Urease inhibitors: opportunities for meeting EU national obligations to reduce ammonia emission ceilings by 2030 in EU countries

Anthropogenic NH3 emissions, primarily from agriculture, have led to significant damage to human health and ecosystems. In the European Union (EU), the National Emission Ceilings (NEC) Directive 2016/2284/EU sets ambitious reduction targets by more than 30% for some countries by 2030 compared to 2005 levels. As urease inhibitors (UIs) can reduce the NH3 emission from urea by up to 70%, Germany has enforced their addition to granular urea by the national Fertilizer Ordinance since 2020. Therefore, this study investigates the implementation of UIs for urea fertilizers via national policy regulations to evaluate their contribution to achieving the 2030 targets in the EU countries. The results indicate that the contribution of UIs for countries with high reduction targets can reach 20%–60% of the required NEC reduction. The assessment of costs and benefits of UI implementation demonstrates that the ratio of benefits to costs can reach 70. Therefore, we recommend that adding UIs to urea fertilizers is one of the best strategies for mitigation of NH3 emissions not only in the EU but also in other regions such as China.


Introduction
Anthropogenic NH 3 emissions, primarily from agriculture (e.g. 80%-95% in the European Union (EU) in 2018) (EEA 2019), have led to the causes of air pollution, soil acidification, and surface water eutrophication, which can significantly damage human health and ecosystems (Giannadaki et al 2018). The total environmental cost of reactive nitrogen was estimated at €75-485 billion year −1 , and about 60% of the cost is related to impacts on ecosystems, 40% to impacts on human health (van Grinsven et al 2013). Therefore, mitigation of NH 3 emissions has received high priority in the EU.
In 2001, the EU adopted the National Emission Ceilings (NEC) Directive (2001/81/EC) to control major air pollutants (EEA 2019). Most significantly, sulfur dioxide (SO 2 ), nitrogen oxides (NO x ), non-methane volatile organic compounds, and particulate matter (PM 2.5 ) emissions from 2005 to 2016 fell by 70%, 37%, 28%, and 21%, respectively (EEA 2019). Since 2000, however, only modest reductions of ammonia (NH 3 ) emissions were achieved in the EU. According to the European Monitoring and Evaluation Programme (EMEP)-Trend from the United Nations Economic Commission for Europe (UNECE) (2020), the observations of air ammonium concentrations showed no significant downward trend for Europe as a whole after 2000. Agricultural NH 3 emissions have exhibited the least reduction. Although agricultural NH 3 emissions decreased by 5% between 2005 and 2013 in the EU, they increased by >3% between 2013 and 2016 (EEA 2019, Giannakis et al 2019). Even though a few countries have relatively strict regulations in place, there is no extensive body of EU legislation focused on reducing NH 3 emissions from agriculture. Furthermore, emission projections in Europe also indicate that future ammonia emission reductions will be relatively small if these depend on current legislation (UNECE 2020). In contrast, significant reductions in NH 3 volatilization have been achieved during the last 20 years in some EU member countries such as Denmark, the Netherlands, and the UK through the implementation of environmental policies. In contrast, NH 3 emissions in Spain increased by 14% from 1990to 2011(Sanz-Cobena et al 2014. The NEC Directive 2016/2284/EU sets ambitious reduction targets for NH 3 emissions by 2030. For instance, some EU countries are required to reduce NH 3 emissions by >30% by 2030 from 2005 levels. The respective countries must determine policy regulations to mitigate agricultural NH3 emissions to comply with such targets. Germany amended the Fertilizer Act in 2017 and passed a new Fertilizer Ordinance to comply with this NEC Directive. The German Fertilizer Ordinance (BLE 2020) states: 'from 1 February 2020, urea as a fertilizer is applied either with additive urease inhibitors (UIs) or is worked by incorporating urea into soils without delay or at the latest within four hours of spreading urea fertilizer' .
Incorporation of urea application is hindered by constraints such as labor shortage, soil conditions, high plant density, and/or established tree crops or forages at the time of application. Therefore, the addition of UI to urea is the most feasible solution legally targeted by the revised German policy regulation. To the best of our knowledge, Germany is the first country to enforce UI implementation for urea to mitigate NH 3 emissions. The current commercial UIs can effectively reduce enzyme activity to decrease the urea hydrolysis rate. Many studies have shown that such UIs can reduce NH 3 emissions from surface-applied urea fertilizer by 50%-80% (Schraml et al 2016, Li et al 2017, Silva et al 2017, Cantarella et al 2018. Moreover, no additional field application facilities are required for the use of urea coated with UI. After the first UI product for urea entered the market in the mid-1990, new and novel UIs that reached the market in the 2000s have increased the UI efficiency by improving the product shelf life and stability at high and low temperatures during the transport, storage, and application (Schraml et al 2016, Li et al 2017.
The respective contribution of such measures to achieve the 2030 targets and the related benefits and costs for the farmers and the society should be assessed to aid the formulation of specific implementation measures for individual EU countries.

Contribution of UIs added to urea fertilizers to NH 3 reduction targets set by the NEC Directive in the EU
Urea accounts for >50% of all synthetic N fertilizers worldwide, and it is the most popular N fertilizer used by farmers because of its high N content (46%), relatively low price per unit N, and relative safety and ease of handling in transportation, storage, and application (Cantarella et al 2018). However, urea also has disadvantages, such as the rapid hydrolysis by soil ureases, which can cause NH 3 volatilization. As a result, the global average NH 3 loss from urea fertilizers is estimated to reach 40% (Cui et al 2010, Cantarella et al 2018.
The NEC Directive 2016/2284/EU requires all EU countries to reduce the NH 3 emissions by an average of 19% by 2030 relative to 2005 levels and sets individual targets for each country.
To reliably analyze the role of UI in reducing NH 3 emissions, we assessed the UI contribution to the NEC target for NH 3 emissions in each EU country (C UI , %) as: where U cons is the urea consumption of a given country (t/y), EF u is the emission factor (EF) of urea (g NH 3 -N/kg N applied or %), UI eff is the UI efficiency for NH 3 reduction from urea-N (%), and E NH3 is the targeted reduction of NH 3 emissions for the given country (t NH 3 -N/y) from 2017/18 to 2030. A report from Fertilizer Europe (2021) has indicated that there will be an increase in N fertilizer use across the EU by an average of −0.5% year −1 between 2020 and 2030. Therefore, we used 2017 and 2018 U cons data from IFASTAT (2021). NH 3 volatilization from urea is influenced by temperature, soil water content, and soil pH. Therefore, an EF is commonly adopted to quantify global or regional NH 3 emissions from urea. The EF value represents the percentage of applied urea-N that volatilizes as NH 3 (g NH 3 /kg N applied or %). According to EEA (2019), EFs of urea N fertilizers in the EU range 15.5%-21% for cool and normal soil pH and warm and high soil pH. In this assessment, an EF of 15.9% for a temperate climate and normal soil pH was used (EEA 2019). Because the UI efficiency (UI eff ) ranges within 50%-80% (Schraml et al 2016, Li et al 2017, Silva et al 2017, Cantarella et al 2018, 50% and 70% of UI efficiencies (UI eff ) for the reduction of NH 3 emissions from urea were considered as the options of UI efficiencies in this study. Figure 1 demonstrates that the contribution of UI to achieve the NEC targets varies among EU countries, as it is influenced by urea consumption and the specific target value. The assessment of the UI contribution in 2017 and 2018 was similar for most EU countries, which agrees with the expectation that urea consumption in the EU will remain stable until 2030. The addition of UI with 70% efficiency further enhanced the results compared to those at 50%.
According to the NEC Directive 2016/2284/EU, the targeted reduction in NH 3 by 2030 ranges from 0.1 to 187 (10 3 × t NH 3 /y). Countries like Germany, France, and Spain have NH 3 reduction targets higher than 10 000 t NH 3 /y by 2030. Figure 1 demonstrates that the potential contribution of UI under 50%-70% efficiency for the reduction of NH 3 emissions by 2030 is 44%-69%, 41%-60%, 40%-63%, 32%-50%, 25%-39%, 24%-41%, 10%-17%, and 3% for France, Italy, Poland, Spain, Romania, the UK, Germany, and the Netherlands, respectively, based on the urea consumption of 2017 and 2018. For Bulgaria and Ireland, the targeted NH 3 reduction can be achieved if UI with 50% or 70% efficiency is used ( figure 1(b)). The assessment of the UI contribution to the NH 3 emission abatements in different EU countries presented in this study can help guide policy priorities.
Among other measures for abatement of NH 3 emission from urea, a ban on urea use suggested in the UK (DEFRA 2020) could be the most effective measure. In Germany, urea amended with UI is still considered the best practice by farmers since it is cheaper than calcium ammonium nitrate. Furthermore, a shift from solid urea to ammonium nitrate fertilizer will increase greenhouse gas emissions through additional direct emissions of nitrous oxide (N 2 O) (DEFRA 2020). DEFRA (2020) also reports that the benefit-cost ratio would be highest with the option urea and UI. Although a shift from urea to ammonium nitrate presents a possible option in West Europe, this is still less likely to other regions such as the USA, China, and India, where nitrate fertilizers play only a marginal role.
Furthermore, although inorganic fertilizers could be replaced by organic fertilizers, especially in intensive livestock regions, there is a need to develop low-emission technology to improve organic fertilizer usage. Since manure from livestock farming is responsible for more than 70% of the NH 3 emissions in Europe (DEFRA 2020), abatements of NH 3 emissions in the whole manure management chain, namely, feeding, housing, treatment, storage, and manure application, are required (Sajeev et al 2018). Low-emission manure application remains the cornerstone of an effective ammonia abatement strategy being the measure with the largest emission reduction potential. In Germany, low-emission manure application would cover almost 60% of the total technical abatement potential (Wulf et al 2017), and similarly, in France, the direct incorporation and injection would offer 60% of the total technical abatement potential (Mathias et al 2013, DEFRA 2020, UNECE 2020). Therefore, the low-emission application of slurry in Germany has been mandatory in arable farming since 2020 and is further required in grassland from 2025.

Implementation costs
The most widely used UIs in the market are N-(n-butyl) thiophosphoric triamide (NBPT), N-(2-nitrophenyl) phosphoric triamide (2-NPT), and a formulation combining NBPT and N-(npropyl) thiophosphoric triamide (NPPT). UIs are mainly applied as a liquid coating or incorporated into urea granules (UI/urea-N: 0.02%-0.3% w/w). There are generally no additional handling costs for transportation, storage, and field application when urea is coated with UIs. Therefore, the cost of NH 3 emission reduction by UIs (C UIR , € kg −1 NH 3 ) mainly derive from the industrial process used to incorporate UI to urea, which can be estimated as: where UI p is the cost of UI addition to urea (€ kg −1 urea-N); EF u is the EF of urea (g NH 3 -N/kg N applied); UI eff is the UI efficiency for NH 3 reduction from urea-N (%), and 1.21 is the conversion factor of the cost unit from € kg −1 NH 3 -N to € kg −1 NH 3 (molecular mass ratio of NH 3 to N). According to DEFRA (2020) and BLE (2020) with industry sources, the addition of UIs to urea accounts for 10% of the urea unit price, i.e. ∼0.08 € kg −1 urea-N in 2017 or 2018. Contrary to the EF values suggested by EEA (2019), the lowest EF from urea can reach 6% (Schraml et al 2016). The EF from urea in China can reach 37% because of high temperatures (Cui et al 2010). Therefore, to provide a critical and comprehensive assessment of UI costs, EFs of 5%, 10%, 15%, and 20% were considered, along with 50% and 70% UI efficiencies. The cost assessment values related to UI implementation for NH 3 emission abatement are shown in table 1.
The costs to implement UI for NH 3 emission abatement (€ kg −1 NH 3 ) decrease with increasing EF and with increasing UI efficiency at a given EF (table 1). This suggests that the implementation of UIs can significantly affect regions with higher urea EF, such as China.

Human and ecosystem health benefits
The monetization of health benefits can help policymakers devise effective NH 3 emission control programs. The concepts for estimating the social benefits of using UIs mainly deal with the reduction in the damage to human and ecosystem health by NH 3 emissions, since NH 3 emissions adversely affect air pollution to increase air particulate matter (PM) 2.5 and soil acidification, leading to tremendous damage to human health and ecosystems (Giannadaki et al 2018).
Damage costs from different studies are often of limited comparability because of variations in views on what damage should be quantified, doseresponse and valuation functions, the release of and exposure to air pollutants in different countries, and scale. Brink and van Grinsven (2011) estimated the health impact cost as 12 € kg −1 NH 3 in the EU. Similarly, Wagner et al (2017) estimated the costs relative to ecosystems, such as terrestrial biodiversity, as 5-15 € kg −1 NH 3 . According to the UNECE (2020), the current damage in the EU to ecosystems and human health due to ammonia emissions was monetized by CE-Delft (de Bruyn et al 2018), i.e. 17.50 € kg −1 NH 3 (margin €10-25.2). The estimates are, amongst others, based on the Health risks of air pollution in Europe (HRAPIE) methodology of WHO (2013) and the valuation of ecosystem damage (Holland and Maas 2014). These external costs include the contribution of ammonia to environmental damage from acidification and eutrophication, particulate matter formation, and related loss of live years. An extensive methodological description can be found in the Environmental Prices Handbook (EU28 version) (de Bruyn et al 2018). The damage costs vary across countries and depend amongst others on the population density: in Belgium, Netherlands, and Germany, the damage is estimated at around €30 kg −1 ammonia, while in Ireland, Spain and Finland, the damage is less than €10 kg −1 based on the robust estimation of social damage of NH 3 emissions by UNECE (2020).
The benefit of NH 3 emission abatement for human health and ecosystems is an average of 17.5 € per NH 3 in the EU, the benefit-to-cost ratio ranges ∼7.6-43. As the benefits exceed the abatement costs for all EFs and UI efficiencies analyzed in this study, principally, UIs can be recommended for implementation. In countries with high population density like Belgium, Netherlands, and Germany, the benefit-to-cost ratio will range from 13 to 73. Furthermore, because the social benefits greatly exceed the abatement costs, governments can potentially transfer some benefits to farmers as investment support for the abatement measures.
Additionally, farmers can save urea and obtain higher yields. If urea-N losses of 5%-20% occur from urea application in the field due to NH 3 emissions, approximately 0.02-0.12 € kg −1 urea-N can be saved by farmers. In a recent review, Cantarella et al (2018) concluded that the yield gain from the use of NBPT with urea varied between 0.8% and 10.2%, depending on the crop species. Cost-benefit analysis of mitigating NH 3 emissions from urea by adding UI by Sanz-Cobena et al (2015) showed that a potential grain value of 8.93 € kg −1 NH 3 -N mitigated was obtained across the EU countries.
UI use can also benefit fertilizer companies. UIs are by far still non-commodity fertilizers (Ramspacher 2017); stabilized N fertilizers, including UIs and nitrification inhibitors, comprise only 8%-10% of the fertilizers used in Europe, 1% in the USA, and only 0.25% in the world (Shaviv 2005). Therefore, regulations such as the one in Germany can help increase UI demand.

Application for other regions
Our results indicate that if UI addition to urea fertilizers is implemented in the EU through regulations, its contribution to the targeted NH 3 emission reduction required by NEC in 2030 for countries with high targets can potentially reach 20%-60% (figures 1(a) and (b)). The social benefits-to-costs ratio can reach ∼70. Therefore, adding UIs to urea is one of the best potential strategies to mitigate NH 3 emissions in the EU and other regions.
The UK is currently discussing the UI implementation to urea fertilizers as well (DEFRA 2020). The current propositions include (a) to ban the use of solid urea; (b) impose approved UI incorporation to solid urea before application; and (c) restrict the application of solid urea to the period between 15 January and 31 March (DEFRA 2020). Proposition 2 presents lower estimated costs and a greater benefitto-cost ratio, and the respective new regulations for NH 3 emission abatement might be adopted in the UK by 2022 (DEFRA 2020).
China consumed 34% of the global urea in 2019, which was around 40% of all synthetic N fertilizers in China, and thus, has the highest quantities of NH 3 emissions worldwide. In contrast to 5% of world NH 3 emissions in the EU, such losses account for 30% in China, before India (24%) and the USA (5.4%) (Zhan et al 2021). Muller and Mendelsohn (2007) reported that the cost for health damage in the US ranges from 0.1 to 73 US $ kg −1 NH 3 . Its average may be similar to that in the EU. In China, however, the estimation of the cost for health and ecosystem damage is about 6.5 US $ kg −1 NH 3 (Ying et al 2017), which is lower than the social damage cost in EU28. This may indicate a lower benefit-to-cost ratio in China compared with that in EU countries. However, NH 3 emission in China is around six times higher than in the EU countries, leading to a high mitigation potential. Zhang et al (2020) showed that the current mitigation potential of agricultural NH 3 emissions is 38%-67% compared with 20%-35% in the EU countries. Despite the high losses, China has not implemented regulations to mitigate measures for NH 3 emissions. Our results indicate that countries like China can greatly benefit from implementing UI addition to urea to mitigate NH 3 emissions.

Data availability statement
All data that support the findings of this study are included within the article (and any supplementary files).