FERTILIZANTES FOSFORADOS

Revista científica de la Asociación Argentina de la Ciencia del Suelo

NITROUS OXIDE EMISSIONS FROM A TYPICAL ARGIUDOL SOIL

Vanina Rosa Noemí Cosentino 12*, Mónica Gabriela Pérez 3, Mauro Ezequiel Ostinelli 3,
Romina Ingrid Romaniuk 1, Natalia Andrea Mórtola 1, Pedro Federico Rizzo 4,
Alejandro Oscar Costantini 13

1 Instituto Nacional de Tecnología Agropecuaria, Centro de Investigación de Recursos Naturales, Instituto de Suelos,
Buenos Aires, Argentina.
2 Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina.
3 Facultad de Agronomía, Universidad de Buenos Aires, Argentina.
4 Instituto Nacional de Tecnología Agropecuaria, Instituto de Microbiología y Zoología Agrícola, Laboratorio de
Transformación de Residuos, Argentina.

ABSTRACT

Diversification in fertilizer sources will be necessary to meet the growing demand for food worldwide. For
this reason, organic amendments emerge as a synthetic fertilizers alternative. Composting organic waste
stabilizes the nitrogen (N) content and delays N release to the soil. Applying composted amendments to the
soil could reduce the losses of N, including nitrous oxide (N2O), a greenhouse gas with great potential for
global warming. The objective of this work was to evaluate the N2O emission in typical Argiudol soil after
applying a traditional synthetic fertilizer, raw poultry manure, composted poultry manure and control soil.
Cumulative N2O emission rates during the 32 days of the trial were 1273, 965, 423, and 244 g N2O-N/ha-1
from the soil using urea, poultry manure, composted poultry manure, and control, respectively. Our results
suggest that the application of composted poultry manure to the soil produces lower N2O emissions than
the application of raw poultry manure or urea. The presence of more stabilized compounds in the compos-
ted manure decreases the soil nitrate availability.

Keywords: amendment – greenhouse gases - organic fertilizer - nitrogen losses.

EMISIONES DE ÓXIDO NITROSO DESDE UN SUELO ARGIUDOL TÍPICO

RESUMEN

El aumento de las fuentes de fertilización será necesario para satisfacer la creciente demanda de alimentos
en todo el mundo. Por este motivo, las enmiendas orgánicas surgen como una alternativa a los fertilizantes
sintéticos. El compostaje de residuos orgánicos estabiliza el contenido de nitrógeno (N) y retrasa la libe-
ración de N al suelo. La aplicación de enmiendas compostadas al suelo podría reducir las pérdidas de N,
* Autor de contacto: incluido el óxido nitroso (N2O), un gas de efecto invernadero con gran potencial de calentamiento global.
[email protected] El objetivo de este trabajo fue evaluar la emisión de N2O desde un suelo Argiudol típico luego de aplicar un
fertilizante sintético tradicional, guano de ave crudo y compostado y un suelo control. Las tasas emisión
Recibido:
10-02-22
de N2O acumuladas durante los 32 días que duro el ensayo fueron 1273, 965, 423 y 244 g de N2O-N ha-1
desde el suelo con aplicación de urea, guano de ave, compost de guano de ave y control, respectivamente.
Recibido con revisiones: Nuestros resultados sugieren que la aplicación de compost de guano al suelo produce menores emisiones
10-06-22 de N2O que la aplicación de guano de ave crudo o de urea. La presencia de compuestos más estabilizados
en el compost de guano disminuye la disponibilidad de nitrato del suelo.
Aceptado:
10-06-22 Palabras claves: enmienda - gases de efecto invernadero - fertilizantes orgánicos - pérdidas de nitrógeno.

102 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

INTRODUCTION

Due to the increase in the average individual incomes and the population growth, projections for 2050 indi-
cate the necessity to increase food production to supply worldwide demand. This food demand is expec-
ted to increase by 60% compared to 2005/2007 (Alexandratos, 2012; Godfray, 2018), and could affect the
quality of soils, resulting in a decrease in productivity and the ability to provide ecosystem services (Popp
et al., 2014).

World egg production increased by 25% from 2003 to 2013 (Rizzo et al., 2020), and part of the large amount
of waste that it generates, is applied to the soil as fertilizer in agriculture (Quiroga et al., 2010). Poultry ma-
nure is a source of nutrients, mainly nitrogen (N), which could satisfy part of the nutritional requirements of
crops (Gómez, 2000). However, although the direct application of raw organic waste to the soil, as fertilizer,
can increase crop yield, this practice can promote nitrogen losses through volatilization of ammonia (NH3),
leaching of nitrate (NO3-), or by the emission of nitrous oxide (N2O) (Mahmud et al., 2021). In this sense,
increasing their N2O emissions from croplands is expected due to the extensive use of nitrogen fertilizers
and organic amendments associated with increased food production (Galloway et al., 2008). Therefore, it
is essential to adjust the amount of waste required by the system, to minimize the environmental cost that
N loss may cause. For this, it is necessary to develop fertilization strategies with low environmental impact.

The terrestrial biosphere can release or absorb greenhouse gases (GHG), and thus it has a vital role in regu-
lating the atmospheric composition and climate (Tian et al., 2016). The N2O is a GHG that has a half-life time
in the atmosphere of 121 years (Intergovernmental Panel on Climate Change [IPCC], 2014) with a global war-
ming potential of 265 times greater than CO2 contributing around 6% to the global warming effect (Rapson
& Dacres, 2014). Nitrification and denitrification are the main microbial processes that produce N2O in the
soil, with the N2O emission produced by the nitrification process (aerobic) being lower than that produced
by the denitrification process (anaerobic; Davidson 1991). Both processes are affected by the availability
of N, temperature and water content, between other factors (Steenwerth & Belina, 2008). Globally, cropland
area is around 13% of the ice-free land area and produces about 40% of total soil N2O emissions emitted
from agriculture (Paustian et al., 2016). In this context, evaluations of management practices that minimize
the N2O emissions are fundamental to offer adaptable mitigation strategies to different management.

Poultry manure composting is an alternative management that reduces the volume of waste, facilitating
storage, transportation, and application (Tyson & Cabrera, 1993). Some studies showed that the compos-
ting process immobilizes N and stabilizes organic matter, delaying the release of nutrients (Bustamante et
al., 2008; Tyson & Cabrera, 1993). The risk of N losses increases when the available N for crops is higher
than the demand. For this reason, the slow release of nutrients from the composted waste can reduce har-
mful environmental consequences such as N losses by leaching or emission to the atmosphere (Snyder et
al., 2009). Hence, countries with significant agricultural production possess a high potential to replace part
of synthetic fertilizers uses with organic residues amendments. The use of these practices could contribute
to the circular economy and the principles of sustainable agriculture. To achieve this, the quantification of
possible externalities caused by organic amendments in the biogeochemical cycles is necessary.

The reduction of GHG emissions from agricultural systems is a key factor to sustainable production. The
N2O emissions quantification from amended soil with organic materials will allow the design of sustainable
agricultural systems (Hénault et al., 2012). Although some authors studied N2O emissions after residues
application (Gregorutti & Caviglia, 2017; Hayakawa et al., 2009), few studies compared N2O emissions ge-
nerated in fertilization systems with raw and composted poultry manure. The aim of this study was to eva-
luate the N2O emission from a control soil and after application of raw poultry manure, composted poultry
manure and chemical fertilizer.

MATERIALS AND METHODS

Study site and experimental design

The study was performed during the winter 2017, from July 3 to August 4, on an experimental area under a
pasture composed mainly of Festuca sp. and Trifolium repens. The experiment was made at the National
Agricultural Research Center (CNIA) of the National Institute of Agricultural Technology (INTA) in Hurlin-
gham, Buenos Aires, Argentina (34 ° 36 ‘15 “S, 58 ° 40’ 16” O). The soil was classified as a typical Argiudol
(INTA, 2019). The topsoil has a silty-loam texture, while the subsoil has a clay loam texture.

103 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

The experiment had a randomized complete block design (RCBD) with three blocks and four treatments. Treat-
ments consisted of poultry manure (PM), composted poultry manure (CPM), urea (U) as synthetic fertilizer,
and control (C, no added N) (n = 3 for each treatment). Within each block, a plot of 25 m2 was settled randomly
for treatments application. 260 kg ha-1 of urea, 1770 kg ha-1 of PM and 6944 kg ha-1 of CPM were applied. The
doses of PM, CPM, and U were calculated considering the pasture requirement (120 kg N ha-1), the N-NO3- the
content of the soil, and the different contents of N of the applied materials were considered. The application of
the amendments was done superficially and by hand. During the experiment, the average temperatures were
12 °C and 13°C for soil and air, respectively, and the accumulated precipitation was 93,6 mm.

AMENDMENTS PRECEDENCY

Poultry manure (PM) was obtained from an automated poultry farm located at CNIA, INTA. The compost
(CPM) was made by mixing 50% PM and 50% horse litter (v / v), using an open composting system with
manual turning. The composting process lasted 90 days, reaching the hygiene requirements (temperature ≥
55 ° C) established in the Argentine Composting Standard (SCyMA & SENASA, 2019). The characterization
of PM and CPM is shown in Table 1.

Table 1. Mean values of total organic carbon (%), total nitrogen Kjeldahl (%) and the C / N ratio of the poultry manure and
the composted poultry manure. Values are expressed on a dry weight basis (Mean ± SEM).

Tabla 1. Valores medios de carbono orgánico total (%), nitrógeno total Kjeldahl (%) y la relación C / N del guano de ave y
del guano de ave compostado. Los valores se expresan sobre una base de peso seco (Media ± SEM).

NITROUS OXIDE EMISSION

Fifteen N2O samplings were taken in 32 days. They were collected 1, 2, 3, 4, 5, 7, 9, 11, 14, 16, 18, 21, 23, 25,
and 32 days after the application (DAA) of the treatments. The sampling effort tried to capture as well as
possible the changes in N2O emissions to minimize the error. The sampling of N2O emissions was perfor-
med using closed-static chambers (surface 0,13 m2, height 0,125 m) with an iron frame base and a PVC
cover according to the criteria of Rochette & Eriksen-Hamel (2008). The chamber headspace was connec-
ted to the exterior by a two-way valve for gas sampling. Bases were inserted into the soil (0,05 m depth) 24
h before the beginning of the monitoring period, and they were not moved or rotated during the trial period t
(Alves et al., 2012; Chirinda et al., 2019). Gas samples were taken from the chamber headspace at intervals
of 0, 15, and 30 min after closing the chambers. The collection was made with a syringe (60 mL) and a part
of it was transferred into 10 cm3 glass vials after evacuation using a manual vacuum pump with a manome-
ter (Cosentino et al., 2020). Gas sampling was performed between 09:00 and 12:00, which best represents
the average daily N2O emission in the study area (Cosentino et al., 2012). Within seven days of sampling,
N2O was analyzed in the laboratory with a GC 6890 Agilent Technologies Network gas chromatograph (Agi-
lent Network GC System, A´ ECD, Santa Clara, CA, USA).

The N2O emission (f) was calculated as:

where ΔC/Δt is the change in N2O concentration in the chamber during the deployment time Δt, V is the
volume of the chamber (16,3 dm3), A is the soil area (0,13 m2) covered by the chamber, m is the molecular
mass of N2O and Vm is the molar volume of N2O. Gas emission was calculated as the increase in concen-
tration during deployment time (period while the chamber is closed).

104 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

Once a week and at the same time as the N2O emission, topsoil temperature was measured at 0,10 m depth
beside each chamber. After gas sampling, soil samples (0–0,2 m depth) were taken from the chamber perime-
ter and analyzed for NO3- -N by nitration of salicylic acid method (Cataldo et al., 1975). The bulk density (BD)
was determined by the cylinder method with 100 cm³ and 0.05 m in diameter (Blake, 1965) and gravimetric
water content (GWC, by drying in an oven until constant weight). Water filled pore space (WFPS) were calcu-
late using bulk density and gravimetric water content, and assuming a particle density (Dp) of 2,65 Mgm−3.

Cumulative emissions for the total trial period (32 days) after the application were calculated using the
linear interpolation method, and the emission factors were determined (Dorich et al., 2020). To interpolate
the punctual emissions, N2O emissions were converted to a daily scale. N2O emission values unmeasured
were calculated from the average between the emissions measured the day before and the day after. Finally,
emission factors were calculated from the difference in the total emissions from each treatment (MT), and
the control treatment (MC), divided by the N applied, as described by Equation:

where EF is emission factor (N2O–N emitted as % of N applied) and Treatment N applied is the N applied
(total kg N ha-1).

Statistical differences in the N2O emission soil temperature, WFPS, and soil NO3- -N between treatments
for each date were tested with ANOVA. The software used was INFOSTAT (Di Rienzo et al., 2008). When the
ANOVA indicated significant differences (p < 0.05), the treatment means were compared using the Tukey
test (α = 0,05). Linear regressions and correlation analysis were also performed using INFOSTAT..

RESULTS

The N2O emission ranged between 0,4 and 574 μg N2O-N m-2 h-1 with high variability even between repeti-
tions. Despite the similar pattern observed by all the treatments over time, the N2O emission rate presented
significant differences (p <0.05) between the treatments in 10 of the 15 sampling dates (Figure 1a). On ave-
rage, the treatment with the application of U presented the highest N2O emission, followed by the treatment
with the application of PM.

105 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

Figure 1. Evolution of a) the emission of N2O in the Control (C, ) and after the application of Poultry Manure (PM, ),
Composted Poultry Manure (CPM, ) and Urea (U, ); b) WFPS (-  -) and rainfall , and c) the soil temperature
(-  -). The horizontal line represents the water filled pore space (WFPS) value of 60% (b) and the corresponding tempe-
rature value of 10 °C (c). Different letters indicate significant differences between treatments for each measurement day.

Figura 1. Evolución de a) la emisión de N2O en el Control (C, ) y luego de la aplicación de Guano de Ave (PM, ), Guano
de ave Compostado (CPM, ) y Urea (U, ); b) Espacio Poroso Saturado con Agua WFPS (-  -) y lluvia , y c) la
temperatura del suelo (-  -). La línea horizontal representa el valor del espacio poroso lleno de agua (WFPS) del 60% (b)
y el valor de temperatura correspondiente de 10 ° C (c). Letras diferentes indican diferencias significativas entre trata-
mientos para cada día de medición.

At 5, 21, 23, 25, and 32 DAA, treatment U presented significantly higher N2O emission rates compared to the
other treatments, followed by PM, and lastly by the CPM and C treatments. However, PM presented the highest
N2O emission on 9 DAA, followed by treatment CPM and finally by U and C (without significant differences
between both). The treatments with CPM application and the control presented the lowest emission values of
N2O at 5, 7, 16, 18, 21, 23, 25, and 32 DAA, with significant differences between them at 7 and 23 DAA. For the
rest of the days, no significant differences were observed in N2O emission between treatments (Figure 1a).

On 1, 2, 3, and 4 DAA, the N2O emission values were low and in concordance with low WFPS values (less
than 60%, Figure 1b). Since 5 DAA, the N2O emission values were higher and mainly followed the changes
in the WFPS. On 14, 16, 18, 21, and 32 DAA, N2O emissions were lower than those expected from the WFPS,
probably due to the low soil temperatures (Figure 1c). When the soil temperature was less than 10 °C, the
N2O emission values were intermediate and less variable. Finally, on 5, 7, 9, 11, 23, and 25 DAA, when the
soil temperature exceeded 10 °C, and WFPS was higher than 60%, the N2O emission values were high and
highly variable (Figure 1).

The soil NO3- -N content presented significant differences (p <0.05) between treatments at 7, 14, 21 and
32 DAA (U > PM > CPM = C). U treatment presented the highest values in all the dates evaluated, with sig-

106 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

nificant differences compared to the other treatments at 7, 14, and 21 DAA. The U treatment was followed
by PM and lastly by CPM and C (Figure 2). In addition, during the first 21 DAA, the nitrate content in the soil
increased at a higher rate with the application of U, followed by PM, and finally by C and CPM soils. Despite
those differences, the soil NO3- -N during the experiment was higher than the threshold of 5 mg kg-1 accor-
ding to Dobbie et al. (1999), and then it was not considered a limiting factor for N2O emissions.

Figure 2. Evolution of the soil nitrate content (NO3- -N) in Control (C, ) and after the application of the Poultry Manure
(PM, ), Composted Poultry Manure (CPM, ) and Urea (U, ). Bars indicate the standard error of the mean (SEM).
The different letters indicate statistically significant differences between the treatments for each sampling date.

Figura 2. Evolución del contenido de nitrato del suelo (NO3- -N) en el Control (C, ) y después de la aplicación del Guano
de Ave (PM, ), Guano de Ave Compostado (CPM, ) y Urea (U, ). Las barras indican el error estándar de la media
(SEM). Las diferentes letras indican diferencias estadísticamente significativas entre los tratamientos para cada fecha
de muestreo.

When all the treatments and moments were analyzed together, a direct relationship between the N2O emis-
sion and the soil NO3- -N content of the soil was not demonstrated (data not shown). When analyzing each
sample date in isolation, the highest N2O emissions occurred in the treatments with the highest content
average NO3- -N. However, there were not significant correlation between those variables (Figure 2).

At 32 DAA the cumulative emission rates were on average 1273 ± 30,78 g N2O-N ha-1 from U, 965 ± 129,25
g N2O-N ha-1 from PM, 423 ± 67,06 g N2O-N ha-1 from CPM, and 244 ± 36,13 g N2O-N ha-1 from C. Then, the
soil N2O emission with CPM application was twice than C treatment, while soil emissions from PM and U
were similar (without significant differences between both) and approximately 4,5 times higher than those
observed in C (Figure 3).

Figure 3. Cumulative emissions of N2O in the Control (C) and after the application of the Poultry Manure (PM), Com-
posted Poultry Manure (CPM) and Urea (U) 32 DAA. The different letters indicate statistically significant differences
between the treatments.

Figura 3. Emisiones acumuladas de N2O en el Control (C) y después de la aplicación de Guano de Ave (PM), Guano de
Ave Compostado (CPM) y Urea (U) a los 32 DAA. Letras diferentes indican diferencias significativas entre tratamientos.

107 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

The emission factor (EF) for urea added to the soil was significantly greater than for PM and CPM (p <0.05),
with means of 0.86% (SE 0,03%). Finally, the EF for PM was significantly greater than for CPM (P <0.05), with
means of 0.6% (SE 0,13%) and 0,15% (SE 0,12%), respectively.

DISCUSSION

On 1, 2, 3, and 4 DAA, the N2O emissions were low, probably related to the low WFPS values (less than
60%, Figure 1b). The soil water availability plays a central role in the oxygen dynamics and, therefore, in the
activity of the different soil microorganisms (nitrifiers and denitrifiers). When the WFPS is low, the primary
process driving the N2O emission is the nitrification (aerobic), while when the WFPS increases, the denitri-
fication gains relevance (anaerobic; Davidson, 1991). Therefore, a minimum of 60% of WFPS is considered
a threshold value to find detectable emission rates, while values close to 80% are considered optimal for
denitrification and N2O emissions (Schindlbacher et al., 2004; Zechmeister-Boltenstern et al., 2007).

Since 5 DAA, the N2O emission was higher and mainly followed the changes in the WFPS. Shelton et al.
(2000) obtained a correlation between the N2O emission and the soil water content, at a WFPS range be-
tween 60 and 100%. On days 14, 16, 18, 21, and 32 DAA, N2O emissions were lower than those expected
from the WFPS contents, probably due to the low soil temperatures (Figure1c). Similar results were reported
by other authors (Cosentino et al., 2013; Perez et al., 2021). Finally, on days 5, 7, 9, 11, 23, and 25 DAA, when
soil temperature exceeded 10 °C, and WFPS was higher than 60%, the N2O emissions were high and highly
variables (Figure 1). Soil situations characterized by high temperatures and WFPS could generate relatively
high N2O production rates, as long the soil NO3- -N availability is not a limiting factor (Castaldi, 2000).

During the first 21 DAA, the soil nitrate content increased at a higher rate with the U application, followed
by PM and finally by C and CPM. These differences were due to the form in which the N was found in each
treatment. Several studies have shown that the composting process immobilizes N and produces mineral
N-associated organic matter that can be used as a source of organic materials delaying nutrient release
(Bustamante et al., 2008; Tyson & Cabrera, 1993). The slow release of nutrients can reduce adverse envi-
ronmental impacts such as N leaching in-depth or losses as N2O (Snyder et al., 2009). Rizzo et al. (2015)
worked with similar materials to use in the present experiment. These authors evaluated the composting
process of poultry manure, reporting higher unstable organic matter (labile organic matter) contents and
a large part of N as NH4+ -N in the raw poultry manure before composting. While in the composted poultry
manure, the organic matter was stabilized, and the N content was as organic N and as NO3- -N.

When all the treatments and moments were analyzed together, a direct relationship between the N2O emis-
sion and the soil NO3- -N content of the soil was not observed, this is possibly due to the multifactorial effect
of the regulatory variables of N2O emissions. The ecological stoichiometry approach provides a tool for
analyzing how the balance of the multiple factors required by soil organisms affects N2O production (Hes-
sen et al., 2004; Sterner & Elser, 2002). Similar results were found by Cosentino et.al (2013) in an agricultural
field in Argentina.

The highest N2O emissions were observed in those treatments with the highest NO3- -N contents. Howe-
ver, there were not significant correlation between those variables (Figure 2). Similar results were shown
by other authors who reported an increase in soil NO3- -N after adding organic amendments (Masaka et
al., 2014; Roig et al., 2012). According to Dalal et al. (2003), the rate of N2O emission by denitrification
increases with NO3- -N content if the soil presents predisposing conditions of moisture, temperature, and
availability of labile carbon.

In the present research, the N2O emission rates accompanied the changes in values of WFPS and tem-
perature when they were between 30-90% and 6-16 °C, respectively. Generally, the highest N2O emission
rates were observed at high levels of soil NO3- -N contents on those sampling dates where neither the soil
temperature nor the WFPS limited the N2O production. Similar results were reported by Dalal et al. (2010),
showing a positive correlation between the emission of N2O and soil NO3- -N content when the soil tempe-
rature ranged between 10 and 30 °C and the WFPS was between 30% and 80%.

The cumulative emissions in the present research were higher than the reported by Gregorutti & Caviglia
(2017). After 150 days of applying the equivalent of 450 Kg Nha-1 as poultry manure and 266 Kg N ha-1 of
chicken litter compost, observed cumulative N2O emissions of approximately 240 g N ha-1 and 100 g of N

108 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

ha-1, respectively. The authors attribute the low emissions to low WFPS, which never exceeded 60% (Gre-
gorutti & Caviglia, 2017). The cumulative N2O emissions observed in the present study were higher than the
found by authors such as Hayakawa et al. (2009). They applied 120 kg of N ha-1 of manure to a spinach crop,
with temperatures between 15 to 30ºC and WPFS between 40 and 70%, and they obtained accumulated N2O
emission values of 330 g of N2O-N ha-1 after 37 days. One of the reasons for the high emission observed in
the present trial could be the high rate of denitrification and, consequently, the production of N2O (Akiyama
& Tsuruta, 2003).

However, other authors such as Thornton et al. (1998) reported higher accumulated emissions, with values
of 3870 g of N2O-N ha-1 and 1640 g of N2O-N ha-1, 150 days after applying 336 kg of N ha-1 of manures.
The authors applied raw and composted manure (with 3,4% and 3,5% of total N respectively) to a batch with
Bermuda Grass, with a mean temperature of 23 ºC and WFPS between 20% and 80%. The authors attributed
these results to the high amount of residue applied to the soil. Kim et al. (2019) observed N2O emission of
10.8 kg ha-1 yr-1 by applying composted poultry manure. They attribute the N2O emission mainly to the ni-
trification process since soil moisture was low. Finally, as observed in the present research, Martín-Olmedo
& Rees (1999) reported high N2O emissions five days after applying poultry manure. The authors suggest
that the peak of N2O emission was related to the content of available organic carbon in the manure, which
is quickly used by N2O-producing microorganisms.

The EF for urea added to the soil (during 32 DAA) was 0,86%; this value is a little less that annual value re-
ported by the IPCC for the urea (2019). The high N2O emission reported during the present trial was possibly
associated with the high percentage of WFPS, which encourage denitrification emissions. Similarly, the EF
for PM and CPM (during 32 DAA) presented mean values of 0.6% and 0.15%, respectively. Thus, EFs were
greater than the annual value reported by the IPCC (2019). The IPCC states that the EF for poultry waste is
between 0,000-0,014 with an average value of 0,004, lower than the value obtained here; without reporting
EF for soils with the application of composted manure (IPCC, 2019). The difference between EF obtained in
the present research and reported by IPCC, is possibly due to the forms in which N are found in the residues.
Adding N to the soil, mainly NO3-, affects microbial activity and therefore N2O emissions. However, unlike
what happens with inorganic fertilizers such as urea, the time and intensity with which organic fertilizers
affect the activity of the microorganisms involved in the production of N2O from the soil is specific of each
residue. For this reason, EF from organic waste cannot be predicted from simple measurements such as
total N, which is a reasonably good estimator of EF from synthetic fertilizers as urea (Kim & Dale, 2008).

The higher soil cumulative emission and EF values after applying U and PM compared to those from the
soil with CPM application was possibly due to the differences in the N forms to each material. The immo-
bilization of nutrients during composting leads to a lower content of inorganic N readily available to soil
microorganisms, decreasing the N2O production by nitrification and denitrification processes.

CONCLUSION

According to our results, the application of composted poultry manure to the soil produced lower losses
of N as N2O than the application of raw poultry manure or chemical fertilizers like urea. In addition, the
presence of more stabilized compounds in the composted manure decreases the soil nitrate availability.
This less soil nitrate availability could maximize the synchronization between the availability of resources
and the grassland demand, minimizing the environmental losses. For this, soil amendment with com-
posted material could be considered sustainable alternative management to reduce the use of synthetic
fertilizers, improve soil health and contribute to climate change mitigation. Finally, to advance on this line
of research, more studies should be carried out to validate the emission factors for these manure mana-
gement alternatives. The use of default IPCC emission factors could be underestimating their impact on
the environment.

ACKNOWLEDGEMENTS

This work was supported by PNNAT 1128023 Project, PD I518 Project “Aprovechamiento de residuos, des-
cartes y subproductos agroalimentarios y agropecuarios: tecnologías para la obtención de alimentos y
bioproductos para cadenas productivas” and PD I058 Project “Emisiones (GEI) en los sistemas agropecua-
rios y forestales. Medidas de mitigación” (INTA, Argentina).

109 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

REFERENCIAS

Akiyama, H., & Tsuruta, H. (2003). Nitrous Oxide, Nitric Oxide, and Nitrogen Dioxide Fluxes from Soils after Manure and Urea Application.
Journal of Environmental Quality, 32, 423–431.

Alexandratos, N. (2012). World agriculture towards 2030 / 2050. The 2012 Revision PROOF COPY. ESA Work Pap. 12: 146.

Alves, B.J.R., Smith, K. A., Flores, R. A., Cardoso, A. S., Oliveira, W. R. D., Jantalia, C. P., Urquiaga, S. & Boddey, R. M. (2012). Selection of
the most suitable sampling time for static chambers for the estimation of daily mean N2O flux from soils. Soil Biology & Biochemistry,
46, 129–135.

Blake, G. (1965). Bulk Density. Methods of soil analysis. Part 1: Physical and mineralogical properties, including statistics of measurement
and sampling.

Bustamante, M. A., Paredes, C., Marhuenda-Egea, F. C., Pérez-Espinosa, A., Bernal, M. P. & Moral, R. (2008). Co-composting of distillery
wastes with animal manures: Carbon and nitrogen transformations in the evaluation of compost stability. Chemosphere, 72, 551–557.

Castaldi, S. (2000). Responses of nitrous oxide, dinitrogen and carbon dioxide production. Biology and Fertility of Soils, 32, 67–72.

Cataldo, D. A., Haroon, M. H., Schrader, L. E. & Youngs, V. L. (1975). Rapid colorimetric determination of nitrate in plant tissue by nitration
of salicylic acid. Communications in Soil Science and Plant Analysis, 6, 71–80.

Chirinda, N., Loaiza, S., Arenas, L., Ruiz, V., Faverín, C., Alvarez, C., Savian, J. V., Belfon, R., Zuniga, K., Morales-Rincon, L. A., Trujillo, C.,
Arango, M., Rao, I., Arango, J., Peters, M., Barahona, R., Costa, C., Rosenstock, T. S., Richards, M., Martinez-Baron, D. & Cardenas, L.
(2019). Adequate vegetative cover decreases nitrous oxide emissions from cattle urine deposited in grazed pastures under rainy season
conditions. Scientific Reports, 9, 1–9.

Cosentino, V. R. N., Fernandez, P. L., Figueiro, S. A. & Taboada, M. A. (2012). N2O emissions From a Cultivated Mollisol : Optimal Time of
Day for Sampling and the Role of Soil. Revista Brasileira de Ciência do Solo, 36, 1814–1819.

Cosentino, V. R. N., Figueiro Aureggui, S. A. & Taboada, M. A. (2013). Hierarchy of factors driving N2O emissions in non-tilled soils under
different crops. European Journal of Soil Science, 64, 550–557.

Cosentino, V. R. N., Romaniuk, R. I., Lupi, A. M., Gómez, F. M., Rimski Korsakov, H., Álvarez, C. R. & Ciarlo, E. (2020). Comparison of field
measurement methods of nitrous oxide soil emissions: from the chamber to the vial. Revista Brasileira de Ciência do Solo, 44:e0190100.

Dalal, R. C., Gibson, I., Allen, D. E. & Menzies, N. W. (2010). Green waste compost reduces nitrous oxide emissions from feedlot manure
applied to soil. Agriculture, Ecosystems & Environment, 136, 273–281.

Dalal, R. C., Wang, W., Robertson, G. P. & Parton, W. J. (2003). Nitrous oxide emission from Australian agricultural lands and mitigation
options: a review. Australian Journal of Soil Research, 41, 165–195.

Davidson, E. A. (1991). Fluxes of nitrous oxide and nitric oxide from terrestrial ecosystems. In J. E. Rogers & W. Whitman (Eds.). Microbial
production and consumption of greenhouse gases: methane, nitrógeno oxides, and halomethanes.

Di Rienzo, J. A., Casanoves, F., Balzarini, M. G., Gonzalez, L., Tablada, M. & Robledo, C. K. (2020). InfoStat versión 2020. Group InfoStat,
Universidad Nacional de Córdoba.

Dorich, C., Conant, R., & Grace, P. (2020). Global Research Alliance N2O chamber methodology guidelines: Guidance for gap-filling missing
measurements. Journal of Environmental Quality, 9, 1186–1202.

Galloway, J. N., Townsend, A. R., Erisman, J. W., Bekunda, M., Cai, Z., Freney, J. R., Martinelli, L. A., Seitzinger, S. P. & Sutton, M. A. (2008).
Transformation of the nitrogen cycle: Recent trends, questions, and potential solutions. Science, 320, 889–892.

Godfray, H. C. J., Aveyard, P., Garnett, T., Hall, J. W., Key, T. J., Lorimer, J., & Jebb, S. A. (2018). Meat consumption, health, and the environ-
ment. Science, 361(6399), eaam5324.

Gómez, J. (2000). Abonos orgánicos. Feriva S. A. Colombia.

Gregorutti, V. C. & Caviglia, O. P. (2017). Nitrous oxide emission after the addition of organic residues on soil surface. Agriculture, Ecosys-
tems & Environment, 246, 234–242.

Hayakawa, A., Akiyama, H., Sudo, S. & Yagi, K. (2009). N2O and NO emissions from an Andisol field as influenced by pelleted poultry ma-
nure. Soil Biology & Biochemistry, 41, 521–529.

Hénault, C., Grossel, A., Mary, B., Roussel, M. & LéOnard, J. (2012). Nitrous Oxide Emission by Agricultural Soils: A Review of Spatial and
Temporal Variability for Mitigation. Pedosphere, 22, 426–433.

Hessen, D. O., Agren, G. I., Anderson, T. R., Elser, J. J. & De Ruiter, P. C. (2004). Carbon sequestration in ecosystems: the role of stoichiome-
try. Ecology, 85, 1179–1192.

Instituto Nacional de Tecnología Agropecuaria (INTA). (2019). Instituto Nacional de Tecnología Agropecuaria. http://anterior.inta.gov.ar/
suelos/cartas/.

Intergovernmental Panel on Climate Change. (IPCC). (2014). Climate Change 201: Synthesis Report. Contribution of Working Groups I, II
and III to the Fifth Assessment Report of the Intergovernmental Panel on Climate Change.

Intergovernmental Panel on Climate Change. (IPCC). (2019). Intergovernmental panel on climate change. Refinement to the 2006 IPCC

110 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica
 FERTILIZANTES FOSFORADOS

Guidelines for National Greenhouse Gas Inventories. Volume 4. Agriculture, Forestry and Other Land Use. Chapter 10. Emissions from
livestock and manure management.

Kim, S. & Dale, B. E. (2008). Effects of nitrogen fertilizer application on greenhouse gas emissions and economics of corn production.
Environmental Science & Technology, 42, 6028–6033..

Kim, S. U., Ruangcharus, C., Kumar, S., Lee, H. H., Park, H. J., Jung, S. E. & Hong, C. O. (2019). Nitrous oxide emission from upland soil
amended with different animal manures. Applied Biological Chemistry, 62, 8.

Martín-Olmedo, P., & Rees, R. M. (1999). Short-term N availability in response to dissolved-organic-carbon from poultry manure, alone or in
combination with cellulose. Biology and Fertility of Soils, 29, 386–393.

Masaka, J., Nyamangara, J. & Wuta, M. (2014). Nitrous oxide emissions from wetland soil amended with inorganic and organic fertilizers.
Archives of Agronomy and Soil Scienc, 60, 1363–1387.

Mahmud, K., Panday, D., Mergoum, A. & Missaoui, A. Nitrogen Losses and Potential Mitigation Strategies for a Sustainable Agroecosystem.
(2021). Sustainability, 13 (4), 2400.

Paustian, K., Lehmann, J., Ogle, S., Reay, D., Robertson, G. P., Smith, P. & Kellogg, W. K. (2016). Climate-smart soils. Nature, 532, 49–57.

Perez, M. G., Romaniuk, R. I., Cosentino, V. R. N., Busto, M., González, F. A., Taboada, M. A., Alves, B. J. R. & Costantini, A. O. (2021). Winter
soil N2O emissions from a meat production system under direct grazing of Argentine Pampa. Animal Production Science, 61, 156–162.

Popp, J., Lakner, Z., Harangi-Rákos, M. & Fári, M. (2014). The effect of bioenergy expansion: Food, energy, and environment. Renewable and
Sustainable Energy Reviews, 32, 559–578.

Quiroga, G., Castrillón, L., Fernández-Nava, Y. & Marañón, E. (2010). Physico-chemical analysis and calorific values of poultry manure.
Waste Management, 30, 880–884.

Rapson, T. D. & Dacres, H. (2014). Analytical techniques for measuring nitrous oxide. Trends in Analytical Chemistry, 54, 65–74.

Rizzo, P. F., Bres, P. A., Young, B. J., Zubillaga, M. S., Riera, N. I., Beily, M. E., Argüello, A., Crespo, D. C., Sánchez, A., & Komilis, D. (2020).
Temporal variation of physico-chemical, microbiological, and parasitological properties of poultry manure from two egg production
systems. Journal of Material Cycles and Waste Management, 22, 1140–1151.

Rizzo, P. F.,Della Torre, V., Riera, N. I., Crespo, D., Barrena, R. & Sánchez, A. (2015). Co-composting of poultry manure with other agricultural
wastes: process performance and compost horticultural use. Journal of Material Cycles and Waste Management, 17, 42–50.

Rochette, P. & Eriksen-Hamel, N. S. (2008). Chamber Measurements of Soil Nitrous Oxide Flux: Are Absolute Values Reliable?. Soil Science
Society of America Journal, 72, 331–342.

Roig, N., Sierra, J., Martí, E., Nadal, M., Schuhmacher, M. & Domingo, J. L. (2012). Long-term amendment of Spanish soils with sewage
sludge: Effects on soil functioning. Agriculture, Ecosystems & Environment, 158, 41–48.

Schindlbacher, A., Zechmeister-Boltenstern, S. & Butterbach-Bahl, K. (2004). Effects of soil moisture and temperature on NO, NO2, and N2O
emissions from European forest soils. Journal of Geophysical Research, 109, 1–12.

SCyMA & SENASA. (2019). Resolución Conjunta 1/19 - Marco Normativo para la Producción, Registro y Aplicación de Compost. Ciudad
Autónoma de Buenos Aires.

Shelton, D. R., Sadeghi, A. M. & McCarty, G. W. (2000). Effect of soil water content on denitrification during cover crop decomposition. Soil
Science, 165, 365-371.

Snyder, C. S., Bruulsema, T. W. , Jensen, T. L. & Fixen, P. E. (2009). Review of greenhouse gas emissions from crop production systems and
fertilizer management effects. Agriculture, Ecosystems & Environment, 133, 247–266.

Steenwerth, K. & Belina, K. M. (2008). Cover crops and cultivation: Impacts on soil N dynamics and microbiological function in a Mediterra-
nean vineyard agroecosystem. Applied Soil Ecology, 40, 370-380.

Sterner, R. W. & Elser, J. J. (2002). Stoichiometry and homeostasis. In: R.W. Sterner & J. Elser (Eds), Ecological Stoichiometry: The Biology
of Elements from Molecules to the Biosphere (pp. 1–42). Princeton University,

Thornton, F. C., Shurpali, N. J., Bock, B. R. & Reddy, K. C. (1998). N2O and NO emissions from poultry litter and urea applications to Bermuda
grass. Atmospheric Environment, 32, 1623–1630.

Tian, H., Lu, c., Ciais, P., Michalak, A., M., Canadell, J. G., Saikawa, E., Huntzinger, D. N., Gurney, K. R., Sitch, S., Zhang, B., Yang, J., Bousquet,
P., Bruhwiler, L., Chen, G., Dlugokencky, E., Friedlingstein, P., Melillo, J., Pan, S., Poulter, B., Prinn, R., Saunois, M., Schwalm, C. R. & Wofsy,
S. C. (2016). The terrestrial biosphere as a net source of greenhouse gases to the atmosphere. Nature, 531, 225–228.

Tyson, S. C. & Cabrera, M. L. (1993). Nitrogen Mineralization in Soils Amended with Composted and Uncomposted Poultry Litter. Commu-
nications in Soil Science and Plant Analysis, 24, 2361–2374.

Zechmeister-Boltenstern, S., Schaufler, G. & Kitzler, B. (2007). NO, NO2, N2O, CO2 and CH4 fluxes from soils under different land use: tem-
perature sensitivity and effects of soil moisture. 2007. Geophysical Research Abstracts, 9, 7968.

111 Cienc. Suelo 40 (1): 102-111, 2022 ISSN 1850-2067 Versión electrónica