossRef Google scholar
[62]
Pagliai M, Vignozzi N, Pellegrini S. Soil structure and the effect of management practices. Soil & Tillage Research, 2004, 79( 2): 131–143
CrossRef Google scholar
[63]
Kabir Z. Tillage or no-tillage: impact on mycorrhizae. Canadian Journal of Plant Science, 2005, 85( 1): 23–29
CrossRef Google scholar
[64]
Yang T, Siddique K H M, Liu K. Cropping systems in agriculture and their impact on soil health—a review. Global Ecology and Conservation, 2020, 23 : e01118
CrossRef Google scholar
[65]
Berdeni D, Turner A, Grayson R P, Llanos J, Holden J, Firbank L G, Lappage M G, Hunt S P F, Chapman P J, Hodson M E, Helgason T, Watt P J, Leake J R. Soil quality regeneration by grass-clover leys in arable rotations compared to permanent grassland: effects on wheat yield and resilience to drought and flooding. Soil & Tillage Research, 2021, 212 : 105037
CrossRef Google scholar
[66]
Lehmann A, Zheng W, Rillig M C. Soil biota contributions to soil aggregation. Nature Ecology & Evolution, 2017, 1( 12): 1828–1835
CrossRef Google scholar
[67]
Anderson C, Beare M, Buckley H L, Lear G. Bacterial and fungal communities respond differently to varying tillage depth in agricultural soils. PeerJ, 2017, 5( 10): e3930
[68]
Sun R, Li W, Dong W, Tian Y, Hu C, Liu B. Tillage changes vertical distribution of soil bacterial and fungal communities. Frontiers in Microbiology, 2018, 9 : 699
CrossRef Google scholar
[69]
Yvan C, Stéphane S, Stéphane C, Pierre B, Guy R, Hubert B. Role of earthworms in regenerating soil structure after compaction in reduced tillage systems. Soil Biology & Biochemistry, 2012, 55 : 93–103
CrossRef Google scholar
[70]
Langmaack M, Schrader S, Rapp-Bernhardt U, Kotzke K. Soil structure rehabilitation of arable soil degraded by compaction. Geoderma, 2002, 105( 1−2): 141–152
CrossRef Google scholar
[71]
Shah A N, Tanveer M, Shahzad B, Yang G, Fahad S, Ali S, Bukhari M A, Tung S A, Hafeez A, Souliyanonh B. Soil compaction effects on soil health and cropproductivity: an overview. Environmental Science and Pollution Research International, 2017, 24( 11): 10056–10067
CrossRef Google scholar
[72]
Grave R A, Nicoloso R da S, Cassol P C, da Silva M L B, Mezzari M P, Aita C, Wuaden C R. Determining the effects of tillage and nitrogen sources on soil N2O emission. Soil & Tillage Research, 2018, 175 : 1–12
CrossRef Google scholar
[73]
Schneider F, Don A, Hennings I, Schmittmann O, Seidel S J. The effect of deep tillage on crop yield—what do we really know. Soil & Tillage Research, 2017, 174 : 193–204
CrossRef Google scholar
[74]
Intergovernmental Panel on Climate Change (IPCC). Climate Change and Land: an IPCC special report on climate change, desertification, land degradation, sustainable land management, food security, and greenhouse gas fluxes in terrestrial ecosystems. IPCC, 2019. Available at IPCC website on March 16, 2022
[75]
Arai M, Miura T, Tsuzura H, Minamiya Y, Kaneko N. Two-year responses of earthworm abundance, soil aggregates, and soil carbon to no-tillage and fertilization. Geoderma, 2018, 332 : 135–141
CrossRef Google scholar
[76]
Lenssen A W, Sainju U M, Hatfield P G. Integrating sheep grazing into wheat-fallow systems: crop yield and soil properties. Field Crops Research, 2013, 146 : 75–85
CrossRef Google scholar
[77]
Elias D, Wang L, Jacinthe P A. A meta-analysis of pesticide loss in runoff under conventional tillage and no-till management. Environmental Monitoring and Assessment, 2018, 190( 2): 79
CrossRef Google scholar
[78]
Hull R, Tatnell L V, Cook S K, Beffa R, Moss S R. Current status of herbicide-resistant weeds in the UK. In: Crop Production in Southern Britain: Precision Decisions for Profitable Cropping. Aspects of Applied Biology, 2014, 127: 261–272
[79]
Davies L R, Hull R, Moss S, Neve P. The first cases of evolving glyphosate resistance in UK poverty brome (Bromus sterilis) populations. Weed Science, 2019, 67( 1): 41–47
CrossRef Google scholar
[80]
Collavo A, Sattin M. Resistance to glyphosate in Lolium rigidum selected in Italian perennial crops: bioevaluation, management and molecular bases of target-site resistance. Weed Research, 2012, 52( 1): 16–24
CrossRef Google scholar
[81]
Alskaf K, Sparkes D L, Mooney S J, Sjögersten S, Wilson P. The uptake of different tillage practices in England. Soil Use and Management, 2020, 36( 1): 27–44
CrossRef Google scholar
[82]
Martin G, Durand J L, Duru M, Gastal F, Julier B, Litrico I, Louarn G, Médiène S, Moreau D, Valentin-Morison M, Novak S, Parnaudeau V, Paschalidou F, Vertès F, Voisin A S, Cellier P, Jeuffroy M H. Role of ley pastures in tomorrow’s cropping systems. A review. Agronomy for Sustainable Development, 2020, 40( 3): 17
CrossRef Google scholar
[83]
Da Silva F D, Amado T J C, Bredemeier C, Bremm C, Anghinoni I, Carvalho P C de F. Pasture grazing intensity and presence or absence of cattle dung input and its relationships to soybean nutrition and yield in integrated crop-livestock systems under no-till. European Journal of Agronomy, 2014, 57 : 84–91
CrossRef Google scholar
[84]
Detheridge A P, Brand G, Fychan R, Crotty F V, Sanderson R, Griffith G W, Marley C L. The legacy effect of cover crops on soil fungal populations in a cereal rotation. Agriculture, Ecosystems & Environment, 2016, 228 : 49–61
CrossRef Google scholar
[85]
Tracy B F, Davis A S. Weed biomass and species composition as affected by an integrated crop-livestock system. Crop Science, 2009, 49( 4): 1523–1530
CrossRef Google scholar
[86]
Christensen B T, Rasmussen J, Eriksen J, Hansen E M. Soil carbon storage and yields of spring barley following grass leys of different age. European Journal of Agronomy, 2009, 31( 1): 29–35
CrossRef Google scholar
[87]
Franzluebbers A J, Stuedemann J A. Early response of soil organic fractions to tillage and integrated crop-livestock production. Soil Science Society of America Journal, 2008, 72( 3): 613–625
CrossRef Google scholar
[88]
Low A J. Improvements in the structural state of soils under leys. Journal of Soil Science, 1955, 6( 2): 179–199
CrossRef Google scholar
[89]
Kautz T, Lüsebrink M, Pätzold S, Vetterlein D, Pude R, Athmann M, Küpper P M, Perkons U, Köpke U. Contribution of anecic earthworms to biopore formation during cultivation of perennial ley crops. Pedobiologia, 2014, 57( 1): 47–52
CrossRef Google scholar
[90]
Mytton L R, Cresswell A, Colbourn P. Improvement in soil structure associated with white clover. Grass and Forage Science, 1993, 48( 1): 84–90
CrossRef Google scholar
[91]
Kell D B. Large-scale sequestration of atmospheric carbon via plant roots in natural and agricultural ecosystems: why and how. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 2012, 367( 1595): 1589–1597
CrossRef Google scholar
[92]
Riley H, Pommeresche R, Eltun R, Hansen S, Korsaeth A. Soil structure, organic matter and earthworm activity in a comparison of cropping systems with contrasting tillage, rotations, fertilizer levels and manure use. Agriculture, Ecosystems & Environment, 2008, 124( 3−4): 275–284
CrossRef Google scholar
[93]
Hodge A. Microbial ecology of the arbuscular mycorrhiza. FEMS Microbiology Ecology, 2000, 32( 2): 91–96
CrossRef Google scholar
[94]
Püschel D, Janoušková M, Voříšková A, Gryndlerová H, Vosátka M, Jansa J. Arbuscular mycorrhiza stimulates biological nitrogen fixation in two Medicago spp. through improved phosphorus acquisition. Frontiers in Plant Science, 2017, 8 : 390
CrossRef Google scholar
[95]
Haynes R J. Labile organic matter fractions and aggregate stability under short-term, grass-based leys. Soil Biology & Biochemistry, 1999, 31( 13): 1821–1830
CrossRef Google scholar
[96]
Studdert G A, Echeverría H E, Casanovas E M. Crop-pasture rotation for sustaining the quality and productivity of a typic argiudoll. Soil Science Society of America Journal, 1997, 61( 5): 1466–1472
CrossRef Google scholar
[97]
Hallam J, Berdeni D, Grayson R, Guest E J, Holden J, Lappage M G, Prendergast-Miller M T, Robinson D A, Turner A, Leake J R, Hodson M E. Effect of earthworms on soil physico-hydraulic and chemical properties, herbage production, and wheat growth on arable land converted to ley. Science of the Total Environment, 2020, 713 : 136491
CrossRef Google scholar
[98]
Prendergast-Miller M T, Jones D T, Berdeni D, Bird S, Chapman P J, Firbank L, Grayson R, Helgason T, Holden J, Lappage M, Leake J, Hodson M E. Arable fields as potential reservoirs of biodiversity: earthworm populations increase in new leys. Science of the Total Environment, 2021, 789 : 147880
CrossRef Google scholar
[99]
van Eekeren N, Bommelé L, Bloem J, Schouten T, Rutgers M, de Goede R, Reheul D, Brussaard L. Soil biological quality after 36 years of ley-arable cropping, permanent grassland and permanent arable cropping. Applied Soil Ecology, 2008, 40( 3): 432–446
CrossRef Google scholar
[100]
Säle V, Aguilera P, Laczko E, Mäder P, Berner A, Zihlmann U, van der Heijden M G A, Oehl F. Impact of conservation tillage and organic farming on the diversity of arbuscular mycorrhizal fungi. Soil Biology & Biochemistry, 2015, 84 : 38–52
CrossRef Google scholar
[101]
Abdalla M, Hastings A, Chadwick D R, Jones D L, Evans C D, Jones M B, Rees R M, Smith P. Critical review of the impacts of grazing intensity on soil organic carbon storage and other soil quality indicators in extensively managed grasslands. Agriculture, Ecosystems & Environment, 2018, 253 : 62–81
CrossRef Google scholar
[102]
Stavi I, Lal R, Owens L B. Effects of cattle grazing during the dormant season on soil surface hydrology and physical quality in a moist-temperate region. Ecohydrology, 2011, 4( 1): 106–114
CrossRef Google scholar
[103]
Martin G, Moraine M, Ryschawy J, Magne M A, Asai M, Sarthou J P, Duru M, Therond O. Crop–livestock integration beyond the farm level: a review. Agronomy for Sustainable Development, 2016, 36( 3): 53
CrossRef Google scholar
[104]
Ambus J V, Reichert J M, Gubiani P I, de Faccio Carvalho P C. Changes in composition and functional soil properties in long-term no-till integrated crop-livestock system. Geoderma, 2018, 330 : 232–243
CrossRef Google scholar
[105]
do Nascimento D M, Cavalieri-Polizeli K M V, da Silva A H, Favaretto N, Parron L M. Soil physical quality under long-term integrated agricultural production systems. Soil & Tillage Research, 2019, 186 : 292–299
CrossRef Google scholar
[106]
Schuster M Z, Pelissari A, de Moraes A, Harrison S K, Sulc R M, Lustosa S B C, Anghinoni I, Carvalho P C F. Grazing intensities affect weed seedling emergence and the seed bank in an integrated crop–livestock system. Agriculture, Ecosystems & Environment, 2016, 232 : 232–239
CrossRef Google scholar
[107]
Greenwood K L, McKenzie B M. Grazing effects on soil physical properties and the consequences for pastures: a review. Australian Journal of Experimental Agriculture, 2001, 41( 8): 1231–1250
CrossRef Google scholar
[108]
Laurenson S, Houlbrooke D J. Assessing the agronomic benefit of noninversion tillage for improving soil structure following winter grazing of cattle and sheep. Soil Use and Management, 2014, 30( 4): 595–602
CrossRef Google scholar
[109]
Ball B C, Watson C A, Baddeley J A. Soil physical fertility, soil structure and rooting conditions after ploughing organically managed grass/clover swards. Soil Use and Management, 2007, 23( 1): 20–27
CrossRef Google scholar
[110]
Six J, Frey S D, Thiet R K, Batten K M. Bacterial and fungal contributions to carbon sequestration in agroecosystems. Soil Science Society of America Journal, 2006, 70( 2): 555–569
CrossRef Google scholar
[111]
Jones D L, Cooledge E C, Hoyle F C, Griffiths R I, Murphy D V. pH and exchangeable aluminum are major regulators of microbial energy flow and carbon use efficiency in soil microbial communities. Soil Biology & Biochemistry, 2019, 138 : 107584
CrossRef Google scholar
[112]
Murphy D V, Stockdale E A, Poulton P R, Willison T W, Goulding K W T. Seasonal dynamics of carbon and nitrogen pools and fluxes under continuous arable and ley-arable rotations in a temperate environment. European Journal of Soil Science, 2007, 58( 6): 1410–1424
CrossRef Google scholar
[113]
Mellado-Vázquez P G, Lange M, Gleixner G. Soil microbial communities and their carbon assimilation are affected by soil properties and season but not by plants differing in their photosynthetic pathways (C3 vs. C4). Biogeochemistry, 2019, 142( 2): 175–187
CrossRef Google scholar
[114]
Collins M, Knutti R, Arblaster J, Dufresne J L, Fichefet T, Friedlingstein P, Gao X, Gutowski W J, Johns T, Krinner G, Shongwe M, Tebaldi C, Weaver A J, Wehner M F, Allen M R, Andrews T, Beyerle U, Bitz C M, Bony S, Booth B B B. Long-term climate change: projections, commitments and irreversibility. In: Stocker T F, Qin D, Plattner G K, Tignor M M B, Allen S K, Boschung J, Nauels A, Xia Y, Bex V, Midgley P M, eds. Climate Change 2013—the Physical Science Basis: Contribution of Working Group I to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. New York: Cambridge University Press, 2013, 1029–1136
[115]
Bölscher T, Ågren G I, Herrmann A M. Land-use alters the temperature response of microbial carbon-use efficiency in soils—a consumption-based approach. Soil Biology & Biochemistry, 2020, 140 : 107639
CrossRef Google scholar
[116]
McAuliffe G A, López-Aizpún M, Blackwell M S A, Castellano-Hinojosa A, Darch T, Evans J, Horrocks C, Le Cocq K, Takahashi T, Harris P, Lee M R F, Cardenas L. Elucidating three-way interactions between soil, pasture and animals that regulate nitrous oxide emissions from temperate grazing systems. Agriculture, Ecosystems & Environment, 2020, 300 : 106978
CrossRef Google scholar
[117]
Qu T, Guo W, Yang C, Zhang J, Yang Y, Wang D. Grazing by large herbivores improves soil microbial metabolic activity in a meadow steppe. Grassland Science, 2021, 67( 1): 30–40
CrossRef Google scholar
[118]
Kautz T, Amelung W, Ewert F, Gaiser T, Horn R, Jahn R, Javaux M, Kemna A, Kuzyakov Y, Munch J C, Pätzold S, Peth S, Scherer H W, Schloter M, Schneider H, Vanderborght J, Vetterlein D, Walter A, Wiesenberg G L B, Köpke U. Nutrient acquisition from arable subsoils in temperate climates: a review. Soil Biology & Biochemistry, 2013, 57 : 1003–1022
CrossRef Google scholar
[119]
Jarvis N, Forkman J, Koestel J, Kätterer T, Larsbo M, Taylor A. Long-term effects of grass-clover leys on the structure of a silt loam soil in a cold climate. Agriculture, Ecosystems & Environment, 2017, 247 : 319–328
CrossRef Google scholar
[120]
Zarea M J, Ghalavand A, Goltapeh E M, Rejali F, Zamaniyan M. Effects of mixed cropping, earthworms (Pheretima sp.), and arbuscular mycorrhizal fungi (Glomus mosseae) on plant yield, mycorrhizal colonization rate, soil microbial biomass, and nitrogenase activity of free-living rhizosphere bacteria. Pedobiologia, 2009, 52( 4): 223–235
CrossRef Google scholar
[121]
Chen X, Henriksen T M, Svensson K, Korsaeth A. Long-term effects of agricultural production systems on structure and function of the soil microbial community. Applied Soil Ecology, 2020, 147 : 103387
CrossRef Google scholar
[122]
Minasny B, Malone B P, McBratney A B, Angers D A, Arrouays D, Chambers A, Chaplot V, Chen Z S, Cheng K, Das B S, Field D J, Gimona A, Hedley C B, Hong S Y, Mandal B, Marchant B P, Martin M, McConkey B G, Mulder V L, O’Rourke S, Richer-de-Forges A C, Odeh I, Padarian J, Paustian K, Pan G, Poggio L, Savin I, Stolbovoy V, Stockmann U, Sulaeman Y, Tsui C C, Vågen T G, van Wesemael B, Winowiecki L. Soil carbon 4 per mille. Geoderma, 2017, 292 : 59–86
CrossRef Google scholar
[123]
Ostle N J, Levy P E, Evans C D, Smith P. UK land use and soil carbon sequestration. Land Use Policy, 2009, 26(Suppl 1): S274−S283
[124]
Poulton P, Johnston J, Macdonald A, White R, Powlson D. Major limitations to achieving “4 per 1000” increases in soil organic carbon stock in temperate regions: Evidence from long-term experiments at Rothamsted Research, United Kingdom. Global Change Biology, 2018, 24( 6): 2563–2584
CrossRef Google scholar
[125]
UK Government. A Green Future: Our 25 Year Plan to Improve the Environment. UK Government, 2018. Available at UK Government website on January 20, 2020
[126]
Börjesson G, Bolinder M A, Kirchmann H, Kätterer T. Organic carbon stocks in topsoil and subsoil in long-term ley and cereal monoculture rotations. Biology and Fertility of Soils, 2018, 54( 4): 549–558
CrossRef Google scholar
[127]
Krauss M, Ruser R, Müller T, Hansen S, Mäder P, Gattinger A. Impact of reduced tillage on greenhouse gas emissions and soil carbon stocks in an organic grass-clover ley-winter wheat cropping sequence. Agriculture, Ecosystems & Environment, 2017, 239 : 324–333
CrossRef Google scholar
[128]
Chan K Y, Conyers M, Li G D, Helyar K, Poile G, Oates A, Barchia I. Soil carbon dynamics under different cropping and pasture management in temperate Australia: results of three long-term experiments. Soil Research, 2011, 49( 4): 320–328
CrossRef Google scholar
[129]
Bolinder M A, Kätterer T, Andrén O, Ericson L, Parent L E, Kirchmann H. Long-term soil organic carbon and nitrogen dynamics in forage-based crop rotations in Northern Sweden (63–64°N). Agriculture, Ecosystems & Environment, 2010, 138( 3−4): 335–342
CrossRef Google scholar
[130]
Chirinda N, Olesen J E, Porter J R, Schjønning P. Soil properties, crop production and greenhouse gas emissions from organic and inorganic fertilizer-based arable cropping systems. Agriculture, Ecosystems & Environment, 2010, 139( 4): 584–594
CrossRef Google scholar
[131]
Clement C R, Williams T E. Leys and soil organic matter: I. The accumulation of organic carbon in soils under different leys. Journal of Agricultural Science, 1964, 63( 3): 377–383
CrossRef Google scholar
[132]
Hanley F, Ridgman W J, Allen E J. Some effects of the inclusion of leys in a six-course rotation on light land. Journal of Agricultural Science, 1973, 80( 1): 53–62
CrossRef Google scholar
[133]
Sun Z, Chen Q, Han X, Bol R, Qu B, Meng F. Allocation of photosynthesized carbon in an intensively farmed winter wheat-soil system as revealed by 14CO2 pulse labelling. Scientific Reports, 2018, 8( 1): 3160
CrossRef Google scholar
[134]
Jensen J L, Schjønning P, Watts C W, Christensen B T, Obour P B, Munkholm L J. Soil degradation and recovery—changes in organic matter fractions and structural stability. Geoderma, 2020, 364 : 114181
CrossRef Google scholar
[135]
Knight S, Stockdale E, Stoate C, Rust N. Scoping study—achieving sustainable intensification by integrating livestock into arable systems—opportunities and impacts. Department for Environment, Food and Rural Affairs, 2019
[136]
Crews T E, Peoples M B. Legume versus fertilizer sources of nitrogen: ecological tradeoffs and human needs. Agriculture, Ecosystems & Environment, 2004, 102( 3): 279–297
CrossRef Google scholar
[137]
Fornara D A, Tilman D. Plant functional composition influences rates of soil carbon and nitrogen accumulation. Journal of Ecology, 2008, 96( 2): 314–322
CrossRef Google scholar
[138]
Norton J, Ouyang Y. Controls and adaptive management of nitrification in agricultural soils. Frontiers in Microbiology, 2019, 10 : 1931
CrossRef Google scholar
[139]
Coskun D, Britto D T, Shi W, Kronzucker H J. How plant root exudates shape the nitrogen cycle. Trends in Plant Science, 2017, 22( 8): 661–673
CrossRef Google scholar
[140]
Zerulla W, Barth T, Dressel J, Erhardt K, Horchler von Locquenghien K, Pasda G, Rädle M, Wissemeier A. 3,4-Dimethylpyrazole phosphate (DMPP)—a new nitrification inhibitor for agriculture and horticulture: an introduction. Biology and Fertility of Soils, 2001, 34( 2): 79–84
CrossRef Google scholar
[141]
Ministry for Primary Industries (MPI). New Zealand Government assures safety of country’s dairy products. New Zealand: MPI, 2013. Available at New Zealand Government media website on February 21, 2021
[142]
Abalos D, Jeffery S, Sanz-Cobena A, Guardia G, Vallejo A. Meta-analysis of the effect of urease and nitrification inhibitors on crop productivity and nitrogen use efficiency. Agriculture, Ecosystems & Environment, 2014, 189 : 136–144
CrossRef Google scholar
[143]
Misselbrook T H, Cardenas L M, Camp V, Thorman R E, Williams J R, Rollett A J, Chambers B J. An assessment of nitrification inhibitors to reduce nitrous oxide emissions from UK agriculture. Environmental Research Letters, 2014, 9( 11): 115006
CrossRef Google scholar
[144]
Marsden K A, Jones D L, Chadwick D R. DMPP is ineffective at mitigating N2O emissions from sheep urine patches in a UK grassland under summer conditions. Agriculture, Ecosystems & Environment, 2017, 246 : 1–11
CrossRef Google scholar
[145]
Subbarao G V, Sahrawat K L, Nakahara K, Ishikawa T, Kishii M, Rao I M, Hash C T, George T S, Srinivasa Rao P, Nardi P, Bonnett D, Berry W, Suenaga K, Lata J C. Biological nitrification inhibition—a novel strategy to regulate nitrification in agricultural systems. Advances in Agronomy, 2012, 114 : 249–302
CrossRef Google scholar
[146]
Dietz M, Machill S, Hoffmann H C, Schmidtke K. Inhibitory effects of Plantago lanceolata L. on soil N mineralization. Plant and Soil, 2013, 368( 1−2): 445–458
CrossRef Google scholar
[147]
Gardiner C A, Clough T J, Cameron K C, Di H J, Edwards G R, de Klein C A M. Potential inhibition of urine patch nitrous oxide emissions by Plantago lanceolata and its metabolite aucubin. New Zealand Journal of Agricultural Research, 2018, 61( 4): 495–503
CrossRef Google scholar
[148]
Wu D, Cárdenas L M, Calvet S, Brüggemann N, Loick N, Liu S, Bol R. The effect of nitrification inhibitor on N2O, NO and N2 emissions under different soil moisture levels in a permanent grassland soil. Soil Biology & Biochemistry, 2017, 113 : 153–160
CrossRef Google scholar
[149]
Navarrete S, Kemp P D, Pain S J, Back P J. Bioactive compounds, aucubin and acteoside, in plantain (Plantago lanceolata L.) and their effect on in vitro rumen fermentation. Animal Feed Science and Technology, 2016, 222 : 158–167
CrossRef Google scholar
[150]
Office for National Statistics (ONS). Final UK greenhouse gas emissions national statistics: 1990–2017. UK: ONS, 2020. Available at UK Government website on June 30, 2020
[151]
Intergovernmental Panel on Climate Change (IPCC). Climate Change 2014: Synthesis Report. Contribution of Working Groups I, II and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change. Geneva: IPCC, 2014. Available on IPCC website March 21, 2021
[152]
Liu S, Proudman J, Mitloehner F M. Rethinking methane from animal agriculture. CABI Agriculture and Bioscience, 2021, 2( 1): 22
CrossRef Google scholar
[153]
Allen M R, Shine K P, Fuglestvedt J S, Millar R J, Cain M, Frame D J, Macey A H. A solution to the misrepresentations of CO2-equivalent emissions of short-lived climate pollutants under ambitious mitigation. NPJ Climate and Atmospheric Science, 2018, 1( 1): 16
[154]
Eggleston S, Buendia L, Miwa K, Ngara T, Tanabe K. 2006 IPCC Guidelines for National Greenhouse Gas Inventories. Japan: IGES, 2006
[155]
Aboagye I A, Beauchemin K A. Potential of molecular weight and structure of tannins to reduce methane emissions from ruminants: a review. Animals, 2019, 9( 11): 856
CrossRef Google scholar
[156]
Bodas R, Prieto N, García-González R, Andrés S, Giráldez F J, López S. Manipulation of rumen fermentation and methane production with plant secondary metabolites. Animal Feed Science and Technology, 2012, 176( 1−4): 78–93
CrossRef Google scholar
[157]
Martin C, Morgavi D P, Doreau M. Methane mitigation in ruminants: from microbe to the farm scale. Animal, 2010, 4( 3): 351–365
CrossRef Google scholar
[158]
Ramírez-Restrepo C A, Barry T N. Alternative temperate forages containing secondary compounds for improving sustainable productivity in grazing ruminants. Animal Feed Science and Technology, 2005, 120( 3−4): 179–201
CrossRef Google scholar
[159]
Bharanidharan R, Arokiyaraj S, Kim E B, Lee C H, Woo Y W, Na Y, Kim D, Kim K H. Ruminal methane emissions, metabolic, and microbial profile of Holstein steers fed forage and concentrate, separately or as a total mixed ration. PLoS One, 2018, 13( 8): e0202446
CrossRef Google scholar
[160]
Wallace R J. Antimicrobial properties of plant secondary metabolites. Proceedings of the Nutrition Society, 2004, 63( 4): 621–629
CrossRef Google scholar
[161]
Hatew B, Hayot Carbonero C, Stringano E, Sales L F, Smith L M J, Mueller-Harvey I, Hendriks W H, Pellikaan W F. Diversity of condensed tannin structures affects rumen in vitro methane production in sainfoin (Onobrychis viciifolia) accessions. Grass and Forage Science, 2015, 70( 3): 474–490
CrossRef Google scholar
[162]
Aboagye I A, Oba M, Castillo A R, Koenig K M, Iwaasa A D, Beauchemin K A. Effects of hydrolyzable tannin with or without condensed tannin on methane emissions, nitrogen use, and performance of beef cattle fed a high-forage diet. Journal of Animal Science, 2018, 96( 12): 5276–5286
CrossRef Google scholar
[163]
Chen L, Bao X, Guo G, Huo W, Xu Q, Wang C, Liu Q. Treatment of alfalfa silage with tannin acid at different levels modulates ensiling characteristics, methane mitigation, ruminal fermentation patterns and microbiota. Animal Feed Science and Technology, 2021, 278 : 114997
CrossRef Google scholar
[164]
Stewart E K, Beauchemin K A, Dai X, MacAdam J W, Christensen R G, Villalba J J. Effect of tannin-containing hays on enteric methane emissions and nitrogen partitioning in beef cattle. Journal of Animal Science, 2019, 97( 8): 3286–3299
CrossRef Google scholar
[165]
Niderkorn V, Copani G, Martin C, Maxin G, Torrent A, Anglard F, Rochette Y, Ginane C. Effects of including bioactive legumes in grass silage on digestion parameters, nitrogen balance and methane emissions in sheep. Grass and Forage Science, 2019, 74( 4): 626–635
CrossRef Google scholar
[166]
Sun X Z, Hoskin S O, Zhang G G, Molano G, Muetzel S, Pinares-Patiño C S, Clark H, Pacheco D. Sheep fed forage chicory (Cichorium intybus) or perennial ryegrass (Lolium perenne) have similar methane emissions. Animal Feed Science and Technology, 2012, 172( 3-4): 217–225
CrossRef Google scholar
[167]
Fraser M D, Fleming H R, Theobald V J, Moorby J M. Effect of breed and pasture type on methane emissions from weaned lambs offered fresh forage. Journal of Agricultural Science, 2015, 153( 6): 1128–1134
CrossRef Google scholar
[168]
Niderkorn V, Jayanegara A. Opportunities offered by plant bioactive compounds to improve silage quality, animal health and product quality for sustainable ruminant production: a review. Agronomy, 2021, 11( 1): 86
CrossRef Google scholar
[169]
Simon P L, de Klein C A M, Worth W, Rutherford A J, Dieckow J. The efficacy of Plantago lanceolata for mitigating nitrous oxide emissions from cattle urine patches. Science of the Total Environment, 2019, 691 : 430–441
CrossRef Google scholar
[170]
López-Aizpún M, Horrocks C A, Charteris A F, Marsden K A, Ciganda V S, Evans J R, Chadwick D R, Cárdenas L M. Meta-analysis of global livestock urine-derived nitrous oxide emissions from agricultural soils. Global Change Biology, 2020, 26( 4): 2002–2013
CrossRef Google scholar
[171]
Butterbach-Bahl K, Baggs E M, Dannenmann M, Kiese R, Zechmeister-Boltenstern S. Nitrous oxide emissions from soils: how well do we understand the processes and their controls. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences, 2013, 368( 1621): 20130122
CrossRef Google scholar
[172]
Dangal S R S, Tian H, Xu R, Chang J, Canadell J G, Ciais P, Pan S, Yang J, Zhang B. Global nitrous oxide emissions from pasturelands and rangelands: magnitude, spatiotemporal patterns, and attribution. Global Biogeochemical Cycles, 2019, 33( 2): 200–222
CrossRef Google scholar
[173]
Misselbrook T H, Powell J M, Broderick G A, Grabber J H. Dietary manipulation in dairy cattle: laboratory experiments to assess the influence on ammonia emissions. Journal of Dairy Science, 2005, 88( 5): 1765–1777
CrossRef Google scholar
[174]
van Groenigen J W, Kuikman P J, De Groot W J M, Velthof G L. Nitrous oxide emission from urine-treated soil as influenced by urine composition and soil physical conditions. Soil Biology & Biochemistry, 2005, 37( 3): 463–473
CrossRef Google scholar
[175]
Marsden K A, Lush L, Holmberg J A, Whelan M J, King A J, Wilson R P, Charteris A F, Cardenas L M, Jones D L, Chadwick D R. Sheep urination frequency, volume, N excretion and chemical composition: implications for subsequent agricultural N losses. Agriculture, Ecosystems & Environment, 2020, 302 : 107073
CrossRef Google scholar
[176]
Bristow A W, Whitehead D C, Cockburn J E. Nitrogenous constituents in the urine of cattle, sheep and goats. Journal of the Science of Food and Agriculture, 1992, 59( 3): 387–394
CrossRef Google scholar
[177]
Dijkstra J, Oenema O, van Groenigen J W, Spek J W, van Vuuren A M, Bannink A. Diet effects on urine composition of cattle and N2O emissions. Animal, 2013, 7(Suppl 2): 292–302
[178]
Gardiner C A, Clough T J, Cameron K C, Di H J, Edwards G R, de Klein C A M. Potential for forage diet manipulation in New Zealand pasture ecosystems to mitigate ruminant urine derived N2O emissions: a review. New Zealand Journal of Agricultural Research, 2016, 59( 3): 301–317
CrossRef Google scholar
[179]
Huyen N T, Desrues O, Alferink S J J, Zandstra T, Verstegen M W A, Hendriks W H, Pellikaan W F. Inclusion of sainfoin (Onobrychis viciifolia) silage in dairy cow rations affects nutrient digestibility, nitrogen utilization, energy balance, and methane emissions. Journal of Dairy Science, 2016, 99( 5): 3566–3577
CrossRef Google scholar
[180]
Intergovernmental Panel on Climate Change (IPCC). Chapter 11: N2O Emissions from Managed Soils, and CO2 Emissions from Lime and Urea Application In: 2006 IPCC Guidelines for National Greenhouse Gas Inventories. IPCC, 2006, 11.1–11.48
[181]
Cardenas L M, Misselbrook T M, Hodgson C, Donovan N, Gilhespy S, Smith K A, Dhanoa M S, Chadwick D. Effect of the application of cattle urine with or without the nitrification inhibitor DCD, and dung on greenhouse gas emissions from a UK grassland soil. Agriculture, Ecosystems & Environment, 2016, 235 : 229–241
CrossRef Google scholar
[182]
Misselbrook T, Fleming H, Camp V, Umstatter C, Duthie C A, Nicoll L, Waterhouse T. Automated monitoring of urination events from grazing cattle. Agriculture, Ecosystems & Environment, 2016, 230 : 191–198
CrossRef Google scholar
[183]
Tully K L, Abwanda S, Thiong’o M, Mutuo P M, Rosenstock T S. Nitrous oxide and methane fluxes from urine and dung deposited on Kenyan pastures. Journal of Environmental Quality, 2017, 46( 4): 921–929
CrossRef Google scholar
[184]
Chadwick D R, Cardenas L M, Dhanoa M S, Donovan N, Misselbrook T, Williams J R, Thorman R E, McGeough K L, Watson C J, Bell M, Anthony S G, Rees R M. The contribution of cattle urine and dung to nitrous oxide emissions: quantification of country specific emission factors and implications for national inventories. Science of the Total Environment, 2018, 635 : 607–617
CrossRef Google scholar
[185]
Forrestal P J, Krol D J, Lanigan G J, Jahangir M M R, Richards K G. An evaluation of urine patch simulation methods for nitrous oxide emission measurement. Journal of Agricultural Science, 2017, 155( 5): 725–732
CrossRef Google scholar
[186]
Hoogendoorn C J, Luo J, Lloyd-West C M, Devantier B P, Lindsey S B, Sun S, Pacheco D, Li Y, Theobald P W, Judge A. Nitrous oxide emission factors for urine from sheep and cattle fed forage rape (Brassica napus L.) or perennial ryegrass/white clover pasture (Lolium perenne L./Trifolium repens). Agriculture, Ecosystems & Environment, 2016, 227 : 11–23
CrossRef Google scholar
[187]
Hyde B P, Forrestal P J, Jahangir M M R, Ryan M, Fanning A F, Carton O T, Lanigan G J, Richards K G. The interactive effects of fertiliser nitrogen with dung and urine on nitrous oxide emissions in grassland. Irish Journal of Agricultural and Food Research, 2016, 55( 1): 1–9
CrossRef Google scholar
[188]
Krol D J, Carolan R, Minet E, McGeough K L, Watson C J, Forrestal P J, Lanigan G J, Richards K G. Improving and disaggregating N2O emission factors for ruminant excreta on temperate pasture soils. Science of the Total Environment, 2016, 568 : 327–338
CrossRef Google scholar
[189]
O’Connor P J, Minogue D, Lewis E, Lynch M B, Hennessy D. Applying urine collected from non-lactating dairy cows dosed with dicyandiamide to lysimeters and grass plots: Effects on nitrous oxide emissions, nitrate leaching and herbage production. Journal of Agricultural Science, 2016, 154( 4): 674–688
CrossRef Google scholar
[190]
Pelster D E, Gisore B, Goopy J, Korir D, Koske J K, Rufino M C, Butterbach-Bahl K. Methane and nitrous oxide emissions from cattle excreta on an East African grassland. Journal of Environmental Quality, 2016, 45( 5): 1531–1539
CrossRef Google scholar
[191]
Thomas B W, Gao X, Beck R, Hao X. Are distinct nitrous oxide emission factors required for cattle urine and dung deposited on pasture in western Canada. Environmental Science and Pollution Research International, 2017, 24( 33): 26142–26147
CrossRef Google scholar
[192]
Yamulki S, Jarvis S C, Owen P. Nitrous oxide emissions from excreta applied in a simulated grazing pattern. Soil Biology & Biochemistry, 1998, 30( 4): 491–500
CrossRef Google scholar
[193]
Balvert S F, Luo J, Schipper L A. Do glucosinolate hydrolysis products reduce nitrous oxide emissions from urine affected soil? Science of the Total Environment, 2017, 603–604: 370–380
[194]
Di H J, Cameron K C, Podolyan A, Edwards G R, de Klein C A M, Dynes R, Woods R. The potential of using alternative pastures, forage crops and gibberellic acid to mitigate nitrous oxide emissions. Journal of Soils and Sediments, 2016, 16( 9): 2252–2262
CrossRef Google scholar
[195]
Galbally I E, Meyer M C P, Wang Y P, Smith C J, Weeks I A. Nitrous oxide emissions from a legume pasture and the influences of liming and urine addition. Agriculture, Ecosystems & Environment, 2010, 136( 3−4): 262–272
CrossRef Google scholar
[196]
Marsden K A, Jones D L, Chadwick D R. The urine patch diffusional area: an important N2O source. Soil Biology & Biochemistry, 2016, 92 : 161–170
CrossRef Google scholar
[197]
Owens J, Clough T J, Laubach J, Hunt J E, Venterea R T. Nitrous oxide fluxes and soil oxygen dynamics of soil treated with cow urine. Soil Science Society of America Journal, 2017, 81( 2): 289–298
CrossRef Google scholar
[198]
Owens J, Clough T J, Laubach J, Hunt J E, Venterea R T, Phillips R L. Nitrous oxide fluxes, soil oxygen, and denitrification potential of urine- and non-urine-treated soil under different irrigation frequencies. Journal of Environmental Quality, 2016, 45( 4): 1169–1177
[199]
van der Weerden T J, Styles T M, Rutherford A J, de Klein C A M, Dynes R. Nitrous oxide emissions from cattle urine deposited onto soil supporting a winter forage kale crop. New Zealand Journal of Agricultural Research, 2017, 60( 2): 119–130
CrossRef Google scholar
[200]
Loick N, Dixon E, Abalos D, Vallejo A, Matthews P, McGeough K, Watson C, Baggs E M, Cardenas L M. “Hot spots” of N and C impact nitric oxide, nitrous oxide and nitrogen gas emissions from a UK grassland soil. Geoderma, 2017, 305 : 336–345
CrossRef Google scholar
[201]
Allen A G, Jarvis S C, Headon D M. Nitrous oxide emissions from soils due to inputs of nitrogen from excreta return by livestock on grazed grassland in the U.K. Soil Biology & Biochemistry, 1996, 28( 4−5): 597–607
CrossRef Google scholar
[202]
Liu R, Hayden H L, Hu H, He J, Suter H, Chen D. Effects of the nitrification inhibitor acetylene on nitrous oxide emissions and ammonia-oxidizing microorganisms of different agricultural soils under laboratory incubation conditions. Applied Soil Ecology, 2017, 119 : 80–90
CrossRef Google scholar
[203]
Edwards G R, Bryant R H, Smith N, Hague H, Taylor S, Ferris A, Farrell L. Milk production and urination behaviour of dairy cows grazing diverse and simple pastures. Proceedings of the New Zealand Society of Animal Production, 2015, 75 : 79–83
[204]
Woodward S L, Waugh C D, Roach C G, Fynn D, Phillips J. Are diverse species mixtures better pastures for dairy farming. Proceedings of the New Zealand Grassland Association, 2013, 75 : 79–84
CrossRef Google scholar
[205]
Woodward S L, Waghorn G C, Bryant M A, Benton A. Can diverse pasture mixtures reduce nitrogen losses? In: Proceedings of the 5th Australasian Dairy Science Symposium. Tallygaroopna: Australasian Dairy Science Symposium, 2012, 463–464
[206]
Coles G C. Anthelmintic resistance—looking to the future: a UK perspective. Research in Veterinary Science, 2005, 78( 2): 99–108
CrossRef Google scholar
[207]
ADAS. Economic Impact of Health and Welfare Issues in Beef Cattle and Sheep in England. UK: ADAS, 2011
[208]
Hoste H, Torres-Acosta J F J. Non chemical control of helminths in ruminants: adapting solutions for changing worms in a changing world. Veterinary Parasitology, 2011, 180( 1−2): 144–154
CrossRef Google scholar
[209]
Lazarus M, Rogers W P. The mode of action of phenothiazine as an anthelmintic; the uptake of 35S-labelled phenothiazine by the tissues of nematode parasites and their hosts. Australian Journal of Scientific Research, Series B: Biological Sciences, 1951, 4( 2): 163–179
CrossRef Google scholar
[210]
AHDB. Worm Control in Sheep for Better Returns. UK: AHDB Beef and Sheep, 2013
[211]
Marley C L, Cook R, Keatinge R, Barrett J, Lampkin N H. The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Veterinary Parasitology, 2003, 112( 1−2): 147–155
CrossRef Google scholar
[212]
Roeber F, Jex A R, Gasser R B. Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance—an Australian perspective. Parasites & Vectors, 2013, 6( 1): 153
CrossRef Google scholar
[213]
Knight T L, Moss R A, Fraser T J, Rowarth J S, Burton R N. Effect of pasture species on internal parasites of lambs. Proceedings of the New Zealand Grassland Association, 1996, 58 : 59–62
CrossRef Google scholar
[214]
French K E. Plant-based solutions to global livestock anthelmintic resistance. Ethnobiology Letters, 2018, 9( 2): 110–123
CrossRef Google scholar
[215]
Alomar D, Ruiz P, Balocchi O, Valenzuela G, Goic D. Finishing lambs on a chicory-plantain mixture or a temperate grass-based pasture: live weight gain and gastrointestinal parasitism. Agrarian Science and Research, 2018, 45( 1): 11–20
[216]
Corner-Thomas R A, Cranston L M, Kemp P D, Morris S T, Kenyon P R. The performance of single-rearing ewes and their lambs offered ryegrass pasture or herb−clover mix during lactation. New Zealand Journal of Agricultural Research, 2018, 61( 1): 67–80
CrossRef Google scholar
[217]
Somasiri S C, Kenyon P R, Kemp P D, Morel P C H, Morris S T. Mixtures of clovers with plantain and chicory improve lamb production performance compared to a ryegrass-white clover sward in the late spring and early summer period. Grass and Forage Science, 2016, 71( 2): 270–280
CrossRef Google scholar
[218]
Corner-Thomas R A, Cranston L M, Kemp P D, Morris S T, Kenyon P R. The influence of three herbage types on the liveweight change of twin-bearing hoggets and their lambs. New Zealand Journal of Agricultural Research, 2020, 63( 3): 365–378
CrossRef Google scholar
[219]
Kenyon P R, Morel P C H, Corner-Thomas R A, Perez H L, Somasiri S C, Kemp P D, Morris S T. Improved per hectare production in a lamb finishing system using mixtures of red and white clover with plantain and chicory compared to ryegrass and white clover. Small Ruminant Research, 2017, 151 : 90–97
CrossRef Google scholar
[220]
Taylor B R, Younie D, Matheson S, Coutts M, Mayer C, Watson C A, Walker R L. Output and sustainability of organic ley/arable crop rotations at two sites in northern Scotland. Journal of Agricultural Science, 2006, 144( 5): 435–447
CrossRef Google scholar
[221]
Agricultural Industries Confederation (AIC). AIC Fertilizer Statistics Report 2019. UK: AIC, 2019
[222]
Cougnon M, Van Den Berge K, D’Hose T, Clement L, Reheul D. Effect of management and age of ploughed out grass-clover on forage maize yield and residual soil nitrogen. Journal of Agricultural Science, 2018, 156( 6): 748–757
CrossRef Google scholar
[223]
Alloway B J. Micronutrients and Crop Production: An Introduction. In: Alloway B J, eds. Micronutrient deficiencies in global crop production. Dordrecht: Springer, 2008, 1–39
[224]
Gupta U C, Wu K, Liang S. Micronutrients in soils, crops, and livestock. Earth Science Frontiers, 2008, 15( 5): 110–125
CrossRef Google scholar
[225]
Ritchie H, Reay D S, Higgins P. Quantifying, projecting, and addressing India’s hidden hunger. Frontiers in Sustainable Food Systems, 2018, 2 : 11
CrossRef Google scholar
[226]
Fisher G E J. Micronutrients and animal nutrition and the link between the application of micronutrients to crops and animal health. Turkish Journal of Agriculture and Forestry, 2008, 32( 3): 221–233
[227]
Lindström B E M, Frankow-Lindberg B E, Dahlin A S, Wivstad M, Watson C A. Micronutrient concentrations in common and novel forage species and varieties grown on two contrasting soils. Grass and Forage Science, 2013, 68( 3): 427–436
CrossRef Google scholar
[228]
Pirhofer-Walzl K, Søegaard K, Høgh-Jensen H, Eriksen J, Sanderson M A, Rasmussen J, Rasmussen J. Forage herbs improve mineral composition of grassland herbage. Grass and Forage Science, 2011, 66( 3): 415–423
CrossRef Google scholar
[229]
Smith L G, Kirk G J D, Jones P J, Williams A G. The greenhouse gas impacts of converting food production in England and Wales to organic methods. Nature Communications, 2019, 10( 1): 4641
CrossRef Google scholar

Acknowledgements

This work was supported by funding provided by the UK Biotechnology and Biological Sciences Research Council under the Sustainable Agriculture Research and Innovation Club (SARIC) program (BB/R021716/1). We thank the two anonymous reviewers for their extremely helpful comments that helped to improve this manuscript.

Compliance with ethics guidelines

Emily C. Cooledge, David R. Chadwick, Lydia M. J. Smith, Jonathan R. Leake, and Davey L. Jones declare that they have no conflicts of interest or financial conflicts to disclose. This article does not contain any study with human or animal subjects performed by any of the authors.

RIGHTS & PERMISSIONS

The Author(s) 2022. Published by Higher Education Press. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0)
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