Animal fertility and longevity

In a self-replacing New Zealand flock of 1000 ewes, Cruickshank et al. (Reference Cruickshank, Thomson and Muir2008) found that lambing replacements as yearlings (hoggets) instead of waiting to lamb them later (as two-tooth ewes) had the greatest potential for reducing enteric CH₄ emissions (Table 1). This strategy maximized lamb output from the maintenance costs of the existing ewes. Similar findings in the direction and magnitude of change were modelled in a study by ADAS (Reference Rees and Philips2010), suggesting that lambing at 12 months rather than 2 years could reduce CH₄ and N₂O emissions by 9·4 kg CO₂e/kg of carcase meat. In the self-replacing Australian flocks modelled by Alcock & Hegarty (Reference Alcock and Hegarty2011), mating replacements at 7 months was estimated to reduce enteric CH₄ emissions by 12% per kg of LW lamb produced. However, in their second and third sheep enterprise types, replacements were not home-reared but brought in 2 weeks before mating. Consequently, mating at 7 months increased enteric CH₄ emissions between 3 and 9% per kg LW lamb produced. In these scenarios there was no unproductive young stock on farm and mating at an earlier age only served to reduce lambing percentages and growth rates.

The Institute of Biological, Environmental and Rural Studies et al. (2011b) found selection for ewe-litter size to be the genetic trait with the greatest stand-alone potential for emission reduction in Welsh flocks over a 10-year period. Similar strategies of increasing scanning percentage and the number of lambs weaned per ewe resulted in substantial enteric CH₄ savings of 3–4 and 7·8%, respectively (Cruickshank et al. Reference Cruickshank, Thomson and Muir2008; Alcock & Hegarty Reference Alcock and Hegarty2011). Increasing ewe longevity and decreasing lamb mortality also have potential to reduce lamb production emissions.

Animal growth rates and feed

In each of their three modelled enterprise types (Table 1) Alcock & Hegarty (Reference Alcock and Hegarty2011) found that production and creep feeding to finish lambs earlier had the greatest potential to reduce enteric CH₄ per kg of LW lamb produced; however, their study only considered enteric CH₄ emissions and did not consider the emissions burden of grain production. The effect on emissions of genetic selection for faster growth rate in lambs is dependent on whether or not this also results in a correlated increase in ewe mature weight. The Institute of Biological, Environmental and Rural Studies et al. (2011b) estimated that selection for lamb growth over 10 years in Welsh hill flocks would decrease enteric CH₄ emissions by 1·3% with no change in ewe weight, and increase them by 0·4% if ewe weight increased in synchrony. It is reported that improvements in lamb growth rates were behind most of the genetic-related reduction in GHG emissions in the UK sheep industry in the last 20 years (Genesis Faraday 2008). However, the net benefit was constrained by the increased emissions associated with the higher mature weights of the ewes. Net N₂O emissions demonstrated a marginal increase over time as a result of faster lamb growth rates, underlining the importance of incorporating all GHGs in any emissions calculation.

While the efficiency of feed use is widely used for selective breeding in other livestock species, limited use has been made of traits such as RFI in the ruminant industry (Genesis Faraday 2008; Wall et al. Reference Wall, Simm and Moran2010). Studies have demonstrated that cattle with lower RFI have reduced dry matter intake (DMI) and may also have lower daily rates of CH₄ production (Nkrumah et al. Reference Nkrumah, Okine, Mathison, Schmid, Li, Basarab, Price, Wang and Moore2006; Hegarty et al. Reference Hegarty, Goopy, Herd and Mccorkell2007). The modelled sheep flock scenarios of Alcock & Hegarty (Reference Alcock and Hegarty2011) found selection of sheep for lower RFI to be the most promising genetic improvement option for reducing enteric CH₄ emissions. If achieved, low RFI animals will provide a mitigation option suited to both intensive and extensive systems (Waghorn & Hegarty Reference Waghorn and Hegarty2011).

There is increasing interest in breeding directly for CH₄-reducing traits and feed nitrogen conversion efficiency (Wall et al. Reference Wall, Bell, Simm, Rowlinson, Steele and Nefzaoui2008; Keogh & Cottle Reference Keogh and Cottle2009; Hegarty & McEwan Reference Hegarty and Mcewan2010). Inter-sheep variation was estimated to be responsible for 70–80% of the differences in CH₄ emissions per unit of feed intake recorded from livestock fed the same diet in large-scale experiments (O'Hara et al. Reference O'hara, Freney and Ulyatt2003). Persistent variation in CH₄ emissions between sheep has been recorded under grazing conditions (Pinares-Patino et al. Reference Pinares-Patino, Ulyatt, Lassey, Barry and Holmes2003). Making use of this variation in breeding schemes is contingent upon the heritability of CH₄ traits, and the repeatability of this variation for different age classes and diets (Hegarty & McEwan Reference Hegarty and Mcewan2010).

Animal health

Improvements to animal health present opportunities to improve productivity and fertility by reducing culling rates and the subsequent number of replacements needed to maintain maternal flock size (Wall et al. Reference Wall, Simm and Moran2010). Stott et al. (Reference Stott, Macleod and Moran2010) estimated that prophylactic disease treatment in a hypothetical extensive sheep farm would reduce overall CH₄ emissions by 28%.

Animal nutrition

Nutritional strategies for reducing emissions from sheep target the inefficient use of dietary nitrogen and the loss of feed energy as CH₄. Between 0·75 and 0·95 of ingested nitrogen is excreted (Eckard et al. Reference Eckard, Grainger and de Klein2010), and gross feed energy intake lost as CH₄ ranges from 0·02 to 0·15 (Weiske Reference Weiske2005; Lassey Reference Lassey2007; Hopkins & Lobley Reference Hopkins and Lobley2009; Eckard et al. Reference Eckard, Grainger and de Klein2010).

Enteric methanogenesis

The volume of CH₄ produced during digestion depends on intake levels, diet composition and the rate and extent of digestion by microflora (Weiske Reference Weiske2005; PGgRc 2007). Typically, forages of high fibre or low digestibility that have a long residence time in the rumen will tend to produce high levels of CH₄ (PGgRc 2007). Models suggest that as sheep DMI increases LW gain (LWG) and daily CH₄ also increase, the overall result of which is a decrease in CH₄ production per kg LWG (Fig. 2) (Hegarty et al. Reference Hegarty, Alcock, Robinson, Goopy and Vercoe2010). As diet digestibility increases, CH₄/kg LWG decreases because of an underlying increase in LWG (Fig. 2) (Hegarty et al. Reference Hegarty, Alcock, Robinson, Goopy and Vercoe2010).

Fig. 2.

The modelled relationship between DMI and CH₄ production per kg of LWG at three different levels of diet digestibility (▼65%, ○75%, ●85%) for a 30 kg Border Leicester × Merino wether offered ad libitum access to roughage (adapted from Hegarty et al. Reference Hegarty, Alcock, Robinson, Goopy and Vercoe2010).

Increasing feed intake and digestibility can be achieved through replacing structural carbohydrates (cellulose and hemicelluloses) in the diet with non-structural carbohydrates (starch and sugars) (O'Mara et al. Reference O'mara, Beauchemin, Kreuzer, Mcallister, Rowlinson, Steele and Nefzaoui2008), or through altering forage type. Feeding higher starch, such as grain-based diets, not only increases diet digestibility and feed intake but also favours propionate production in the rumen providing an alternative pathway to methanogenesis for hydrogen use (Eckard et al. Reference Eckard, Grainger and de Klein2010; Martin et al. Reference Martin, Morgavi and Doreau2010). Benchaar et al. (Reference Benchaar, Pomar and Chiquette2001) estimated that increasing the proportion of concentrates in the diet from 0 to 0·20 would reduce CH₄ production in ruminants as a proportion of gross energy intake (GEI) by 3%. However, in a meta-analysis of 87 studies, Sauvant & Giger-Reverdin (Reference Sauvant, Giger-Reverdin, Ortigues-Marty, Miraux and Brand-Williams2007) found CH₄ losses as a proportion of GEI to be relatively constant for diets containing 0·30–0·40 concentrate, suggesting higher proportions of concentrates are needed to gain any mitigation benefit. Dragosits et al. (Reference Dragosits, Chadwick, Del Prado, Scholefield, Mills, Crompton, Newbold, Crighton and Audsley2008) suggested that feeding a high starch diet nationally to sheep flocks would only reduce CH₄ emissions by 1%. Production emissions associated with the grain and the baseline productivity and emissions of the farming system will determine the net GHG impacts of increasing the quantity of grain fed. The applicability of feeding high-concentrates diets is restricted to more intensive production systems.

In other research areas, the breeding of grasses and legumes with high water-soluble carbohydrate (WSC) content may potentially reduce direct CH₄ emissions from both intensive and extensive farming systems. For instance, IBERS (2010) found that lambs reared on a mix of three high WSC grasses produced up to 25% less CH₄/kg LWG compared with the control diet of conventional (normal WSC) grass. This was possibly due to increased ruminal bacterial numbers in lambs on the high WSC diet, leading to greater capture of metabolic hydrogen and reducing availability for methanogenic archaea. Other forage-based options include grazing animals on less mature herbages (Deighton et al. Reference Deighton, Wims, O'loughlin, Lewis and O'donovan2010) and feeding ensiled forages (Lima et al. Reference Lima, Díaz, Castro and Fievez2011). Results from studies investigating the emission reduction benefits of feeding or grazing leguminous forages and pastures have been inconclusive. It is thought that legumes have a faster rate of ruminal breakdown than grasses and consequently a higher voluntary intake, lowering CH₄ yields/kg of DMI (Rochon et al. Reference Rochon, Doyle, Greef, Hopkins, Molle, Sitzia, Scholefield and Smith2004; Hammond et al. Reference Hammond, Hoskin, Burke, Waghorn, Koolaard and Muetzel2011). Waghorn et al. (Reference Waghorn, Tavendale and Woodfield2002) found significant promise for mitigating emissions through changing forage type with a doubling of CH₄ emissions/kg DMI over a range of fresh forage diets, ranging from 11·5 g CH₄/kg on a ryegrass and white clover pasture to 25·7 g CH₄/kg on a diet of lotus forage. Knight et al. (Reference Knight, Molano, Nichols and Clark2007) also found significant differences in CH₄ yield/kg DMI through varying legume species and proportion in the diet. In contrast, two separate feeding trials concluded that CH₄ yield is not influenced by forage species or maturity and that ‘there are no simple relationships between chemical components of fresh forages and CH₄ yield’ (Hammond et al. Reference Hammond, Hoskin, Burke, Waghorn, Koolaard and Muetzel2011; Sun et al. Reference Sun, Hoskin, Zhang, Molano, Muetzel, Pinares-Patiño, Clark and Pacheco2012).

Nitrogen conversion efficiency

Low efficiency of dietary nitrogen use in ruminants and subsequent high urea nitrogen losses are primarily attributed to imbalances in dietary protein and energy (non-structural carbohydrates), and feeding regimes that contain nitrogen in excess of dietary requirements (O'Hara et al. Reference O'hara, Freney and Ulyatt2003; Moorby et al. Reference Moorby, Chadwick, Scholefield, Chambers and Williams2007; Prosser et al. Reference Prosser, Bowes, Thomas, Stebbings, Skates, Leroux, Williams, Bevan and Davies2008). Decreasing the quantity of nitrogen excreted would be expected to reduce N₂O losses, both directly from soils and indirectly when leached nitrate is converted to N₂O in water bodies or when volatilized ammonia is deposited on the land.

Increasing the efficiency of nutrient use entails correctly formulating animal diets, matching feed provision more closely to animal nutrient requirement, which requires characterization of feed composition and nutritional advice (Moorby et al. Reference Moorby, Chadwick, Scholefield, Chambers and Williams2007; Prosser et al. Reference Prosser, Bowes, Thomas, Stebbings, Skates, Leroux, Williams, Bevan and Davies2008). This can be achieved by avoiding excess nitrogen diets and by increasing the proportion of dietary nitrogen utilized through feeding a diet balanced in energy and protein. Pastures and fresh forages typically contain high levels of protein, in excess of available energy, resulting in the excretion of ammonia (Abberton et al. Reference Abberton, Marshall, Humphreys, Macduff, Rowlinson, Steele and Nefzaoui2008; Eckard et al. Reference Eckard, Grainger and de Klein2010; Luo et al. Reference Luo, de Klein, Ledgard and Saggar2010). Lowering the crude protein content of the diet is known to reduce dietary nitrogen losses (Schils et al. Reference Schils, Eriksen, Ledgard, Vellinga, Kuikman, Luo, Petersen and Velthof2011), although careful management is required to ensure maintenance of yield (Nielsen et al. Reference Nielsen, Kristensen, Nørgaard and Hansen2003). For example, Seip et al. (Reference Seip, Breves, Isselstein and Abel2011) showed that supplementing grass and legume silage of adult sheep with barley reduced urinary nitrogen excretion in an unfertilized grassland system. Numerous examples exist of the efficacy of this strategy in dairy systems (Luo et al. Reference Luo, de Klein, Ledgard and Saggar2010; Schils et al. Reference Schils, Eriksen, Ledgard, Vellinga, Kuikman, Luo, Petersen and Velthof2011). Increasing the carbohydrate content of the diet is the alternative option for balancing energy and protein, e.g. balancing high protein forages with high energy supplements (O'Hara et al. Reference O'hara, Freney and Ulyatt2003; Eckard et al. Reference Eckard, Grainger and de Klein2010) or through feeding high WSC grasses (Merry et al. Reference Merry, Lee, Davies, Dewhurst, Moorby, Scollan and Theodorou2006). Feeding trials have shown that high WSC grasses can reduce nitrogen excretion by up to 24% whilst also increasing DMI and improving LWG (IGER 2005).

Feed additives and ruminal manipulation

Many studies have tested the effects of a range of dietary additives and alternative methods of rumen manipulation on enteric CH₄ and dietary nitrogen losses (Table 2). The rumen-based CH₄ mitigation strategies listed in Table 2 have several different modes of action. Feed additives such as condensed tannins and bacteriocins directly inhibit methanogenesis (Kreuzer et al. Reference Kreuzer, Kirchgessner and Müller1986; O'Mara et al. Reference O'mara, Beauchemin, Kreuzer, Mcallister, Rowlinson, Steele and Nefzaoui2008). Others, such as organic acids and probiotics, provide an alternative sink or pathway for H₂ use in the rumen, displacing CH₄ production (O'Mara et al. Reference O'mara, Beauchemin, Kreuzer, Mcallister, Rowlinson, Steele and Nefzaoui2008; Martin et al. Reference Martin, Morgavi and Doreau2010); while plant saponins and ionophores eliminate rumen protozoa that are thought to have a symbiotic relationship with some methanogenic archaea (Kreuzer et al. Reference Kreuzer, Kirchgessner and Müller1986; Kumar et al. Reference Kumar, Puniya, Puniya, Dagar, Sirohi, Singh and Griffith2009; Eckard et al. Reference Eckard, Grainger and de Klein2010). A number of the strategies act to reduce emissions in multiple ways. For example, ionophores are known to improve feed conversion efficiency (Grainger & Beauchemin Reference Grainger and Beauchemin2011). Fat supplementation may reduce nitrogen losses and CH₄ emissions concomitantly (Machmüller et al. Reference Machmüller, Ossowski and Kreuzer2006). Oil supplementation may improve digestibility and energy use efficiency (Klevenhusen et al. Reference Klevenhusen, Zeitz, Duval, Kreuzer and Soliva2011).

Table 2.

Dietary and ruminal manipulation strategies for emissions mitigation

Research interest appears to be focusing on the use of natural feed additives such as tannins, essential oils and lipids and on the novel approaches of vaccination and defaunation. Supplementation with lipids is one strategy at the forefront of dietary mitigation research. Martin et al. (Reference Martin, Morgavi and Doreau2010) recently reviewed the results of 67 dietary supplementation experiments from the literature, concluding that overall, for sheep and cattle combined, with every 1% addition of fat, mean CH₄ emissions decreased by 3·8%. Martin et al. (Reference Martin, Morgavi and Doreau2010) also found that medium chain fatty acids (most frequently coconut oil) showed the greatest mitigation potential. In a similar study, a meta-analysis of studies limiting supplementation within the practical range of feeding, Grainger & Beauchemin (Reference Grainger and Beauchemin2011) found a slightly greater decrease in cattle CH₄ emissions/g of fat added to the diet. In contrast to Martin et al. (Reference Martin, Morgavi and Doreau2010), Grainger & Beauchemin (Reference Grainger and Beauchemin2011) found that fatty acid type had no effect on CH₄ yield. Nor did the form of fat added (oil v. oilseed) or fat source (e.g. coconut v. sunflower). Grainger & Beauchemin (Reference Grainger and Beauchemin2011) suggested that their results were more robust than those of Martin et al. (Reference Martin, Morgavi and Doreau2010) because they were based on a covariance analysis of CH₄ yield data as opposed to average data, and also because the dataset used by Grainger & Beauchemin (Reference Grainger and Beauchemin2011) was restricted to practical dietary fat levels. Grainger & Beauchemin (Reference Grainger and Beauchemin2011) also highlighted a significant difference in the relationship between dietary fat and CH₄ yield among beef, dairy and sheep, finding that more data are needed to give an accurate assessment of the effect of fat supplementation in sheep. In a recent study in Wales, IBERS (2010) measured CH₄ production and nitrogen retention in store lambs fed diets supplemented with linseed oil or a novel high fat naked oat. Linseed oil supplementation reduced CH₄ emissions by 22% and the naked oats by 33% compared with the control diet. Neither supplements affected nitrogen retention significantly.

Lipid supplementation research highlights the uncertainties that persist in the application of many dietary mitigation strategies, e.g. optimal lipid source, dosage level, dependence on diet type, transfer to animal products and possible human health impacts and limited sheep specific data (Hook et al. Reference Hook, Wright and Mcbride2010; Martin et al. Reference Martin, Morgavi and Doreau2010). Despite these uncertainties, implementation is beginning to be considered including using drinking water to administer supplements in extensive grazing systems and the identification of high fatty acid content grasses (Grainger & Beauchemin Reference Grainger and Beauchemin2011).

Soil moisture

Several studies have demonstrated that N₂O emissions and overall nitrogen losses are accentuated in high moisture conditions. For example, Chambers et al. (Reference Chambers, Smith and Pain2000) showed that NO₃⁻ leaching from the application of organic manure to grassland sites was greatest when applied in the autumn and winter. Cardenas et al. (Reference Cardenas, Thorman, Ashlee, Butler, Chadwick, Chambers, Cuttle, Donovan, Kingston, Lane, Dhanoa and Scholefield2010) reported far higher N₂O emissions from fertilized grazed grasslands in the West of the UK compared with the East, which they attributed to the wetter conditions in the West. Frequently, N₂O emissions positively correlate with soil water-filled pore space (WFPS), with maximum emissions occurring at 0·60–80 m³ water/m³ pore space (Fig. 4) (Clayton et al. Reference Clayton, Mctaggart, Parker, Swan and Smith1997; Jones et al. Reference Jones, Rees, Skiba and Ball2007; Rafique et al. Reference Rafique, Hennessy and Kiely2011). In poorly aerated soils (WFPS >0·60 m³/m³) denitrification becomes dominant, and >0·80 m³/m³ N₂ becomes the dominant product of denitrification (Dalal et al. Reference Dalal, Wang, Robertson and Parton2003). Flechard et al. (Reference Flechard, Ambus, Skiba, Rees, Hensen, Van Amstel, van den Pol-van Dasselaar, Soussana, Jones, Clifton-Brown, Raschi, Horvath, Neftel, Jocher, Ammann, Leifeld, Fuhrer, Calanca, Thalman, Pilegaard, Di Marco, Campbell, Nemitz, Hargreaves, Levy, Ball, Jones, Van De Bulk, Groot, Blom, Domingues, Kasper, Allard, Ceschia, Cellier, Laville, Henault, Bizouard, Abdalla, Williams, Baronti, Berretti and Grosz2007) found that N₂O emission factors from European grassland sites were highest for soils where WFPS mostly remained in what they called the ‘optimum range for N₂O emissions of 60–90%’.

Fig. 4.

Relationship between WFPS in soil and the relative fluxes of N₂O (●) and N₂ (○) from both nitrification and denitrification within sheep pasture systems (adapted from Dalal et al. Reference Dalal, Wang, Robertson and Parton2003).

Water table management

In many northern European countries, water table manipulation through soil drainage presents a practical option for controlling WFPS in sheep-grazed grasslands (Dobbie & Smith Reference Dobbie and Smith2006). A small number of studies have investigated the relationship between water table level and N₂O emissions in the field (Table 3). Dobbie & Smith (Reference Dobbie and Smith2006) and Kammann et al. (Reference Kammann, Grünhage, Müller, Jacobi and Jäger1998) demonstrated a significant decrease in N₂O emissions as water table depth below the soil surface increased. As the water table falls, WFPS and soil moisture decrease, leading to an increase in aeration in the upper soil, which in turn reduces the presence of anaerobic zones for denitrification and enhances root growth leading to better fertilizer N use efficiency. Dobbie & Smith (Reference Dobbie and Smith2006) concluded that draining grasslands to keep the water table more than 0.35 m below the surface when nitrogen is available for denitrification could cut N₂O emissions by 50% during the growing season. However, mitigation through water table management is complex (Fig. 4). If for example, soil is drained below saturation but WFPS remains above 0·40 m³/m³, N₂O emissions could potentially increase (Eckard et al. Reference Eckard, Grainger and de Klein2010). The WFPS values at which nitrification and denitrification dominate N₂O production are site- and soil-specific (Müller & Sherlock Reference Müller and Sherlock2004). Although drainage can effectively reduce CH₄ and N₂O emissions from mineral soils, the case for GHG is more complicated for organic (peat) soils. Draining peat soils may reduce CH₄ and N₂O; however, this can be negatively offset by increased CO₂ emissions as the increased oxygenation stimulates aerobic mineralization of soil organic matter (e.g. van Beek et al. Reference Van Beek, Pleijter, Jacobs, Velthof, Van Groenigen and Kuikman2010; Table 3). The overall GHG balance of improved drainage is also uncertain due to the increased potential for nitrate leaching (and increased indirect N₂O emissions) (Smith et al. Reference Smith, Martino, Cai, Gwary, Janzen, Kumar, Mccarl, Ogle, O'mara, Rice, Scholes, Sirotenko, Howden, Mcallister, Pan, Romanenkov, Schneider, Towprayoon, Wattenbach and Smith2008; Eckard et al. Reference Eckard, Grainger and de Klein2010).

Table 3.

The influence of water table depth on N₂O emissions from grassland soils in Western Europe

Soil compaction

The deposition of excreta on waterlogged soils increases nitrogen supply for denitrification and subsequent emissions may be exacerbated by soil compaction through animal trafficking. The likelihood and severity of compaction increases at elevated soil moisture content creating anaerobic sites in the soil (Rafique et al. Reference Rafique, Hennessy and Kiely2011). In separate field experiments, Sitaula et al. (Reference Sitaula, Hansen, Sitaula and Bakken2000), Van Groenigen et al. (Reference Van Groenigen, Velthof, Van Der Bolt, Vos and Kuikman2005) and Bhandral et al. (Reference Bhandral, Saggar, Bolan and Hedley2007) demonstrated that soil compaction increased average N₂O emissions from agricultural soils receiving urine and/or fertilizer by a factor of 1·7, 2·2 and 7, respectively, compared with no compaction. On an intra-farm scale, Matthews et al. (Reference Matthews, Chadwick, Retter, Blackwell and Yamulki2010) showed that poached land surrounding water troughs on beef and sheep farms can have significantly higher N₂O emissions rates than surrounding managed pasture. Information on the impact of sheep grazing on soil compaction and subsequent N₂O emissions is scarce (Saggar et al. Reference Saggar, Hedley, Giltrap and Lambie2007). While the hoof pressures of sheep are lower than those of cows (83 kPa compared with 192 kPa), there is evidence that infiltration in soil decreases with increased sheep-stocking rate (Willatt & Pullar Reference Willatt and Pullar1984). Decreased infiltration indicates that soil is compacted. Betteridge et al. (Reference Betteridge, Mackay, Shepherd, Barker, Budding, Devantier and Costall1999) found that the effect of a severe short-term treading event on wet hill soils was greater for cattle than sheep stocked at the same metabolic LW/ha, but they also indicated that at soil water contents above the critical water content for compaction the ratio of soil compaction to deformation may be greater for sheep than for cattle. Many opportunities to reduce soil compaction on pastures are already well established as best practice for limiting poaching, water pollution and safeguarding animal welfare when out-wintering stock. These include sale of barren ewes to reduce stocking rates in winter, and the use of electric fences to control access to forage crops and boggy areas.

There has been little follow-through research on the impact of these measures on N₂O emissions. Restricted grazing on wet pastures (e.g. through housing animals) may reduce N₂O emissions provided that collected excreta is spread uniformly (Hopkins & Lobley Reference Hopkins and Lobley2009). The extent to which this mitigation measure is relevant to sheep farms will depend on the stocking rate and current winter housing and grazing practice. Schils et al. (Reference Schils, Verhagen, Aarts and Šebek2005) modeled the GHG budget of reducing grazing time on a case study dairy farm. Reduced N₂O emissions from excreta were offset by an increase in CH₄ emissions from manure storage, suggesting that restricted grazing may not offer mitigation potential at a whole farm level. Luo et al. (Reference Luo, de Klein, Ledgard and Saggar2010) suggested that for grazed winter forage crops, the method of tillage used to establish the crop will impact on the subsequent soil compaction by grazing animals and therefore N₂O emission. Direct drilling to establish forage crops was suggested as a means of emissions reduction.

Reducing stocking rates also holds potential for emissions reduction. Howden et al. (Reference Howden, White and Bowman1996) found that CO₂e emissions/ha grassland increased linearly with stocking rate at low to moderate stocking rates (from 2 to 8 or 9 ewes/ha), but remained constant at higher stocking rates from 10 to 14 ewes/ha, although the causality of this relationship was not explored. Rafique et al. (Reference Rafique, Hennessy and Kiely2011) found that intensively grazed grasslands produced N₂O fluxes up to three times higher per hour than their extensive counterparts, which they attributed to greater urine and dung excretion and soil compaction on intensive sites.

Fertilizer and nutrient management

Soil moisture should also be taken into account when planning fertilizer applications. High WFPS, low oxygen conditions promote denitrification when carbon and NO₃⁻ supplies are non-limiting, indicating that fertilizer applications should be avoided in late autumn and winter and early spring. In conditions where denitrification predominates, such as during cool, wet months, N₂O emissions may be lower from the application of a urea-based fertilizer than a NO₃⁻ -based fertilizer. Conversely, emissions may be expected to be higher from ammonium rather than NO₃⁻ -based fertilizers in drier soil conditions favouring nitrification (Eckard et al. Reference Eckard, Johnson and Chapman2006).

Other fertilizer management opportunities for emissions reduction limit the supply of nitrogen feedstock for N₂O producing soil microbes. When fertilizer applications exceed pasture or forage requirements the nitrogen surplus can be immobilized, becoming part of the organic nitrogen pool or lost through the pathways previously defined. As nitrogen supply exceeds the requirements of the pasture the efficiency of use for growth declines (Eckard et al. Reference Eckard, Johnson and Chapman2006). Pasture derived emissions of N₂O are positively correlated with nitrogen input (Jones et al. Reference Jones, Rees, Skiba and Ball2007; Cardenas et al. Reference Cardenas, Thorman, Ashlee, Butler, Chadwick, Chambers, Cuttle, Donovan, Kingston, Lane, Dhanoa and Scholefield2010; Rafique et al. Reference Rafique, Hennessy and Kiely2011). Adoption of a fertilizer recommendation system, which includes a soil and plant nutrient analysis, would ensure the optimization of nutrient supply (O'Hara et al. Reference O'hara, Freney and Ulyatt2003; Moorby et al. Reference Moorby, Chadwick, Scholefield, Chambers and Williams2007). This would also account for the nitrogen content of the soil and any applied manure (as many farmers fail to account for the nutrient content of organic manures when applying fertilizers; Jones et al. Reference Jones, Rees, Skiba and Ball2007). Proper maintenance and calibration of spreader equipment will improve targeting of nutrients to crop needs. Precision in fertilizer timing can also reduce nitrogen losses. These are simple approaches including ensuring application coincides with periods of rapid crop growth; minimizing delays between application and crop uptake and splitting applications into several smaller applications to improve efficiency of nitrogen uptake (Eckard et al. Reference Eckard, Johnson and Chapman2006; Jones et al. Reference Jones, Rees, Skiba and Ball2007).

Pasture renovation and plant selection

Temporary pastures on sheep farms are periodically ploughed and either reseeded to grass to improve sward productivity or planted with a forage crop. Pasture renovation has been associated with temporary, but significant, increases in soil N₂O emissions (Davies et al. Reference Davies, Smith and Vinten2001; Estavillo et al. Reference Estavillo, Merino, Pinto, Yamulki, Gebauer, Sapek and Corré2002; Vellinga et al. Reference Vellinga, Van Den Pol-Van Dasselaar and Kuikman2004). Velthof et al. (Reference Velthof, Hoving, Dolfing, Smit, Kuikman and Oenema2010) found that renovation of intensively managed fertilized grasslands increased N₂O emissions by an average of 1·8–3 times compared with non-reseeded control grasslands. Possible explanations include increased mineral nitrogen content of soil through the incorporation of crop residues, mineralization of N from soil organic matter and limited uptake of nitrogen by crops post-ploughing. Careful management of pasture ploughing (i.e. method and timing) may reduce emissions, although the number of studies supporting this is limited. Contrary to what might be expected, MacDonald et al. (Reference Macdonald, Rochette, Chantigny, Angers, Royer and Gasser2011) showed that full inversion tillage (FIT) reduced N₂O emissions relative to soil NO₃⁻ levels by two or three times compared with a no-till/glyphosate (chemical fallow) regime on poorly drained grassland soils. They suggested that FIT may reduce N₂O emissions in a wet year by placing the most nutrient-rich soil surface at depth where lower oxygen levels lead to the complete reduction of NO₃⁻ to N₂. In the case of chemical fallow, carbon and nitrogen remain available close to the surface, where higher oxygen concentrations may hinder the full conversion of N₂O to N_2. Similarly Velthof et al. (Reference Velthof, Hoving, Dolfing, Smit, Kuikman and Oenema2010) reported lower N₂O emissions from ploughed grassland than grassland renovated through chemical destruction of the sward, perhaps due to increased aeration of soils through ploughing. Grassland renovation in spring as opposed to autumn may reduce total nitrogen losses from soil because the new sward has a higher capacity to take up nitrogen during the growing season (Vellinga et al. Reference Vellinga, Van Den Pol-Van Dasselaar and Kuikman2004; Velthof et al. Reference Velthof, Hoving, Dolfing, Smit, Kuikman and Oenema2010). Davies et al. (Reference Davies, Smith and Vinten2001) have also suggested that avoiding grazing and fertilizer application on pastures prior to ploughing can reduce emissions, however, further work is needed to quantify the overall benefits of this.

Pasture renovation provides an opportunity to select plant varieties that may reduce nitrogen losses over the long term. Mixed pastures of legumes and grass typically fix between 100 and 250 kg/N/ha/year, reducing the need for mineral fertilizer use (Rochon et al. Reference Rochon, Doyle, Greef, Hopkins, Molle, Sitzia, Scholefield and Smith2004). In a life-cycle analysis model of lowland and upland sheep production systems in England, lamb production emissions from fertilized grasslands have been estimated to be 14·6 kg CO₂e/kg of meat compared with 13·1 kg CO₂e/kg produced from an unfertilized grass-clover sward (EBLEX 2009). However, some uncertainty relating to the mitigation potential of clover arises from the possibility that NO₃⁻ and dissolved organic nitrogen leaching may increase with the legume content of the sward and the level of nitrogen fixation (Rochon et al. Reference Rochon, Doyle, Greef, Hopkins, Molle, Sitzia, Scholefield and Smith2004). Possible explanations include low soil nitrogen immobilization and high mineralization due to the low carbon-to-nitrogen ratio of clover litter; and enhanced soil structure (Loiseau et al. Reference Loiseau, Carrère, Lafarge, Delpy and Dublanchet2001; Rochon et al. Reference Rochon, Doyle, Greef, Hopkins, Molle, Sitzia, Scholefield and Smith2004). Forage legumes also represent a small source of N₂O, directly from the process of biological fixation, but primarily as a result of the release of root exudates in the growing season and the decomposition of crop residues post-harvest (Rochon et al. Reference Rochon, Doyle, Greef, Hopkins, Molle, Sitzia, Scholefield and Smith2004). Few studies have compared the overall nitrogen balance of grazed unfertilized grass–clover pastures with grazed fertilized pure grass pastures. In a review of available data, Ledgard et al. (Reference Ledgard, Schils, Eriksen and Luo2009) found total nitrogen leaching losses and N₂O emissions from nitrogen cycling of excreta to be similar in both pasture types with comparable total nitrogen inputs. However, due to fertilizer-specific CO₂ and N₂O emissions (such as increased denitrification losses) whole system GHG emissions were typically lower per unit of produce in grass–clover systems. Research on the comparative nitrogen balance of pure legume pastures is more limited. There is some evidence that nitrogen leaching from pure white clover pasture may be considerably higher than grass–white clover pasture, possibly as a result of high nitrogen concentrations in the clover leading to greater nitrogen excretion, which the pasture is unable to take up (Loiseau et al. Reference Loiseau, Carrère, Lafarge, Delpy and Dublanchet2001).

Plant breeding to improve the efficiency of nitrogen use holds promise for future mitigation through pasture plant and forage crop selection. One area of current research interest is ryegrass breeding for improved fertilizer recovery (Abberton et al. Reference Abberton, Marshall, Humphreys, Macduff, Rowlinson, Steele and Nefzaoui2008). Some species hold interest for future breeding strategies because of features such as improved rooting depths that enable nitrogen uptake from deep in the soil profile; the production of natural NIs in the roots; and greater nitrogen immobilization in soil associated with the quality of the crop residues (Luo et al. Reference Luo, de Klein, Ledgard and Saggar2010; Schils et al. Reference Schils, Eriksen, Ledgard, Vellinga, Kuikman, Luo, Petersen and Velthof2011). Richardson et al. (Reference Richardson, Felgate, Watmough, Thomson and Baggs2009) suggested that plant breeding to control exudates to the soil could be a means of manipulating denitrification to increase the ratio of N₂ to N₂O production. Although these rhizosphere strategies involving manipulation of the soil microbial community hold strong promise it is likely that this technology will not be readily transferable between soil types making its widespread adoption difficult.

Additions to soil

Nitrification inhibitors, urease inhibitors (UIs) and slow-release fertilizers influence the rate at which fertilizer or urine nitrogen is supplied to plants (Shaviv & Mikkelsen Reference Shaviv and Mikkelsen1993). They provide a steadier supply of nutrients to pasture and forage crops and minimize losses of excess nutrients. Slow release fertilizers such as those coated to reduce solubility have been shown to reduce losses of applied nitrogen, avoiding large fluxes of N₂O after rainfall (following a fertilizer application), whilst maintaining yields (Ball et al. Reference Ball, Mctaggart and Scott2004). Despite confidence in their mitigation potential the cost of slow release fertilizers in terms of substitution for a conventional fertilizer and in terms of the cost per tonne of carbon abated is currently prohibitive (Ball et al. Reference Ball, Mctaggart and Scott2004; Moran et al. Reference Moran, Macleod, Wall, Eory, Pajot, Matthews, Mcvittie, Barnes, Rees, Moxey, Williams and Smith2008). Although outreach programmes are increasing farmer awareness of GHG issues, overcoming the barriers to technology adoption will remain difficult without farm subsidies.

Nitrification inhibitors and/or UIs can be applied directly to the crop (e.g. as a spray), incorporated into fertilizers or even infused into the gastrointestinal tract of livestock for excretion onto pasture (Ledgard et al. Reference Ledgard, Menneer, Dexter, Kear, Lindsey, Peters and Pacheco2008). Nitrification inhibitors reduce the rate of conversion of NH₄ to NO₃⁻ in the soil (Di et al. Reference Di, Cameron and Sherlock2007), releasing NO₃⁻ at a rate which better matches crop uptake. Urease inhibitors slow the conversion of urea to NH₄⁺, reducing the potential for NH₃ volatilization (Watson & Akhonzada Reference Watson and Akhonzada2005). Numerous studies have demonstrated the efficacy of NIs (Di et al. Reference Di, Cameron and Sherlock2007; Hoogendoorn et al. Reference Hoogendoorn, de Klein, Rutherford, Letica and Devantier2008; Ledgard et al. Reference Ledgard, Menneer, Dexter, Kear, Lindsey, Peters and Pacheco2008) and UIs (Watson & Akhonzada Reference Watson and Akhonzada2005; Dawar et al. Reference Dawar, Zaman, Rowarth, Blennerhassett and Turnbull2011) in reducing nitrogen losses from pastures and forage crops receiving urine and/or urea. A recent review of studies on the NI dicyandiamide (DCD) found that, when applied above the recommended minimum rate of 10 kg/ha, it reduced N₂O emissions from urine by an average 57% (compared with controls receiving no DCD) (de Klein et al. Reference de Klein, Cameron, Di, Rys, Monaghan and Sherlock2011). However, emission reduction potential varies depending on site-specific factors such as soil type, soil moisture, urine nitrogen application rate and whether or not urea fertilizer is also applied (Luo et al. Reference Luo, de Klein, Ledgard and Saggar2010; de Klein et al. Reference de Klein, Cameron, Di, Rys, Monaghan and Sherlock2011).

Critical knowledge gaps remain for NIs, including their efficacy over the long-term and under non-ideal conditions (Suter et al. Reference Suter, Eckard and Edis2007). The validity of extrapolating data from small-scale experiments to whole farm potentials is also problematic (Suter et al. Reference Suter, Eckard and Edis2007). Most studies to date have been based in New Zealand; therefore efficacy under other climatic conditions is less certain. The UK, for example, has predominantly heavy texture soils and short growing seasons in comparison with the free draining soils and longer growing seasons in New Zealand (Moorby et al. Reference Moorby, Chadwick, Scholefield, Chambers and Williams2007). In contrast, one UI (n-butyl thiophosphoric triamide (NBTPT)) is already available commercially in the UK. When applied with urea to four contrasting soil types (two arable, two grasslands) it inhibited NH₃ loss on average across all soils, temperatures and formulations by 61·2–79·8% (Watson & Akhonzada Reference Watson and Akhonzada2005).

The effect of biochar incorporation on soil nitrogen cycling is an emerging area of research. In addition to the primary objective of sequestering carbon, biochar incorporation in soil may also increase biological nitrogen fixation, reduce N₂O emissions and NO₃⁻ leaching and increase nitrogen retention as NH₃ and NH₄⁺ (Clough & Condron Reference Clough and Condron2010). In the only field-based study to date on the effect of biochar incorporation on emissions from ruminant urine patches on pasture, Taghizadeh-Toosi et al. (Reference Taghizadeh-Toosi, Clough, Condron, Sherlock, Anderson and Craigie2011) incorporated biochar into a renovated perennial ryegrass pasture. The grass was fertilized with urea after emergence, cut to simulate grazing and received an application of urine. Biochar addition at a rate of 30 t/ha was found to reduce cumulative N₂O emissions over a 65-day period by c. 50% compared with a urine-only treatment. This biochar treatment also had the lowest soil NO₃⁻ concentrations and the highest soil NH₄⁺ concentrations. Taghizadeh-Toosi et al. (Reference Taghizadeh-Toosi, Clough, Condron, Sherlock, Anderson and Craigie2011) proposed that the biochar functioned as a sink for urinary NH₃, reducing the inorganic nitrogen pool available to nitrifiers, therefore reducing N₂O emissions and the subsequent formation of NO₃⁻. Work on forage crops and grassland destined for silage has also indicated increased N use efficiency in the presence of biochar; however, the effects were not consistent over a 3-year period, suggesting that it does not offer a reliable strategy for GHG emission reduction (Jones et al. Reference Jones, Rousk, Edwards-Jones, Deluca and Murphy2012). In addition, the high production and transport cost of biochar, competition from other sectors for biochar feedstock (e.g. biomass energy), risks to humans and the environment from pollutants contained within the biochar (e.g. dioxins, PAHs), negative interactions with pesticides and current legislative barriers all limit its use in sheep-based agricultural systems (Jones et al. Reference Jones, Edwards-Jones and Murphy2011). Further work is certainly needed to understand the mechanisms through which biochar affects soil nitrogen cycling, the soil conditions, which favour these mechanisms and cost-effective strategies for implementation.

The addition of lime to soil has been suggested as a mitigation option with small potential for reducing N₂O losses (Clark et al. 2001). The rates of both nitrification and denitrification are sensitive to soil pH (Dalal et al. Reference Dalal, Wang, Robertson and Parton2003; Kemmitt et al. Reference Kemmitt, Wright, Goulding and Jones2006). Bouwman et al. (Reference Bouwman, Boumans and Batjes2002) modelled the relationship between N₂O emissions and controlling environmental and management factors such as climate, soil type and fertilizer type based on 846 published N₂O emission measurements. Soil pH was a significant determinant of N₂O emissions, which were lowest in alkaline conditions. Recent studies by Zaman & Nguyen (Reference Zaman and Nguyen2010) and Galbally et al. (Reference Galbally, Meyer, Wang, Smith and Weeks2010) found that liming pasture soils with and without the addition of urine or nitrate fertilizer has no significant effect on N₂O emissions, demonstrating that understanding of the impacts of liming under different field conditions restricts its viability as an on-farm mitigation option at present. It must also be remembered that lime itself has a high intrinsic GHG cost associated with production, transport and its subsequent decarbonation in soil (Brock et al. Reference Brock, Madden, Schwenke and Herridge2012). As with any GHG intervention, it is therefore important that a full life-cycle assessment (LCA) is performed to evaluate the net GHG balance of the mitigation strategy in a truly holistic sense before blanket policy recommendations are made.