Nitrous oxide and methane fluxes from plasma-treated pig slurry applied to winter wheat

Abstract

The use of livestock waste as an organic fertiliser releases significant greenhouse gas emissions, exacerbating climate change. Innovative fertiliser management practices, such as treating slurry with plasma induction, have the potential to reduce losses of carbon and nitrogen to the environment. The existing research on the effectiveness of plasma-treated slurry at reducing nitrous oxide (N2O) and methane (CH4) emissions, however, is not comprehensive, although must be understood if this technology is to be utilised on a large scale. A randomised block experiment was conducted to measure soil fluxes of N2O and CH4 from winter wheat every two hours over an 83-day period using automated chambers. Three treatments receiving a similar amount of plant-available N were used: (1) inorganic fertiliser (IF); (2) pig slurry combined with inorganic fertiliser (PS); (3) plasma-treated pig slurry combined with inorganic fertiliser (TPS). Cumulative N2O fluxes from TPS (1.14 g N m⁻²) were greater than those from PS (0.32 g N m⁻²) and IF (0.13 g N m⁻²). A diurnal pattern in N2O fluxes was observed towards the end of the experiment for all treatments, and was driven by increases in water-filled pore space and photosynthetically active radiation and decreases in air temperature. Cumulative CH4 fluxes from PS (3.2 g C m⁻²) were considerably greater than those from IF (− 1.4 g C m⁻²) and TPS (− 1.4 g C m⁻²). The greenhouse gas intensity of TPS (0.2 g CO2-eq kg grain⁻¹) was over twice that of PS (0.07 g CO2-eq kg grain⁻¹) and around six times that of IF (0.03 g CO2-eq kg grain⁻¹). Although treating pig slurry with plasma induction considerably reduced CH4 fluxes from soil, it increased N2O emissions, resulting in higher non-CO2 emissions from this treatment. Life-cycle analysis will be required to evaluate whether the upstream manufacturing and transport emissions associated with inorganic fertiliser usage are outweighed by the emissions observed following the application of treated pig slurry to soil.

Full text

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Nutr Cycl Agroecosyst (2024) 129:505–520
https://doi.org/10.1007/s10705-024-10363-8
ORIGINAL ARTICLE
Nitrous oxide andmethane fluxes fromplasma‑treated pig
slurry applied towinter wheat
I.L.Lloyd · R.P.Grayson · M.V.Galdos ·
R.Morrison · P.J.Chapman
Received: 24 August 2023 / Accepted: 25 May 2024 / Published online: 15 June 2024
© The Author(s) 2024
Abstract The use of livestock waste as an organic
fertiliser releases significant greenhouse gas emis-
sions, exacerbating climate change. Innovative
fertiliser management practices, such as treating
slurry with plasma induction, have the potential to
reduce losses of carbon and nitrogen to the environ-
ment. The existing research on the effectiveness
of plasma-treated slurry at reducing nitrous oxide
(N2O) and methane (CH4) emissions, however, is
not comprehensive, although must be understood
if this technology is to be utilised on a large scale.
A randomised block experiment was conducted to
measure soil fluxes of N2O and CH4 from winter
wheat every two hours over an 83-day period using
automated chambers. Three treatments receiving a
similar amount of plant-available N were used: (1)
inorganic fertiliser (IF); (2) pig slurry combined
with inorganic fertiliser (PS); (3) plasma-treated
pig slurry combined with inorganic fertiliser (TPS).
Cumulative N2O fluxes from TPS (1.14 g N m−2)
were greater than those from PS (0.32g N m−2) and
IF (0.13g N m−2). A diurnal pattern in N2O fluxes
was observed towards the end of the experiment for
all treatments, and was driven by increases in water-
filled pore space and photosynthetically active radia-
tion and decreases in air temperature. Cumulative
CH4 fluxes from PS (3.2gC m−2) were considerably
greater than those from IF (− 1.4gC m−2) and TPS
(− 1.4gC m−2). The greenhouse gas intensity of TPS
(0.2g CO2-eq kg grain−1) was over twice that of PS
(0.07g CO2-eqkg grain−1) and around six times that
of IF (0.03 g CO2-eq kg grain−1). Although treat-
ing pig slurry with plasma induction considerably
reduced CH4 fluxes from soil, it increased N2O emis-
sions, resulting in higher non-CO2 emissions from
this treatment. Life-cycle analysis will be required
to evaluate whether the upstream manufacturing and
transport emissions associated with inorganic ferti-
liser usage are outweighed by the emissions observed
following the application of treated pig slurry to soil.
Supplementary Information The online version
contains supplementary material available at https:// doi.
org/ 10. 1007/ s10705- 024- 10363-8.
I.L.Lloyd(*)· R.P.Grayson· P.J.Chapman
School ofGeography, University ofLeeds, LeedsLS29JT,
UK
e-mail: gyil@leeds.ac.uk
R. P. Grayson
e-mail: r.grayson@leeds.ac.uk
P. J. Chapman
e-mail: p.j.chapman@leeds.ac.uk
M.V.Galdos
Rothamsted Research, HarpendenAL52JQ, UK
e-mail: marcelo.galdos@rothamsted.ac.uk
R.Morrison
UK Centre forEcology andHydrology,
WallingfordOX108BB, UK
e-mail: rosrri@ceh.ac.uk
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Keywords Agriculture· Automated chamber·
Carbon dioxide· Greenhouse gases· Greenhouse
gas intensity· Non-co2 greenhouse gases· Organic
fertiliser· Trade-offs
Introduction
Nitrogen (N) is one of the most limiting nutrients for
crop growth in agricultural soils, so organic (i.e., ani-
mal manure and slurry) and inorganic (i.e., synthetic)
N fertilisers are applied to provide a supply of N to
support crop growth and achieve high yields (Lu etal.
2021). Organic fertilisers also provide a source of
other plant nutrients, enhance soil carbon (C) content,
and are increasingly being seen as part of an on-farm
circular economy within the agricultural sector. The
use of fertilisers in agriculture results in significant
emissions of greenhouse gases (GHGs) to the atmos-
phere. Agriculture is responsible for 13% global car-
bon dioxide (CO2) emissions, 50% global methane
(CH4) emissions, and 60% global nitrous oxide (N2O)
emissions (Macharia etal. 2020). Nitrous oxide and
CH4 are of particular concern, as they have global
warming potentials 273 and 27.9 times greater than
CO2 respectively (Smith etal. 2021) and continue to
exacerbate climate change (Mikhaylov et al. 2020).
Agricultural N2O emissions primarily originate from
the use of inorganic and organic N fertilisers, which
has increased markedly over the last 60years (Rudaz
et al. 1999; Cameron et al. 2013; Lu et al. 2021).
Between 2016 and 2019, animal farming in the Euro-
pean Union produced more than 1.4 billion tonnes of
manure annually, and over 90% of this was directly
re-applied to soils (Koninger et al. 2021). Fertiliser
application, particularly organic fertiliser, can also
increase CH4 emissions; CH4 is often produced dur-
ing organic fertiliser storage, as the C supply and stor-
age conditions facilitate methanogenesis, dissolving
CH4 into the fertiliser and releasing it upon applica-
tion to soil (Rochette and Cote 2000; Bastami etal.
2016).
There is an urgent need to minimise the negative
impacts of agriculture on the environment, with the
aim to achieve net zero GHG emissions becoming
increasingly critical (Sakrabani etal. 2023). Despite
the implementation of strategies which aim to reduce
environmental N pollution [i.e., Nitrate Vulner-
able Zones (UK Government 2021) and 4R Nutrient
Stewardship—right source, rate, time and place
(Nutrient Stewardship 2017)], GHG emissions from
agriculture, particularly N2O, remain high (Tian etal.
2020). To reduce GHG emissions from fertiliser use,
crop N use efficiency (NUE)—the efficiency at which
applied N is assimilated by plants (Sharma and Bali
2018)—must be improved. Given the push to increase
the use of livestock waste as fertiliser and build soil
C, a range of practices and innovative technologies
are promoted to reduce GHG emissions from ferti-
liser use and improve NUE. One such example of
this is the treatment of organic fertilisers, such as pig
slurry, with plasma induction. This treatment primar-
ily aims to reduce losses of the non-GHG ammonia
(NH3) by ionising air to form reactive nitrogen gas
which is absorbed into the slurry, creating an N-rich
slurry (Nyang’au et al. 2024). This process lowers
the pH of the slurry and reduces the potential for
NH3 emissions (Nyang’au et al. 2024). An increase
in the N content of the plasma-treated slurry means
the product has the potential to replace synthetic inor-
ganic fertiliser and has been shown to increase yields
compared to untreated slurry (Mousavi et al. 2022;
Cottis etal. 2023), as well as reducing both CH4 and
NH3 emissions during storage (Graves etal. 2018).
Whether the beneficial gains of increasing the amount
of inorganic N available for immediate plant uptake
are counterbalanced by other N losses upon applica-
tion to the soil, such as N2O to the atmosphere, how-
ever, are unknown. Numerous studies have investi-
gated the impacts of fertiliser application on GHG
fluxes, mainly N2O, from agricultural soils (Insels-
bacher etal. 2010; Mateo-Marin etal. 2020; Adele-
kun et al. 2021). The overarching consensus is that
soils amended with organic fertiliser have higher N2O
and CH4 emissions than those amended with inor-
ganic fertiliser (Thangarajan etal. 2013; Walling and
Vaneeckhaute 2020; He et al. 2023). The effects of
using plasma-treated slurry as an organic fertiliser on
soil N2O and CH4 emissions is relatively unknown,
however, and most of the existing research on plasma-
treated organic waste has focused on the effects of
plasma-treated cattle slurry on crop yield, soil biota
and NH3 emissions (Mousavi etal. 2022; 2023; Cottis
etal. 2023). If plasma-treated pig slurry is to become
a potential solution to reduce non-CO2 GHG emis-
sions, it will be necessary to explore the extent to
which it can achieve this relative to non-treated pig
slurry and inorganic fertiliser.
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The aim of this study was therefore to determine
the effects of treating pig slurry with plasma induction
on N2O and CH4 fluxes and crop yield when applied
as an organic fertiliser. This was achieved by carrying
out the following objectives: (1) measure and analyse
the response of N2O and CH4 fluxes to the application
of inorganic and organic fertilisers, including plasma-
treated and non-treated pig slurry; (2) compare winter
wheat yield and its GHG intensity as a result of the
fertiliser treatment used; and (3) quantify and explain
the controls on the diurnal variation of N2O and CH4
fluxes during the main winter wheat growth phase.
Treating pig slurry with plasma-induction has been
proven to reduce NH3 emissions as a result of acidi-
fication, creating an N-enriched product which has a
higher content of inorganic N. Furthermore, a reduc-
tion in the pH of the slurry may prevent methanogen-
esis and thus CH4 formation during slurry storage,
and thus potentially following application. Therefore,
our first hypothesis is that non-CO2 GHG emissions
will be lower from the plasma-treated pig slurry
compared to the non-treated pig slurry. Based on the
existing research on GHG emissions and the impact
of fertiliser type, our second hypothesis is that N2O
and CH4 emissions will be higher from winter wheat
treated with organic fertilisers (i.e., plasma-treated
and non-treated pig slurry treatments) compared to
inorganic fertiliser, as a result of increasing C and N
availability to soil microorgansims, thus increasing
their activity.
Materials andmethods
Field site and experimental design
The University of Leeds Research Farm is a commer-
cial mixed arable and livestock farm near Tadcaster,
UK. It has a temperate climate with mild winters
and warm summers (Beck et al. 2018). The soil is
a well-drained, loamy calcareous Cambisol (Cran-
field University 2018), with a depth of 0.5–0.9 m
(Holden etal. 2019). Soil properties of the study site
are summarised in TableS1. Between 1992 and 2021
mean annual temperature ± standard deviation was
9.5 ± 1°C (Met Office 2019) and mean annual precip-
itation was 639 ± 142mm (Met Office 2006). During
the study period (20/03/2022–13/06/2022), drought
conditions and record maximum temperatures were
experienced in the UK (Turner 2022) (Figure S1);
total precipitation was 112mm and average daily air
temperature was 10.7°C (527 mm lower and 1.2°C
higher than the annual average). On 21/10/2021, win-
ter wheat (WW) (Triticum aestivum), Extase variety,
was sown at a density of 440 seeds m−2 in an arable
field (53° 51′ 56.26″ N 1° 19′ 28.22″ W; 10.4ha; ele-
vation 49m). In February 2022, prior to the applica-
tion of any fertiliser, a randomised block experiment
was set up consisting of nine plots (2 × 0.5 m) and
neighbouring areas for the placement of nine GHG
measurement chambers. Circular collars (0.5m diam-
eter) were inserted into the soil to a depth of 0.1 m
and Eosense eosAC-LT chambers (Eosense, Canada)
with an internal volume of 0.072 m−3 were attached
one month prior to fertiliser application. This allowed
the soil to return to steady state conditions prior to the
commencement of GHG measurements (Charteris
etal. 2020).
Three fertiliser treatments (each with three repli-
cates) were compared (TableS2): three applications
of inorganic fertiliser (IF); two applications of pig
slurry followed by two applications of inorganic fer-
tiliser (PS); and two applications of plasma-treated
pig slurry followed by two applications of inorganic
fertiliser (TPS). Each plot and its neighbouring GHG
chamber received the same fertiliser treatment; fer-
tiliser was applied to the plots and chambers in split
applications, the rates based on recommendations
from MANNER-NPK (ADAS 2013). All fertiliser
treatments were applied by hand; granular fertiliser
was evenly distributed onto the soil surface and slurry
was applied with a watering can, taking care to apply
slurry only to the soil surface and not on WW leaves.
The treatments were applied with the intention of all
plots receiving a total of 220kg available N ha−1. Fol-
lowing analysis of the fertilisers, it was confirmed that
the IF and PS treatments received a total of 220kg
available N ha−1, whereas the TPS treatment received
253kg available N ha−1. More detail on application
types, rates and dates are shown in TableS2. For PS
and TPS, pig slurry was collected from an on-farm
indoor pig facility and for TPS the pig slurry was then
treated using plasma induction. The plasma treat-
ment process uses electricity to ionise air and create
nitrogen oxide gas, which combines with free NH3 to
form involatile ammonium nitrate, thus reducing NH3
emissions and increasing the amount of inorganic N
potentially available for immediate plant uptake upon
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application to the crop (Graves etal. 2018; Nyang’au
etal. 2024). This may in turn reduce the amount of
N available for conversion to N2O, thus reducing
N2O emissions, however this is highly dependent on
the environmental conditions and the crop type and
growth stage. The plasma induction process also
prevents the conditions which facilitate methanogen-
esis and reduces the pH of the slurry, reducing CH4
production in storage and thus CH4 emissions upon
application (Tooth et al. 2021). The nutrient com-
position of the organic fertiliser treatments is shown
in TableS3. The IF treatment received no inputs of
phosphorous or potassium, whereas the PS and TPS
treatments did (Table S3), however this is unlikely
to have limited the growth of wheat as the soil has a
phosphorus index of 3 in the top 10cm, and thus is
not limited in the soil (TableS1).
Soil moisture and temperature were measured in
each plot at a depth of 0.05m using TEROS 11 mois-
ture and temperature sensors (METER Group Inc.
USA), with measurements logged at 15-min intervals.
Soil moisture and bulk density were used to calculate
water-filled pore space (WFPS) according to Eq.(1),
adapted from De and Toor (2015):
where
𝜃
g is soil moisture (%), Bd is bulk density
(g cm−3) and Pd is particle density (g cm−3) (assumed
to be 2.65g cm−3 for arable soils (Schjonning etal.
2017)).
GHG sampling and crop yield measurements
Fluxes of N2O, CH4 and CO2 were measured from
each chamber every 120-min between 20/03/2022
and 13/06/2022 using a Picarro G2508 GHG ana-
lyser (Picarro USA), resulting in 9288 discrete sam-
pling points over 83-days. The analyser uses cavity
ring-down spectroscopy to measure GHG fluxes; the
measurement range of N2O is 0.3–200 ppm, of CH4
is 1.5–12 ppm and of CO2 is 180–5000 ppm (Pic-
arro no date). Chamber measurements were planned
to continue until harvest, however extreme tempera-
tures caused instrument failure, so GHG measure-
ments ceased ~ 6 weeks before harvest. An Eosense
eosMX-P multiplexer (Eosense Canada) and eosLink-
AC software (Eosense Canada) allowed each chamber
to be sampled in turn. Chambers were programmed
(1)
WFPS(%)=((𝜃g×Bd)÷(1−(Bd −Pd))) ×100
to close (i.e., sample) for 7-min each on a continu-
ous loop sequence. On 25/04/2022, vertical exten-
sions (0.7m height) were attached between the cham-
ber collar and lid to accommodate the growing crop,
increasing the internal chamber volume to 0.209 m−3.
The accumulation time of the chambers was then
increased from 7 to 10-min in accordance with the
increased chamber volume.
Winter wheat was harvested from within chamber
collars and from a 0.5 m2 quadrat within each neigh-
bouring plot on 27/07/2022. Harvesting was carried
out by hand, cutting the stems 0.1m above the soil
surface. The harvested WW was weighed before and
after drying at 60°C for 24h to determine its mois-
ture content. At harvest the WW had an average mois-
ture content ± standard deviation of 13.2 ± 3.2%. The
dried WW was threshed using a HALDRUP LT-21
laboratory thresher (HALDRUP Germany), provid-
ing grain, chaff and stalk samples which were ground
and analysed for C and N content using a Vario EL
Cube elemental analyser (Elementar UK) according
to Pella (1990a, b). Separately, filtration and diges-
tion methods were used to calculate grain N content
(Ministry of Agriculture, Fisheries and Food 1973)
which was multiplied by 5.7 to calculate grain protein
content (Sosulski and Imafidon 1990; Ma etal. 2019).
Harvest index, or total WW biomass as grain, was
calculated according to Eq.(2) (Amanullah 2016):
Data processing
Greenhouse gas fluxes were calculated using bespoke
software for the Eosense chamber system (eos-
AnalyzeMX/AC V3.5.0, Eosense Canada); a linear
fit was adjusted to the raw concentration of CO2 by
identifying the start and end of each measurement,
which was then used to calculate fluxes of all gases
for each sampling point (Petrakis et al. 2017; Barba
etal. 2019). Outliers were identified using a modified
version of the method by Elbers etal. (2011) which
quantifies the uncertainty of CO2 fluxes based on
the threshold detection value (u*), statistical screen-
ing, measurement errors, and uncertainties associated
with flux calculations. Measurements of CO2, and
associated N2O and CH4, identified as outliers (261
sampling points) were then removed. Gaps in the
(2)
Harvest index(%)=(grain yield ÷total DM yield)×100
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data, either due to instrument failure during the meas-
urement period or as a result of outlier removal were
then gap-filled. Missing N2O and CH4 data between
20/03/2022 and 13/06/2022 were gap-filled using lin-
ear interpolation and missing daytime and night-time
CO2 data between 20/03/2022 and 13/06/2022 were
gap-filled separately using linear regression (Dorich
et al. 2020; Lucas-Moffat et al. 2022). Thirty-three
percent of the data were gap-filled. Complete gap-
filled data were analysed using The R Language
and Environment for Statistical Computing V4.1.3
(R Core Team 2021). As one flux measurement was
made per chamber every 2-h, measurements were
converted from µmol m−2 s−1 (CO2) or nmol m−2 s−1
(N2O and CH4) to g C m−2 (CO2 and CH4) or g
N m−2(N2O) and daily averages were calculated.
Cumulative CO2, N2O and CH4 fluxes were converted
to CO2-equivalent (g m−2 day−1) by multiplying these
gases by their GWP; 273 for N2O and 27.9 for CH4
(Smith etal. 2021).
Greenhouse gas intensity (GHGI) was calculated
according to Eq. (3) (adapted from Mosier et al.
(2006) and Guo etal. (2022):
where ED is the cumulative CO2-equivalent emissions
from each fertiliser treatment over the measurement
period (i.e., N2O + CH4; kg CO2-equivalent ha−1) and
Y is grain yield from each fertiliser treatment plot
(kg ha−1).
Throughout the paper, GHGIs are based on emis-
sions recorded during the measurement period of this
study; we acknowledge that these will not be GHGIs
for the entire WW growing season.
Nitrogen use efficiency is the percentage of total N
recovered by a plant at harvest (Scottish Government
2023); NUE of the whole crop (NUEtotal) and grain
(NUEgrain) were calculated according to Eq. (4) and
(5):
where N output is N content of whole crop
(kgN ha−1) and N input is total N added via fertiliser
(kgN ha−1).
(3)
GHGI(
kg CO2equivalent kg grain
−1)
=E
D
÷
Y
(4)
NUEtotal(%)=(N output ÷N input)×100
(5)
NUEgrain(%)=(
N output
÷
N input
)×100
where N output is N content of grain (kgN ha−1) and
N input is total N added via fertiliser (kgN ha−1).
Normality tests were conducted using the Shap-
iro–Wilk method. Tests for statistically significant
differences of mean daily and mean cumulative GHG
emissions between each fertiliser treatment were
conducted using Kruskal–Wallis and Wilcoxon tests
as all data followed a non-normal distribution. Tests
for significant differences of average WW dry mat-
ter (DM) yield, grain yield, total and grain C and
N content, and grain protein content between each
treatment were conducted using Kruskal–Wallis and
Wilcoxon or ANOVA and Tukey tests dependent on
the normality of the data. Multiple linear regression
(MLR) was used to investigate the impact of envi-
ronmental factors [i.e., precipitation, air temperature,
soil temperature (0.05 m), WFPS and photosyn-
thetically active radiation (PAR)] on N2O and CH4
fluxes for each treatment. Prior to conducting MLR,
a correlation matrix was used to assess for collinear-
ity between the environmental variables. There was
strong collinearity between soil temperature and air
temperature (0.77); MLR showed a higher R2 value
when air temperature was included compared to
when soil temperature was included, so soil tempera-
ture was removed from MLR to remove the potential
effects of collinearity. When considering the dataset
excluding the 0–7 days after the first two fertiliser
applications, the R2 value was higher when soil tem-
perature was included compared to when air tempera-
ture was included, so for this analysis air temperature
was removed from MLR.
Results
Cumulative N2O fluxes were highest from TPS and
lowest from IF, and cumulative CH4 fluxes were high-
est from PS and lower from IF and TPS (Table 1;
Figure S2). Despite lower CH4 fluxes from TPS
compared to PS, N2O fluxes were highest from TPS,
meaning that total non-CO2 fluxes were highest from
TPS compared to PS, disproving our first hypoth-
esis. Our second hypothesis is proven by the IF treat-
ment having lower non-CO2 GHG emissions than the
organic fertiliser treatments (i.e., TPS and PS). The
response of the non-CO2 fluxes to the fertiliser treat-
ments is discussed in more detail below. Cumulative
CO2 fluxes were highest from PS and lowest from IF,
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and were significantly different between PS and IF but
not between PS and TPS or IF and TPS (TableS4).
Further results on CO2 fluxes, including mean daily
and cumulative CO2 fluxes, and diurnal CO2 fluxes
for each treatment over each WW growth stage are
presented in Figures S2, S3, S4 and S5. These data
are not presented as main results as non-CO2 GHG
fluxes are the focus of this study. CO2-equivalent
fluxes of N2O and CH4 were highest from TPS and
lowest from IF (Table1; Figure S2).
N2O fluxes
Cumulative N2O fluxes were highest from TPS and
lowest from IF and were not significantly different
between treatments (Table 1; Figure S2). Nitrous
oxide fluxes increased with increasing WFPS, air tem-
perature and the application of pig slurry and treated
pig slurry (P = < 0.05), and decreased with increas-
ing PAR (P = < 0.05) (Figures S6 and S7). When
treated pig slurry was applied, significant interac-
tions were observed between N2O fluxes, WFPS, air
temperature and PAR (P = < 0.05) (Figure S7). Pre-
cipitation did not significantly influence N2O fluxes
(P = 0.42). Mean daily N2O fluxes were highest from
TPS and lowest from IF and were significantly differ-
ent between IF and PS (P = 0.004) and IF and TPS
(P = 0.03) but not between PS and TPS (P = 0.82)
(Table 1). Nitrous oxide fluxes increased following
the first fertiliser application to TPS and following the
second fertiliser applications to PS and TPS, peaking
one day after application and decreasing over five to
fourteen days before returning to pre-fertilisation lev-
els (Figs.1 and 2). Nitrous oxide fluxes from TPS and
PS did not respond to the third and fourth fertiliser
applications, which were in the form of inorganic
fertiliser and contained less N than the previous two
applications which were in the form of organic fer-
tiliser (Figs.1 and 2; TableS3). Nitrous oxide fluxes
from IF did not respond to any of the fertiliser appli-
cations (Figs.1 and 2). When considering N2O fluxes
from within seven days of the first two fertiliser appli-
cations only (i.e., when organic fertilisers were added
to TPS and PS) (Fig.3), mean daily N2O fluxes were
highest from TPS and lowest from IF and were signif-
icantly different between all treatments (P = < 0.05)
(Table1).
Diurnal variations in N2O fluxes were identi-
fied throughout the measurement period, apart from
within 0 to 7 days of the first two fertiliser applica-
tions (i.e., when organic fertilisers were applied to PS
and TPS and thus N2O flux activity was at its maxi-
mum). Therefore, to better understand the controls on
the diurnal fluxes of N2O, data from days 0 to 7 after
the first two fertiliser applications were excluded from
further analysis. Following this removal, an increase
in WFPS and PAR were found to increase N2O
fluxes; however N2O fluxes decreased with increasing
soil temperature (Figure S8). There was no significant
effect of precipitation on N2O fluxes (P = > 0.05).
Significant interactions (P = < 0.05) were identified
between pig slurry application and several environ-
mental variables and N2O fluxes (Table S5). There
was no clear diurnal trend in N2O fluxes observed at
Table 1 Mean daily and mean cumulative fluxes, and mean GHGI over the 83-day measurement period ± standard deviation (SD)
for each fertiliser treatment (IF inorganic fertiliser, PS pig slurry, TPS treated pig slurry)
Across each row, different letters indicate significant differences in the variable of interest between fertiliser treatments
IF PS TPS
N2OMean daily ± SD (gN m−2 day−1)0.002 ± 0 a 0.004 ± 0 b 0.013 ± 0 a
Mean cumulative ± SD (gN m−2)0.13 ± 0 a 0.32 ± 0.1 a 1.14 ± 0.1 a
Mean daily 0–7days after first two ferti-
liser applications ± SD (gN m−2 day−1)
0.004 ± 0 a 0.013 ± 0 b 0.068 ± 0 c
CH4Mean daily ± SD (gC m−2 day−1)− 0.0003 ± 05.8e-05 a 0.0004 ± 0.0006 a − 0.0003 ± 0.0001 a
Mean cumulative ± SD (gC m−2)− 1.4 ± 0.3 a 3.2 ± 1.4 a − 1.4 ± 0.6 a
Mean daily 0–7days after first
two fertiliser applications ± SD
(mmol CH4 m−2 day−1)
− 0.0002 ± 0 a 0.004 ± 0 b -0.0001 ± 0 a
CO2-eq
(N2O + CH4)
Mean cumulative ± SD (g CO2-eq m−2)34.2 ± 7.6 a 88.8 ± 14.3 a 311.7 ± 34.9 a
Mean GHGI ± SD (g CO2-eqkg grain−1)0.03 ± 0.005 a 0.07 ± 0.02 a 0.2 ± 0.02 a
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Tillering S5 and Extension S6, although the magni-
tude of N2O flux was higher from TPS compared to IF
and PS at these growth stages (Fig.3). From Exten-
sion S7 onwards a slight diurnal trend in N2O fluxes
became prevalent for all treatments and became more
pronounced from Extension S10 onwards—fluxes
increased during the day and decreased at night, with
the highest fluxes observed between 10:00 and 12:00
(Fig.3).
CH4 fluxes
Cumulative CH4 fluxes were highest from PS and
lower from IF and TPS and were not significantly dif-
ferent between treatments (Table1; Figure S2). Meth-
ane fluxes increased with increasing WFPS, PAR, air
temperature and pig slurry application (P = < 0.05).
(Figure S6; Figure S7). There was no significant
influence of precipitation on CH4 fluxes (P = 0.24).
Mean daily CH4 fluxes were highest from PS and
lower from IF and TPS but were not significantly
different between treatments (P = > 0.05) (Table 1).
Methane fluxes from PS peaked immediately after the
first and second fertiliser applications and remained
elevated for less than 24h before returning to pre-
fertilisation levels (Figs.1 and 2). Methane fluxes did
not respond to the third and fourth fertiliser applica-
tions which were in the form of inorganic fertiliser
(Figs.1 and 2; TableS5). Methane fluxes from IF and
TPS remained low for the entire measurement period
and did not respond to any fertiliser applications
(Figs. 1 and 2). When considering CH4 fluxes from
0 to 7days of the first two fertiliser applications only
(Fig.2), mean daily CH4 fluxes were higher from PS
than IF and TPS but were not significantly different
between treatments (P = > 0.05) (Table1). There was
Fig. 1 2-h fluxes of A N2O, B CH4 and C CO2-equivalent
fluxes of N2O and CH4 for each fertiliser treatment (IF inor-
ganic fertiliser, PS pig slurry, TPS treated pig slurry). Each
data point represents the mean of three chambers used per
treatment and vertical dashed lines represent the split applica-
tions of fertilisers. Error bars have been removed to aid visu-
alisation
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Fig. 2 Two-hour fluxes of A–D N2O and E–H CH4 during
the first 7days of each fertiliser application for each fertiliser
treatment (IF inorganic fertiliser, PS pig slurry, TPS treated pig
slurry). Each data point represents the mean of three chambers
used per treatment and vertical dashed lines represent the split
applications of fertilisers. Error bars have been removed to aid
visualisation
Fig. 3 Mean 2-h fluxes of N2O for each fertiliser treatment (IF
inorganic fertiliser, PS pig slurry, TPS treated pig slurry) for
each winter wheat growth stage over the measurement period.
Each data point represents the mean of three chambers used
per treatment. Error bars have been removed to aid visualisa-
tion. The dates of each growth stage, and the average daily air
temperature and total rainfall per winter wheat growth stage
are shown in TableS7
Fig. 4 Mean 2-h fluxes of CH4 for each fertiliser treatment (IF
inorganic fertiliser, PS pig slurry, TPS treated pig slurry) for
each winter wheat growth stage over the measurement period.
Each data point represents the mean of three chambers used
per treatment. Error bars have been removed to aid visualisa-
tion. The dates of each growth stage, and the average daily air
temperature and total rainfall per winter wheat growth stage
are shown in TableS7
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no clear diurnal trend in CH4 fluxes for any of the
treatments at any of the WW growth stages (Fig.4).
Yield response
The average total WW DM yield did not vary sig-
nificantly between treatments (Table2) and ranged
from 22.75 ± 1.31t ha−1 (PS) to 25.21 ± 3.68t ha−1
(TPS), which is slightly higher than that reported
for the entire field (22.1 ± 3.4t ha−1). Winter wheat
grain yield ranged from 13 ± 1.2 t ha−1 (PS) to
14.5t ha−1 (TPS), which is slightly higher than that
reported for the entire field (12.9 t ha−1). At har-
vest, the harvest index was similar between treat-
ments (Table2). Dry matter yield, total C and N
content, grain yield, grain C and N content, and
grain protein content were not significantly dif-
ferent between any of the treatments (P = > 0.05);
NUEtotal and NUEgrain were highest for IF and
lowest for TPS and were not significantly differ-
ent between any of the treatments (Table2). Mean
GHGI was highest from TPS and lowest from
IF (Table 1) and was not significantly different
between treatments (P = 0.1).
Discussion
Plasma treatment of pig slurry increased N2O
emissions
The large peaks of N2O following the two applica-
tions of treated pig slurry are responsible for TPS
having the highest cumulative N2O emissions. Simi-
larly, the smaller N2O peak following the second
application of pig slurry to PS is responsible for this
treatment having the second highest cumulative N2O
emissions relative to IF. Elevated N2O fluxes follow-
ing N fertiliser application are well-documented and
are often attributed to fertiliser N becoming avail-
able for conversion to N2O shortly after applica-
tion, as there is competition between plant uptake
and soil microbes for the N (Ma etal. 2013; Officer
etal. 2015). Many studies have observed higher N2O
emissions from crops fertilised with organic ferti-
liser, or a combination of organic and inorganic fer-
tiliser, compared to those amended with inorganic
fertiliser only (Pelster etal. 2012; Ball et al. 2014;
Yang et al. 2015). Organic fertilisers have a higher
labile C content which is easily decomposed by soil
Table 2 Seed planting density, total biomass and crop yield,
harvest index, whole crop and grain C and N content, total C
and N removed in whole crop and grain, proportion of total
crop N in grain, grain protein content, nitrogen use efficiency
of total biomass (NUEtotal) and grain yield (NUEgrain), and
the proportion of applied N lost as N2O–N for each treat-
ment (IF inorganic fertiliser, PS pig slurry, TPS treated pig
slurry) ± standard deviation (SD) where appropriate
Note that whole crop refers to the entire harvested plant (i.e., chaff, grain and stalk). Samples taken from plots using a 0.5 m2 quadrat
(N = 3). Across each row, the same letters indicate no significant difference in the variable of interest between fertiliser treatments
Fertiliser treatment IF PS TPS
Planting density ± SD (seeds m2)383.33 ± 137.7 400 ± 114.6 341.67 ± 104.1
Total biomass yield ± SD (t DM ha−1)23.76 ± 1.5 a 22.75 ± 1.3 a 25.21 ± 3.7 a
Grain yield ± SD (t ha−1)13.05 ± 0.9 a 12.98 ± 1.2 a 14.84 ± 2.7 a
Harvest index ± SD (%) 54.92 ± 1.1 a 57 ± 1.7 a 58.66 ± 2.3 a
Whole crop C content ± SD (%) 40.71 ± 0 a 40.58 ± 0.2 a 40.57 ± 0.1 a
Total C removed in whole crop (t ha−1)9.67 ± 0.6 a 9.23 ± 0.5 a 10.23 ± 1.5 a
Grain C content ± SD (%) 39.06 ± 0.7 a 38.80 ± 0.4 a 38.84 ± 0.8 a
Whole crop N content ± SD (%) 0.78 ± 0.1 a 0.79 ± 0 a 0.78 ± 0.1 a
Total N removed in whole crop (t ha−1)0.18 ± 0 a 0.18 ± 0 a 0.2 ± 0 a
Grain N content ± SD (%) 1.29 ± 0.1 a 1.23 ± 0.1 a 1.22 ± 0.1 a
Total N removed in grain (t ha−1)0.17 ± 0 a 0.16 ± 0 a 0.18 ± 0 a
% of total crop N in grain 90.78 ± 1.9 a 88.93 ± 9.6 a 93.21 ± 11.6 a
Grain protein content ± SD (%) 6.17 ± 0.6 a 6.64 ± 0.8 a 5.97 ± 0.7 a
NUEtotal (%) 83.64 ± 3.7 a 81.69 ± 1 a 77.81 ± 17.4 a
NUEgrain (%) 75.89 ± 2.4 a 72.63 ± 7.6 a 71.89 ± 15 a
% of applied N lost as N2O-N 0.6 ± 0.1 a 0.9 ± 0.1 a 4 ± 0.5 a
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microorganisms and releases mineralizable N for the
production of N2O (Hangs and Schoneau 2022); this
is likely to have caused the higher N2O emissions
from TPS and PS compared to IF. Furthermore, the
pig slurry and treated pig slurry had a higher con-
tent of fine solids than the inorganic fertiliser; fine
solids block soil pores and restrict oxygen move-
ment through soil, which creates favourable condi-
tions for N2O production (Chadwick etal. 2000). We
found that the plasma induction process increased the
nitrate–N content of the pig slurry; the higher content
of inorganic N combined with the C in the pig slurry
is likely to be responsible for the higher N2O emis-
sions (Shurpali etal. 2016; Li etal. 2022) from TPS
compared to PS. Mousavi etal. (2023) found that the
nitrification potential of plasma-treated pig slurry was
higher than that of other fertilisers due to its higher
volatile organic C content, which reduces ammonia
immobilisation, and so may also explain the higher
N2O emissions from TPS. Denitrification is highly
influenced by pH, with denitrification being slowed
or even inhibited at lower pH levels (Liu etal. 2010;
Olaya-Abril et al. 2021). At lower pH, the transfor-
mation of N2O to nitrogen gas is inhibited, meaning
that the N2O is available to be emitted from the soil
(Liu etal. 2010; Olaya-Abril etal. 2021). The lower
pH of the treated pig slurry relative to the untreated
pig slurry (Table S3) may therefore also explain the
higher N2O emissions from TPS. It should be noted
that the amount of available N applied to TPS was
slightly higher than to PS and IF which may have con-
tributed to its higher N2O emission, although because
the N2O emissions from TPS are so much higher than
the other two treatments, it is highly unlikely that this
discrepancy is the only reason.
A higher soil moisture content can restrict aera-
tion and reduce soil oxygen concentration, creating
favourable conditions for denitrification and N2O
emission (Westphal etal. 2018; Kostyanosvky etal.
2019; Li et al. 2022). This can explain the higher
N2O emissions from TPS and PS, as the relation-
ship between N2O and WFPS was higher for these
treatments than IF, and WFPS appeared highest
at TPS. The lack of response of N2O fluxes to the
applications of inorganic fertiliser across all treat-
ments is explained by the drought conditions expe-
rienced during the study. The inorganic fertilisers
were applied in the form of solid granules (appli-
cation 1) or a small volume of liquid (subsequent
applications), which did not wet the soil enough to
stimulate N2O emissions. Verdi et al. (2019) also
found low N2O emissions from a dry soil when
solid inorganic fertiliser was added. The volume of
liquid applied as pig slurry and treated pig slurry
was greater, and thus wetted up the soil more,
inducing N2O emission.
Plasma treatment of pig slurry decreased CH4
emissions
The immediate peaks in CH4 fluxes following the
two applications of pig slurry are responsible for
PS having the highest total CH4 fluxes. Methane is
produced during pig slurry storage as the conditions
and C content of the slurry facilitate methanogene-
sis; the CH4 is dissolved into the pig slurry and then
volatilised and emitted to the atmosphere following
slurry application (Rochette and Cote 2000; Bas-
tami et al. 2016). Severin etal. (2015) also meas-
ured higher CH4 emissions from crops amended
with pig slurry. The small CH4 uptake by IF and
TPS is not unexpected, as methanotrophy occurs
in well-drained agricultural soils (Serrano-Silva
etal. 2014). Inorganic fertiliser does not contain a
C source to facilitate methanogenesis (Moreno-Gar-
cia etal. 2020), and thus CH4 production, and the
plasma induction process prevents CH4 production
during slurry storage by acidifying the slurry and
reducing its pH (Tooth 2021; Petersen etal. 2012;
Overmeyer etal. 2021; Ambrose etal. 2023), so no
CH4 was emitted from IF and TPS upon application.
There is the potential for CH4 to be produced in
soil, and then emitted, following the application of
slurry due to the anoxic conditions created by rapid
C mineralisation after the input of C in the organic
fertiliser (Le Mer and Roger 2001; Yuan et al.
2019), this accounts for the elevated CH4 emissions
from PS. The lower pH of the treated pig slurry, as
a result of acidification during plasma treatment,
prohibiting methanogenesis during storage also
appears to inhibit CH4 production on application to
the field, as the C input via treated pig slurry appli-
cation does not induce CH4 emissions. The plasma
induction process therefore has clear benefits in
terms of reducing CH4 emissions during the storage
and application of pig slurry to agricultural soil.
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CO2-equivalent emissions and GHGI highest from
plasma-treated pig slurry
Nitrous oxide has a higher global warming potential
(273) than CH4 (27.9) (Smith et al. 2021), and, as
N2O emissions were considerably higher from TPS
compared to the other treatments, CO2-equivalent
emissions were therefore also highest from TPS. The
higher CH4 fluxes from PS compared to TPS and
IF were not large enough to outweigh the high N2O
fluxes from TPS when converted to CO2-equivalent.
Across the literature, cumulative CO2-equivalent
fluxes from WW fertilised with 100–300kg inorganic
N ha−1 range from 15 to 102.5g CO2-equivalent m−2
(Sainju et al. 2022; Huang et al. 2013) (Table S6);
the CO2-equivalent emissions we measured from
IF are within this range. There is a lack of data on
CO2-equivalent emissions from pig slurry when
used as an organic fertiliser, presenting a significant
research gap that must be addressed to enhance the
understanding of the impacts of fertiliser type on
GHG emissions. As all treatments received a simi-
lar amount of plant-available N, the lack of influence
of treatment type on the WW growth, including DM
yield, grain yield and grain protein content is not
unexpected. Cai etal. (2013) also observed no signifi-
cant difference in grain yield between crops amended
with a similar N rate of inorganic and organic ferti-
lisers. Our results show that it is possible to replace
over half of inorganic N fertiliser with organic N fer-
tiliser and achieve the same yield. As yield was not
significantly different between the treatments, this
meant that GHGI followed the trend of cumulative
CO2-equivalent emissions, with the highest fluxes
from TPS. When considering WW yield, the phos-
phorus and potassium applied to the crop via the fer-
tiliser treatments should be noted—the pig slurry and
treated pig slurry contained phosphorus and potas-
sium whereas the inorganic fertiliser did not. As soil
potassium data is not available, it is not possible to
assess whether this was a factor limiting crop produc-
tion, however it is unlikely as the yield of ~ 12t ha−1
for all treatments is high, and the soil was not P lim-
ited (P index of 3). As we consider cumulative emis-
sions, it is also important to note that ~ 6 weeks of
data are not included in this study due to an error
with the GHG measurement chambers. Given the uni-
form and consistent flux pattern in the weeks prior
to this, and the fact that there were no N fertiliser
applications during this time, we propose that the
addition of this missing data would have a minimal
impact on the cumulative emissions.
Diurnal N2O emissions observed outside of N2O
peaks
The diurnal pattern and peak of N2O emissions dur-
ing the middle of the day (observed from Extension
S10 onwards) for all treatments coincides with maxi-
mum CO2 uptake. This pattern was also reported in a
review by Wu etal. (2021) who found that over half
of the datasets reviewed observed N2O fluxes peak-
ing during the day. Chadwick etal. (2000) and Keane
etal. (2018) hypothesise that increases in soil temper-
ature, WFPS and PAR increased N2O fluxes. Further-
more, Keane et al. (2018) propose that, as C avail-
ability is a key driver of denitrification, higher PAR
and temperature during the middle of the day would
increase photosynthate exudation and microbial res-
piration, reducing oxygen availability, and stimulating
denitrification and N2O emission. Our results support
these hypotheses, as we found that, when excluding
fluxes measured within 0–7days of the first two fer-
tiliser applications, N2O fluxes increased with WFPS
and PAR. The Tillering S5 and Extension S6 growth
stages coincided with the applications of pig slurry
and treated pig slurry, which subsequently caused
peaks of N2O emission, and so no diurnal patterns in
N2O emissions were observed from any treatments
during these growth stages.
Implications for research and policy
We show that treating pig slurry with plasma-
induction does not reduce overall non-CO2 GHG
emissions, in fact it increases them in compari-
son to untreated pig slurry and inorganic fertiliser.
Although soil CH4 emissions were reduced by
treating pig slurry with plasma induction, N2O soil
emissions from plasma-treated slurry were consid-
erably greater than non-treated slurry. Furthermore,
the CO2-equivalent emissions from the organic fer-
tiliser treatments (TPS and PS) were higher than
those from the inorganic fertiliser treatment (IF).
These trade-offs between N2O and CH4 emissions
highlight the need to continue the development of
innovative technologies to improve agricultural
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sustainability. Whilst other research has found ben-
efits of the use of plasma-treated slurries, such as
lower ammonia emissions (Gillbard 2023) and posi-
tive effects on soil fauna (Mousavi etal. 2022), the
high N2O emissions found in our study show that
more research is required to determine how these
emissions can be reduced. This may include de-
watering slurries or using nitrification inhibitors to
reduce N2O emissions associated with the applica-
tion of organic fertilisers to soils to improve on-
farm waste management and farm adherence to
agricultural policy (Ruser and Schulz 2015; Willen
et al. 2016). Further research exploring the influ-
ence of fertiliser type on GHG emissions should
also measure fluxes from a control treatment receiv-
ing no fertiliser, which would enable the calcula-
tion of emission factors, and from a range of envi-
ronments to assess the influence of climate and soil
variables. Whilst we show that, overall, differences
in GHG emissions were considerable between treat-
ments, the cumulative N2O and CH4 emissions were
not significantly different. This is likely to be due
to the small number of replicates per treatment
(N = 3). A replicated study with both an increased
sample size per treatment and control treatment
would strengthen the results. As this experiment
only focuses on emissions from fertiliser applica-
tion until ~ 6 weeks before harvest, future trials
should be longer-term, measuring GHG emissions
across a full crop season as well as across years to
account for inter-annual variability. It is crucial that
this research is conducted prior to the commerciali-
sation of new technologies for organic waste man-
agement. It should be noted that the plasma induc-
tion process reduced slurry pH from ~ 7 to below 5
(TableS3), and that slurry acidification is known to
reduce ammonia emissions by 70% (Kupper et al.
2020). Measuring ammonia emissions alongside
GHGs would provide a more comprehensive under-
standing of the emissions associated with the use
of agricultural fertilisers and ensure that all trade-
offs are fully accounted for. These measurements
should be integrated into dynamic biogeochemical
models and life-cycle analyses to account for other
significant emissions associated with the use of
agricultural fertilisers, such as those generated in
fertiliser manufacturing from the Haber-Bosh pro-
cess, and allow the full environmental and climatic
impact of fertiliser production and application to be
ascertained.
Conclusion
The use of plasma-treated pig slurry as an organic
soil amendment reduced soil CH4 emissions relative
to non-treated pig slurry after application. Plasma-
treated slurry increased N2O emissions consider-
ably, however, which outweighed the savings from
CH4 reduction and so CO2-equivalent emissions
were greater from treated than non-treated pig slurry.
Winter wheat yield was high for all treatments and
was not affected by the fertiliser type used. Plasma-
treated pig slurry is therefore not currently a suitable
soil amendment should farmers wish to reduce GHG
emissions from their land. Furthermore, the applica-
tion of organic fertilisers (i.e., treated and non-treated
pig slurries) resulted in higher GHG emissions than
when inorganic fertiliser was applied. We there-
fore recommend that our results be integrated into a
life-cycle analysis, to determine whether the use of
organic fertilisers still emit more than inorganic fer-
tilisers when the associated downstream GHG emis-
sions are considered. In addition, future research
should focus on how N2O emissions can be reduced
from plasma-treated pig slurry, conducting plot tri-
als to assess the effect of fertiliser rate, timing and
placement.
Acknowledgements The authors would like to acknowledge
the use of the University of Leeds Research Farm and thank
Jarrod Benson, farm manager, for assistance obtaining materi-
als for the field experiment, Santiago Clerici for assisting with
experimental setup, Rob Yardley for providing farm manage-
ment information and advice, David Ashley for laboratory and
analytical support, Alexander Cumming and Nick Nickerson
for data analysis advice, and Lizzie Sagoo for guidance on fer-
tiliser management practices.
Author contribution Isobel L Lloyd: Conceptualisation,
Methodology, Formal analysis, Investigation, Data curation,
Writing—Original draft, Visualisation, Funding acquisition.
Richard P Grayson: Conceptualisation, Methodology, Inves-
tigation, Resources, Writing—Review and editing, Supervi-
sion, Funding acquisition. Marcelo V Galdos: Conceptualisa-
tion, Methodology, Resources, Writing—Review and editing,
Supervision. Ross Morrison: Conceptualisation, Methodology,
Resources, Writing—Review and editing, Supervision. Pippa J
Chapman: Conceptualisation, Methodology, Resources, Writ-
ing—Review and editing, Supervision, Funding acquisition,
Project administration.
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Funding This work was supported by the Leeds-York-
Hull Natural Environmental Research Council (NERC) Doc-
toral Training Partnership (DTP) Panorama under grant NE/
S007458/1.
Data availability The dataset generated during the current
study is under embargo at https:// doi. org/ 10. 5285/ 4ed00 23e-
da9b- 45a8- 86de- 3a371 cc7dc c1, but can be made available by
the corresponding author on reasonable request.
Declarations
Competing interests The authors declare no competing inter-
ests.
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