1. Introduction
Wheat is one of the main cultivated cereals around the world, with 214.8 million hectares under production [
1]. In Spain, wheat production represents 34% of grain cereal production [
2], since the Mediterranean climate allows for producing high-quality wheat with adequate management practices [
3], especially bread wheat, with more demanding quality standards.
Spain is the European country with the highest porcine livestock population, reaching 30.8 million heads in 2018 [
4]. The slurry (PS) produced contains more than 1.3 million tons of nitrogen (N) and is applied as fertilizer to field crops, being the most common recycling method for this product. However, high rates of nutrients on farmland, usually desynchronized with crop demands, increase notably the risk of environmental pollution [
5]. Pollution associated with PS application includes nitrate (NO
3−) leaching, an increase in soil heavy metal concentrations (mainly zinc and copper), and ammonia (NH
3) and nitrous oxide (N
2O) emissions to the atmosphere [
6,
7,
8,
9]. Accordingly, different management practices can be implemented to reduce these environmental risks; e.g., PS applied at adequate rates leads to minimizing N losses by drainage [
10] and early slurry incorporation with tillage after its application is recommended to control NH
3 volatilization [
11].
The emission of N
2O from agricultural soils is mainly related to two biological processes, denitrification and nitrification, although some small N
2O emissions may be also produced through non-biological processes. Denitrification is the reduction of nitrate to molecular nitrogen (N
2) through the mediation of anaerobic denitrifiers; the process can be incomplete and some of the nitrogen is emitted as nitric oxide (NO) and N
2O [
12]. The main factors affecting denitrification in soils are soil nitrate concentration, temperature, humidity, and labile carbon presence [
13]. Denitrification is maximum at high soil nitrate concentrations, with temperatures in the range of 28–36 °C, when the soil water-filled pore space (WFPS) exceeds 60%, although in very wet soils (WFPS >90%) N
2 is the prevalent form of denitrification, and it is enhanced in soils with a ready supply of organic carbon, such as manure or crop residues [
14]. However, PS has low C content, thus its application would be not expected to have a strong influence on N
2O emissions in comparison to synthetic N. Nitrification is the pathway in which ammonium is oxidized to nitrite, and then nitrite is reduced to nitrate; the process is mediated by autotrophic ammonia oxidizers, autotrophic nitrite oxidizers, and heterotrophic nitrifiers [
15]. Nitrification needs soil ammonium, and it is optimum at a temperature between 25 and 30 °C, and when WFPS is around 55% for fine-textured soils, and around 40% WFPS for coarse-textured soils [
16]. The main pathway of N
2O emission in aerobic Mediterranean cultivation is nitrification, with denitrification relevant only on the rare occasions when WFPS > 60%.
The meta-analysis of Aguilera et al. [
8] showed that the use of organic fertilizers significantly reduced direct N
2O emissions in comparison to synthetic fertilizers, but this reduction depended on the type of product, being more effective in solid manure than in liquid slurry, where no reduction was observed. These authors identified some limitations and knowledge gaps of studies with organic fertilization that should be covered, such as measurements for longer periods or evaluation of yield and yield-scaled emissions with different types of products.
Adjusting N fertilizer rate and splitting the N application are well-known strategies to improve nitrogen use efficiency in wheat and reduce reactive N losses to the environment. Nitrogen application at tillering provides yield increase by increasing the number of ears, and latter application in the period of stem elongation-flowering increases the grain protein content [
17]. Pig slurry application at the same nitrogen rate as that used for synthetic fertilizers can result in similar crop yields [
18]. Although the traditional PS application to winter cereals is usually before sowing, PS application at the tillering stage expands its application time window and improves its usability [
19] as this brings the N application time closer to crop uptake. The application of PS to wheat at tillering needs to be based on information about agronomic performance (yield and grain quality) for efficient recycling. However, there is a lack of information on PS efficiency in comparison to synthetic N in Mediterranean irrigated conditions. This incomplete knowledge is partly due to the high variability in PS compositions and environmental conditions. The yield response to PS application is additionally a key factor for the right assessment of N
2O emissions using the concept of yield-scaled emissions.
In the application at tillering, the slurry remains on the surface of the soil [
20], increasing the risk of ammonia gaseous N losses. In this situation, practices such as immediately incorporating the slurry after its application or injecting slurries into the soil, which abate NH
3 and indirect N
2O emissions [
21], are unfeasible, except in irrigated areas where PS can be incorporated by irrigation. The acidification of pig slurry is a solution to reduce NH
3 emissions during its application to the soil as fertilizer. The pH decrease during acidification reduces the concentration of NH
3 relative to NH
4+ in the slurry reducing the risk for ammonia volatilization [
22]. Monocarbamide dihydrogen sulfate (MCDHS; international patent WO 2007/132032 A1) has been classified as a urease inhibitor. Even when the pig slurry urea has been transformed into ammonium, according to the company that owns the MCDHS patent, the ammonium-N form is protected since the micro-acidification, due to hydrolysis of the MCDHS molecule, could reduce ammonia volatilization and affect soil N dynamic. However, this product has not been widely assessed and no information can be found in the scientific literature about its effects on the soil N dynamics.
In this context, the first objective of this study is to evaluate, in a bread wheat crop under semiarid Mediterranean irrigated conditions, the effect of substituting synthetic N fertilizer for pig slurry on crop productivity, nitrous oxide emissions, emission factors, and yield-scaled emissions during three consecutive years. The second objective is to assess the effect of adding the novel urease inhibitor MCDHS to pig slurry on crop productivity, soil nitrogen dynamics, and nitrous oxide emissions through its acidification potential that protects ammonium-N form from ammonia losses.
4. Discussion
The N source at tillering application did not affect grain yield and, as a consequence, pig slurry application produced yields similar to those obtained by fertilizing with urea. No grain yield reduction associated with the use of pig slurry substituting synthetic fertilizers has been reported in other studies for different crops [
39,
40,
41]. A second N application as ammonium nitrate at stem elongation did not increase grain yield compared to a unique side-dress N application, which is in agreement with the inconsistent response of grain yield to variations in the timing and splitting of N fertilizer reported by López-Bellido et al. [
42]. However, the second side-dress N application at stem elongation allowed an increase in grain protein, which corroborates previous studies like that by Debaeke et al. [
17] who suggested that the split and late application of N guarantees a better distribution of N in the kernel. This increase in grain protein was observed when the N rates increased in the application at stem elongation even though they exceeded the critical N rate above which the maximum yield was obtained. Under similar irrigated Mediterranean conditions, Lloveras et al. [
43] also reported that higher N rates are required to achieve high bread-making quality than to obtain the highest grain yield. Furthermore, grain protein was influenced in this study by the N source applied at tillering. Lower N rates at stem elongation were necessary to reach higher protein content when urea was used in the tillering side-dress application, compared to pig slurry. Even if the slurry was applied using trail hoses to reduce NH
3 volatilization—compared to the splash-plate method, for example [
11]—the NH
3 losses were still expected to be higher in the slurry treatments than in the urea treatments. Therefore, higher N availability should be expected in urea treatments, with a subsequent increase in grain protein content. Under similar environmental conditions, Mateo–Marín et al. [
44] measured ammonia losses derived from pig slurry applications comprising up to 28.5% of the N applied.
Unintentionally, the experiment took place under relatively high N availability conditions, associated with large N fertilizer rates relative to crop needs during the previous years, which led to a low grain yield response to N application for the three cropping seasons. Thus, the soil mineral N (0–30 cm depth) in the control treatment was relatively high before the first side-dress application, especially for the first and second year (2015/16: 59 ± 8 kg N ha
−1; 2016/17: 52 ± 5 kg N ha
−1; 2017/18: 27 ± 3 kg N ha
−1). NUEb values during the whole experiment exceeded the threshold of 0.9 proposed as an indicator of soil nutrient removal [
45]. However, as only grain was exported from the plots, the depletion of soil N was not expected to be noteworthy. Soil N removal can also be accelerated by high RE
N [
46]; however, in this study, RE
N values were lower than the mean value of 0.57 in the analysis of Ladha et al. [
46]. After three consecutive years of growing wheat, the average RE
N reached values within the normal range (0.50–0.80) in well-N-managed systems for cereal crops [
47]. The lower values obtained for the first season can be explained by the absence of a response to the N application.
In this study, MCDHS did not affect N2O emissions, as would be expected for the application of a urease inhibitor to pig slurry that has already transformed the urea-N to ammonium-N before the addition of the inhibitor. Nonetheless, the experiment allows discarding other potential effects associated with the presence of dihydrogen sulfate in the molecule, such as decreasing soil pH near the soil-fertilizer interphase, with a subsequent effect on N dynamics. Thus, the MCDHS did not reduce the pH of PS compared to the non-treated slurry (data not shown), which is in agreement with the absence of significant differences in soil mineral N content between both treatments (PI vs. PSI). The only difference in soil nitrate concentrations found (2015/16) between PS fertilizers (with and without MCDHS) was not consistent through soil depths and seasons, and the inorganic N forms (ammonium-N and mineral-N) were not affected by the addition of MCDHS. This absence of differences between treatments proves that the effect of the inhibitor on the soil N dynamics is not detectable; in fact, SMN evolution followed the same pattern, in terms of amounts and temporal dynamics, in both fertilizer treatments.
Nitrous oxide emissions responded to fertilizer application independently of the N source and mainly occurred under soil WFPS conditions (40–70%) that promoted nitrification [
48], although in 23% of the dates WFPS exceeded 60%, and conditions were also ripe for denitrification. The absence of differences in N
2O emissions between urea and pig slurry might be attributed to the similar mineralized nature of the N forms they contain (urea-N in urea fertilizer and ammonium-N in pig slurry). Pig slurry did not promote higher emissions in the moments when denitrification processes were active, probably due to its low carbon content. Noticeable differences in the maximum N
2O flux peaks were observed among the three seasons, with a lower peak during the first year. This fact might be attributed to a rainfall event (24.5 L m
−2) which happened three days after the first fertilizer application of season 2015/16, displacing the mineral-N to deeper layers compared to the other seasons. The importance of the fertilizer position on N
2O emissions was demonstrated by Liu et al. [
49], who reported between 40–70% higher fluxes when fertilizer was injected at 0–5-cm depth compared to fertilizer located at 10–15 cm.
Liu and Powers [
50] indicated that N
2O EF for swine slurry application was similar to the default value (EF
1 = 1%) suggested by the IPCC [
51]. According to a meta-analysis of Cayuela et al. [
52], the organic-liquid fertilizers present the highest EF (0.85% ± 0.30,
n = 30), compared to synthetic fertilizers, which presented EFs values generally lower than 1%. However, the 2019 Refinement to the 2006 IPCC Guidelines for National Gas Inventories [
53] changed the default EF of “all N inputs in dry climates” to 0.5%. The present study did not show consistent differences in N
2O EFs between synthetic urea and slurry treatments, with values close to 1% after two N applications (120 kg N ha
−1 and 30 kg N ha
−1). Nevertheless, the implications and benefits of rational recycling of nutrients from a growing porcine livestock population have to be considered comprehensively (i.e., life-cycle assessment) when comparing synthetic with organic fertilizers.
According to the water balance, the contribution of nitrate leaching to N losses was relatively low in the whole experiment, although the drainage produced in the third season, twenty days after the first side-dress N application, could have been produced in a critical moment for N leaching [
6]. However, the low SMN content (13.6 kg N ha
−1 from 0 to 30 cm the day before the rainfall event) rejects the possibility of large nitrate losses by leaching.
The more N applied, the more unaccounted NO-I. The main components of unaccounted NO-I were NH3 volatilization and net mineralization. Since similar yields were obtained among treatments, no differences in N-immobilization due to straw incorporation should be expected. The trend to higher unaccounted NO-I for slurry treatments compared to urea treatments agrees with lower grain N concentrations in pig slurry than in synthetic-N treatments, since more unaccounted NO-I would mean less available N for the crop.