Using nitrification inhibitors to mitigate agricultural N₂O emission: a double-edged sword?

Abstract

Nitrification inhibitors show promise in decreasing nitrous oxide (N₂O) emission from agricultural systems worldwide, but they may be much less effective than previously thought when both direct and indirect emissions are taken into account. Whilst nitrification inhibitors are effective at decreasing direct N₂O emission and nitrate (NO₃^–) leaching, limited studies suggest that they may increase ammonia (NH₃) volatilization and, subsequently, indirect N₂O emission. These dual effects are typically not considered when evaluating the inhibitors as a climate change mitigation tool. Here, we collate results from the literature that simultaneously examined the effects of nitrification inhibitors on N₂O and NH₃ emissions. We found that nitrification inhibitors decreased direct N₂O emission by 0.2–4.5 kg N₂O-N ha⁻¹ (8–57%), but generally increased NH₃ emission by 0.2–18.7 kg NH₃-N ha⁻¹ (3–65%). Taking into account the estimated indirect N₂O emission from deposited NH₃, the overall impact of nitrification inhibitors ranged from −4.5 (reduction) to +0.5 (increase) kg N₂O-N ha⁻¹. Our results suggest that the beneficial effect of nitrification inhibitors in decreasing direct N₂O emission can be undermined or even outweighed by an increase in NH₃ volatilization.

Introduction

Globally, agriculture contributes about 60% of the total anthropogenic emission of nitrous oxide (N₂O), a greenhouse gas approximately 300 times more potent than carbon dioxide (Ciais et al., 2013). The mitigation of N₂O emission from agricultural systems is an important issue worldwide. Nitrification inhibitors are recommended by the IPCC as a potential mitigation option for agricultural N₂O emission (IPCC, 2014) and have been extensively investigated and widely used across a broad range of agroecosystems (Chen et al., 2008; Qiao et al., 2015). Nitrification inhibitors temporarily suppress the microbial conversion of ammonium (NH₄⁺) to nitrite (NO₂^–) in soil. This reduces substrate availability for nitrate (NO₃^–) formation and subsequent denitrification, thereby decreasing N₂O emission and NO₃^– leaching (Bundy & Bremner, 1973; Chen et al., 2008). Recent meta-analyses indicated that nitrification inhibitors decreased N₂O emission and NO₃^– leaching by 31–48% and 32–59%, respectively, across diverse agricultural ecosystems including upland, grassland and paddy fields (Akiyama et al., 2010; Qiao et al., 2015). Nitrate loss via leaching and run-off may be transported to groundwater, rivers or estuaries where part of it may be converted to N₂O (Nevison, 2000). This indirect N₂O emission can be estimated by the IPCC emission factor EF₅ with a default value of 0.75% (De Klein et al., 2006).

The use of nitrification inhibitors, however, prolongs the retention of NH₄⁺ in soil, which could potentially increase ammonia (NH₃) emission (Zaman & Nguyen, 2012). Deposition of emitted NH₃ not only poses a major threat to environmental quality and ecosystem biodiversity (Erisman et al., 2008), but indirectly it also contributes to N₂O emission (Van Der Gon & Bleeker, 2005) through subsequent nitrification and denitrification. According to the IPCC guidelines (De Klein et al., 2006), about 1% (a range of 0.2–5%) of the NH₃ emitted is converted to N₂O after deposition to land (IPCC emission factor EF₄).

Whilst the effect of nitrification inhibitors on NH₃ volatilization is not as widely studied as that on N₂O emission, Qiao et al. (2015) recently summarized the available studies and concluded that nitrification inhibitors increased NH₃ volatilization from synthetic fertilizers and animal manures in agricultural systems by 33–67%. However, most of the studies included in the synthesis focussed on one or other of these gases, and Qiao et al. (2015) expressed the impact of the inhibitor as percentage change, not absolute difference, in nitrogen (N). The overall inhibitor effect on N₂O emission (direct and indirect), which can be determined from studies that simultaneously measure N₂O and NH₃ emissions and NO₃^– leaching in the field, remains uncertain. The inclusion of indirect N₂O emission is critical for evaluating the effectiveness of nitrification inhibitors in mitigating greenhouse gas emissions from agriculture. We therefore conducted a literature review to address this knowledge gap.

Literature search

To assess the overall contribution of nitrification inhibitors to N₂O emission (direct and indirect), we performed extensive keyword searches of several databases (Web of Science, Scopus, CAB Abstracts, Academic Search complete and Google Scholar) and the reference list of cited references, for studies published prior to October 2015. The keywords used in the search included nitrification inhibitors, names of the inhibitors such as DCD and DMPP, nitrous oxide/N₂O emission, ammonia/NH₃ emission, volatilization, direct/indirect N₂O, greenhouse gas, nitrate/NO₃^– leaching, loss and/or mitigation, agriculture, cropping, pastures and their combinations. Only studies that simultaneously examined N₂O and NH₃ emissions in the same field location were included. The search resulted in 18 observations in pasture and cropping systems (Table 1).

Table 1. Summary of studies that simultaneously investigated the effects of nitrification inhibitors on N₂O and NH₃ emissions, and the estimated overall impacts

Agricultural system	N form	N rate kg N ha^−1	Season	Inhibitor	Effect of nitrification inhibitor (NI)				Overall NI effect on N2O emission		Country	Gas measurement technique		Reference
					Direct N2O emission		NH3 volatilization		(kg N ha^−1) (I + II × EF4) e			N2O	NH3
					%a	Amount b (kg N ha^−1) (I)	%c	Amount d (kg N ha^−1) (II)	EF4 = 1%	EF4 = 5%
Cropping rice	Urea	180	Summer	N-serve	−49.9	−0.57	+64.9	+12.75	−0.44	+0.07	China	CC	OC	Sun et al., 2015
Cropping rice	Urea	240	Summer	N-serve	−19.2	−0.27	+37.5	+15.80	−0.11	+0.52	China	CC	OC	Sun et al., 2015
Cropping maize	Slurry	165	Summer	DCD	−20.4	−0.79	−3.7	−0.40	−0.79	−0.81	Brazil	CC	CC	Aita et al., 2015
Cropping wheat	Slurry	135	Winter	DCD	−52.3	−1.36	+3.1	+0.35	−1.35	−1.34	Brazil	CC	CC	Aita et al., 2015
Cropping wheat/barley; pasture	Urea	120–200	Whole year	DCD	−46.5	−0.52	+6.1	+2.20	−0.50	−0.41	UK	CC	WT	Misselbrook et al., 2014
Cropping wheat/barley; pasture	AN	120–200	Whole year	DCD	−28.7	−0.48	+5.4	+0.15	−0.48	−0.47	UK	CC	WT	Misselbrook et al., 2014
Pasture	Urine	365–625	Spring–autumn	DCD	−56.8	−1.24	−0.8	−0.97	−1.25	−1.29	UK	CC	WT	Misselbrook et al., 2014
Pasture	Urine	365–625	Spring–autumn	PD	−10.6	−0.23	+4.0	+4.87	−0.18	+0.01	UK	CC	WT	Misselbrook et al., 2014
Pasture	Slurry	106–181	Spring–autumn	DCD	−30.1	−0.38	+7.7	+2.55	−0.36	−0.26	UK	CC	WT	Misselbrook et al., 2014
Pasture	Urine	600	Autumn	DCD	−42.1	−2.93	+35.5	+18.65	−2.74	−2.00	New Zealand	CC	OC	Zaman et al., 2013
Pasture	Urine	600	Spring	DCD	−40.5	−2.15	+13.3	+13.87	−2.01	−1.46	New Zealand	CC	OC	Zaman et al., 2013
Pasture	Urine	600	Autumn	DCD	−37.1	−4.47	+43.4	+12.60	−4.34	−3.84	New Zealand	CC	OC	Zaman & Blennerhassett, 2010
Pasture	Urine	600	Spring	DCD	−46.8	−4.33	+18.2	+8.00	−4.25	−3.93	New Zealand	CC	OC	Zaman & Blennerhassett, 2010
Pasture	Urine	600	Spring	DCD	−38.6	−4.40	+9.1	+2.00	−4.38	−4.30	New Zealand	CC	OC	Zaman et al., 2009;
Pasture	Urine	600	Summer	DCD	−20.0	−0.30	+17.2	+8.60	−0.21	+0.13	New Zealand	CC	OC	Zaman et al., 2009
Pasture	Slurry	123	Spring–summer	DMPP	−7.9	−0.18	+13.9	+1.80	−0.16	−0.09	Spain	CC	OC	Menéndez et al., 2009;
Pasture	ANS	97	Spring	DMPP	−8.8	−0.39	−51.7	−0.15	−0.39	−0.40	Spain	CC	OC	Menéndez et al., 2006
Pasture	Slurry	181	Spring	DMPP	−29.1	−4.51	+42.0	+3.16	−4.48	−4.35	Spain	CC	OC	Menéndez et al., 2006

• AN, ammonium nitrate; ANS, ammonium nitrate sulphate; CC, closed chamber; DCD, dicyandiamide; DMPP, 3,4-dimethylpyrazole phosphate; EF₄, emission factor for indirect N₂O emission; NI, nitrification inhibitor; OC, open chamber; PD, pyrazole derivatives 1H-1,2,4-triazole and 3-methylpyrazole; WT, wind tunnel.
• ^a The value was calculated by: (N₂O emission in the treatment with NI – N₂O emission in the control)/N₂O emission in the control × 100%.
• ^b The value was calculated by: N₂O emission in the treatment with NI – N₂O emission in the control.
• ^c The value was calculated by: (NH₃ volatilization in the treatment with NI – NH₃ volatilization in the control)/NH₃ volatilization in the control × 100%.
• ^d The value was calculated by: NH₃ volatilization in the treatment with NI – NH₃ volatilization in the control.
• ^e EF₄ of 1% and 5% represents the mean and upper range, respectively, of the IPCC default emission factor for indirect N₂O emission (De Klein et al., 2006).

Dual effects of nitrification inhibitors on N₂O emission

From the literature review, we found that nitrification inhibitors consistently decreased direct N₂O emission from fertilizers (urea and ammonium based) and animal wastes (slurry and urine), applied at between 97 and 625 kg N ha⁻¹, by 0.2–4.5 kg N₂O-N ha⁻¹ (8–57%) (Table 1). On the other hand, NH₃ volatilization was increased by 0.2–18.7 kg NH₃-N ha⁻¹ (3–65%) following the application of the inhibitors in all but three observations. Applying the default emission factor value of 1% (De Klein et al., 2006) for indirect N₂O emission from NH₃ volatilization and deposition (EF₄), we found there was an overall N₂O-N reduction of 0.1–4.5 kg N ha⁻¹ from the use of nitrification inhibitors. However, when the upper range of EF₄ (5%) (De Klein et al., 2006) was used, the change in N₂O-N ranged from −4.4 (reduction) to +0.5 (increase) kg N ha⁻¹ (Table 1).

We found that only two studies reported the effect of nitrification inhibitors on NO₃^– leaching in addition to that on N₂O and NH₃ emissions. This precludes the estimation of indirect N₂O emission from measured NO₃^– leaching for the studies included in Table 1. Nonetheless, NO₃^– leaching is assumed to be an insignificant source of indirect N₂O emission in dryland cropping systems and grassland systems where the amount of precipitation plus irrigation does not exceed 80% of the potential evapotranspiration (De Klein et al., 2006; U.S. EPA, 2014). A global process-based simulation of terrestrial N cycle estimated that the annual leaching load is around 20 kg N ha⁻¹ for most regions with fertilizer application of >100 kg N ha⁻¹. Based on the default EF₅ value of 0.75% (De Klein et al., 2006), and an average reduction in NO₃^– leaching of 47% by nitrification inhibitors (Qiao et al., 2015), we estimated that the inhibitors may decrease indirect N₂O emission associated with NO₃^– leaching by 0.07 kg N ha⁻¹ or have no effect on the emission when NO₃^– leaching is negligible. This has minimal impact on the overall effect of nitrification inhibitors on N₂O emission.

The results of our literature review (Table 1) indicate that nitrification inhibitors effectively and consistently decrease direct N₂O emission from agricultural systems. Nonetheless, this beneficial effect can be weakened, negated or even reversed by the estimated concomitant increase in indirect N₂O emission from deposited NH₃. This highlights the importance of considering both gases when evaluating the use of nitrification inhibitors as a climate change mitigation option. An alternative approach would be to use a double inhibitor (a combination of a nitrification inhibitor and urease inhibitor). Urease inhibitors slow the hydrolysis of urea and consequently reduce NH₃ volatilization and can be effective on urea (Chen et al., 2008). A recent study showed that both NH₃ volatilization and N₂O emission were decreased when urea was treated with a double inhibitor (Zaman & Blennerhassett, 2010). However, this double inhibitor approach is impractical for decreasing NH₃ volatilization from N sources containing negligible urea but high NH₄⁺ content, such as animal manure and ammonium fertilizers. In this regard, substances with a high affinity for binding onto NH₄⁺ ions may be used as additives to mitigate NH₃ volatilization. For instance, zeolite and, more recently, lignite were shown to effectively lower NH₃ volatilization when mixed with animal manure (Ndegwa et al., 2008; Chen et al., 2015). Alternatively, where practical, manure should be incorporated into soil rather than being surface applied to prevent NH₃ loss.

Summary and implication

Nitrification inhibitors decrease direct N₂O emission and indirect N₂O emission due to NO₃^– leaching from agroecosystems. Yet this beneficial effect is weakened by any accompanying increase in indirect N₂O emission that can result from increased emission and deposition of NH₃. Appropriate NH₃ mitigation measures should be taken where nitrification inhibitors are being used to decrease direct N₂O emissions, to enable effective and viable climate change mitigation.

Acknowledgements

This work was supported by the BIP reinvestment funds of the Faculty of Veterinary and Agricultural Sciences of the University of Melbourne, the Australia-China Joint Research Centre jointly funded by Australian Government Department of Industry and Science and the Chinese Ministry of Science and Technology.