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Soil & Tillage Research
journal homepage: www.elsevier.com/locate/still
Seasonal effects on ammonia, nitrous oxide, and methane emissions for beef
cattle excreta and urea fertilizer applied to a tropical pasture
Abmael da Silva Cardosoa,⁎, Serena Capriogli Oliveiraa, Estella Rosseto Janusckiewiczb,
Liziane Figueiredo Britoa, Eliane da Silva Morgadoc, Ricardo Andrade Reisa,
Ana Cláudia Ruggieria
a Departamento de Zootecnia, Faculdade de Ciências Agrárias e Veterinárias, UNESP – Univ Estadual Paulista, Via de Acesso Prof. Paulo Donato Castellane s/n, 14884-
900, Jaboticabal, SP, Brazil
bUniversidade Estadual do Mato Grosso do Sul, Rodovia Aquidauana/UEMS - Km 12, 79200-970, Aquidauana, MS, Brazil
cUberlandia Federal University, Rua João Naves de Ávila 2121, Santa Mônica, 38408-100, Uberlândia, MG, Brazil
A R T I C L E I N F O
Keywords:
CH4 emission factor
Environmental impact of livestock
Greenhouse gases
Nitrogen cycle
N2O emission factor
A B S T R A C T
In this study we conducted four field trials (two wet- and two dry-season) to quantify N2O and CH4 emissions,
NH3 volatilization, and N2O emission factors (EF3PRP) following the application of cattle dung, urine, dung plus
urine, and urea fertilizer on a palisade-grass pastureland in Brazil. The EF3PRP differed with treatment and
season. Wet season EF3PRP were 0.36%, 1.02%, and 0.84% and dry season EF3PRP were 0.32%, 0.47%, and 0.34%
for dung, urine, and dung plus urine, respectively. These emission factors are maybe lower than the default
proposed by the Intergovernmental Panel on Climate Change (IPCC; 2%). Methane emissions also differed ac-
cording to the treatment and season, and annualized dung emissions were 0.54 kg CH4 head−1 year−1. The
fraction of total-N from animal manure and urine emitted as NH3 (FracGASM) in the wet season for dung, urine
and dung plus urine was 7.2%, 6.3%, and 6.4%, respectively; lower than the rate of dry season volatilization
from urine (14.2%) and dung plus urine (11.5%). Observed FracGASM is probably lower than the IPCC guideline
(20%). Emissions of N2O, CH4, and the volatilization of NH3 after urea treatment were not influenced by season;
N2O emissions from urea were 0.85%, CH4 emissions were 112 g CH4-C ha−1, and N-fertilizer lost as NH3 was
16.9%. The emission factors observed in this experiment differed from the IPCC Guidelines; observed N2O
emissions were lower than the guideline (1%), and FracGASF was higher than the 10% guideline.
1. Introduction
Livestock is responsible for 14.5% of global greenhouse gas (GHG)
emissions. Methane (CH4) is responsible for 44% of these emissions and
is primarily caused by enteric fermentation by ruminants; while nitrous
oxide (N2O) accounts for 29%, primarily associated with animal ex-
cretions (Gerber et al., 2013). In Brazil, 82% and 61% of the total CH4
and N2O emissions, respectively, during 2015 were attributed to live-
stock activity (Ministério de Ciência, Tecnologia e Inovação (MCTI,
2018). Most of these emissions were attributed to the more than
225million head of cattle in the country (IBGE, 2018)
Animal excretions contribute to environmental pollution (Gerber
et al., 2013). For example, N2O and CH4 are important GHGs and
ammonia (NH3) is an indirect emitter of N2O. Nitrate (NO3−-N) can be
leached into the groundwater, and ammonium (NH4+-N) can increase
the acidification of soil and watercourses (Chadwick, 2005). The main
reactions involved in N2O production from soil are nitrification of NH4-
N, and denitrification of NO3-N. Nitrous oxide is one product of these
reactions (Hüther et al., 1997; Luo et al., 2019). The key driving vari-
ables that regulate these processes are available N, soil moisture, and
soil temperature (Firestone and Davidson, 1989). In the guidelines for
GHG national inventories, the Intergovernmental Panel on Climate
Change (IPCC) prescribes that 2% of all N returned to the soil via bo-
vine urine or feces is emitted as N2O (EF3PRP). Recently, studies have
advocated for the disaggregation of this emission factor according to
the type of excreta (van der Weerden et al., 2011; Sordi et al., 2013) or
season (Lessa et al., 2014). However, N2O emission data from dung and
urine excreted in the same area are lacking. For nitrogen fertilizer
https://doi.org/10.1016/j.still.2019.104341
Received 6 December 2016; Received in revised form 26 June 2019; Accepted 15 July 2019
Abbreviations: CH4, methane; EF1, nitrous oxide emissions factor for fertilizer; EF3PRP, N2O emissions factor for animal excreta; FracGASF, fraction of total-N from
fertilizer emitted as NH3; FracGASM, fraction of total-N from animal manure and urine emitted as NH3; NH3, ammonia; N2O, nitrous oxide
⁎ Corresponding author.
E-mail address: abmael2@gmail.com (A.d.S. Cardoso).
Soil & Tillage Research 194 (2019) 104341
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applied to the soil, the emission factor (EF1) prescribes that 1% of total
N is lost as N2O (Intergovernmental Panel on Climate Change (IPCC,
2006). Notwithstanding the huge Brazilian territory occupied by
grasslands, N2O emissions from N fertilization remain unreported.
Hence, it is desirable to develop specific N2O emission factors according
to climatic conditions and characteristics of the beef cattle production
systems, and to identify the key driving variables involved in N2O
production. We hypothesize that: (i) N2O emissions vary according to
the type of cattle excreta; (ii) CH4 emissions are affected by excreta
types; (iii) ammonia volatilization differs according to cattle excreta,
and (iv) N2O EF1, EF3PRP, fraction of total N from animal manure and
urine emitted as NH3 (FracGASM), and fraction of total N fertilizer
emitted as NH3 (FracGASF) differ from the default emission factor
prescribed by the IPCC guidelines.
The production of CH4 occurs via the microbial degradation of the
proteins, organic acids, carbohydrates, and soluble lipids present in
excreta (Khan et al., 1997). According to the IPCC (2006), 1 kg of CH4 is
emitted from dung annually per adult head of beef cattle in Latin
America. Ammonia volatilization mainly results from hydrolysis of the
urea component of excreta. In soils, microorganisms produce the urease
enzyme that hydrolyzes urea to ammonium bicarbonate, and under
most field conditions, the hydrolysis of the urea in urine voided on grass
swards by grazing animals is complete within a few hours (Thomas
et al., 1988). However, large variations in the rate of NH3 volatilization
among excreta types have been reported; the highest overall rates were
measured for urine (Petersen et al., 1998), and the highest seasonal
losses were during the dry season for dung and the wet season for urine
(Lessa et al., 2014). According to the IPCC (2006), 10% of nitrogen
fertilizer (FracGASF) and 20% of nitrogen from FracGASM are volati-
lized as NH3, of which 1% of this amount is indirectly emitted as N2O.
In the grassland region northwest of São Paulo, rainfall varies be-
tween 1200–1600mm annually, with approximately 90% of the pre-
cipitation occurring during the warm summer season from October to
April. Vegetation in this region is Brazilian Savanna (Cerrado biome);
however, the region contrasts with temperate and sub-tropical regions
(Lopes, 1996). During the summer season, temperatures range from 22
to 32 °C. Anoxic microsites in the soil can form as a result of high
temperatures combined with high precipitation, which favor N2O
emissions (Smith et al., 2003). However, when water infiltrates rapidly
into the soil and evapotranspiration rates are high, these anoxic con-
ditions are temporary (Skiba and Ball, 2002; Lessa
et al., 2014).
Therefore, the high seasonality may result in different magnitudes of
GHG emissions and NH3 volatilization. Hence, we hypothesize that
N2O, CH4, and NH3 production will be affected by seasonality. EF3PRP
Recent studies examining NH3 volatilization, and CH4 and N2O
emissions from cattle dung, urine, and N fertilization have been con-
ducted in temperate areas, with little focus on tropical conditions.
Interactions between the key driving variables and CH4 and N2O
emissions are expected in tropical pastureland soils, varying with
season and excreta type. To develop the specific emission factors (EF)
needed to improve CH4 and N2O emission inventories and N2O miti-
gation strategies, it is vital to understand these variables and their
impacts on of CH4 and N2O emissions from livestock in tropical regions.
In this study we assessed CH4 and N2O emissions and NH3 volati-
lization from patches of cattle urine, dung, dung plus urine, and urea in
a tropical pastureland of Brazil to evaluate (i) the applicability of the
guideline EF for each gas in the region; (ii) how excreta type affects
emissions and whether the EF differs between excreta type; and (iii)
how the season affects excreta emission patterns, volatilization, and
emissions associated with fertilizers.
2. Materials and methods
2.1. Site description and soil characteristics
The two years field study was conducted on a palisade-grass
pastureland, Brachiaria brizantha (Hochst.) Stapf., established in 2001
and located in the Forragicultura Sector of the São Paulo State
University Júlio de Mesquita Filho campus of Jaboticabal in São Paulo
State (21°15′22″S and 48°18′08″W; elevation 595m). The region has a
tropical climate, with a dry season (April to September), and a wet
season (October to March) during which more than 80% of annual
precipitation occurs. Average annual rainfall is 1424mm and the
average air temperature is 22.3 °C. The soil is a rhodic Ferralsol (IUSS,
2006) derived from basalt. The soil, at 0–20 cm depth, has a bulk
density of 1.10 g cm−3, contains 420 g kg-1 of clay (sandy clay soil), has
a pH of 5.32 in water, and contains 20 g kg-1 of total carbon, 1.6 g kg-1
of total N, 4.7mg kg-1 of NO3-N, and 15.9 mg kg-1 NH4-N.
2.2. Experimental design and excreta characteristics
Ammonia volatilization, and N2O and CH4 fluxes were measured
during four separate 106-day trials; the 2012 dry season (July
8–October 16), the 2013 wet season (January 9–April 17), the 2013 dry
season (July 3–October 17) and the 2013–2014 wet season (December
17–March 31). Experiments were carried out in an area that had not
been treated with any N (fertilizer) during the previous three years. A
volume of 1.5 l of artificial urine, 1.5 kg of fresh dung, a mixture of
0.75 l of urine plus 0.75 kg of fresh dung, and the equivalent of 80 kg N
ha−1 of urea fertilizer were applied to soil microplots delimited by
rectangular metal chamber bases 0.6× 0.4 m (0.24m2) inserted 5.0 cm
deep into the soil. The chamber bases were inserted three days prior to
treatment application to prevent soil disturbance from influencing gas
emissions. For each trial, the chamber was moved to a new area. The
urine solution was poured onto the soil surface delimited by the walls of
the static chamber base taking care to wet the entire area inside the
chamber. Dung patches were artificially prepared by pouring the dung
into a 24 cm diameter and 3 cm high plastic ring in the center of the
static chamber base. The control was a soil plot that received no excreta
or fertilizer. During trials, when herbage reached a height of 25 cm, it
was cut to 10 cm and removed from the area, simulating grazing.
Artificial urine was created according Doak (1952) by mixing urea
(88.6% of total N), hyppuric acid (6.2% of total N), creatine (0.8% of
total N), allantoin (1.5% of total N), ureic acid (0.4% of total N), and
NH4Cl (2.5% of total N). The treatment volume of 1.5 l was chosen
based on the average range of 1.6–2.2 l per urination event as reported
by Haynes and Williams (1993). Haynes and Williams (1993) also de-
termined a fresh dung weight of 1.5–2.7 kg per excretion event. In
addition to the urine and dung, a mixture of these two excreta was used
as a treatment to simulate conditions in the field. Fresh dung was col-
lected from Nellore beef cattle and analyzed for dry matter according to
AOAC (1995; DM, method Nº 934.01), and total C and N content by dry
combustion (Leco model FP-528; LECO Corporation, St. Joseph, MI).
The total N content of the dung samples varied from 17.0–29.1 g kg−1,
comparable to the previously reported range of 18.0–26.2 g kg−1 (Sordi
et al., 2013). The N application rates for dung varied from 3.93 to
6.73 g N chamber−1, and for dung plus urine from 7.25 to 8.65 g N
chamber−1 (Table 1). The total C in the dung was quantified by dry
combustion and ranged from 385–491 g kg−1, while the C:N ratio
varied from 14.5–28.5. Dung characteristics are shown in Table 2. Urea
fertilizer was spread manually into the chambers to simulate a fertili-
zation.
The experimental design employed a randomized complete block
with 5 replicates. Each of the five treatments was evaluated in three
different contiguous areas. The first area was placed within a static
chamber to evaluate N2O and CH4 emissions, the second area was used
for the evaluation of soil NH4-N and NO3-N, and the third area was used
for the quantification of NH3 volatilization (Fig. 1). The distance be-
tween plots was approximately 1.5m and distance between batches was
approximately 5.0m. After the completion of each trial period, micro-
plots were relocated to an area isolated from the influence of previous
excreta or fertilizer. During the experimental period, the pasture was
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
2
not grazed to avoid any disturbance or influence from animals. Periodic
gas sampling began one day after application (DAA) and ran until 106
DAA, at which time the gas peaks of the treatments equaled those of the
control, with a total of 23 measurements per experiment. The sampling
interval varied over the course of the experiment, occurring daily in the
first week, every 2–3 days from the second to fourth week, once per
week in the second month of the experiment, and finally, every two
weeks until the end of the experiment.
2.3. NH3 volatilization evaluations
The measurement of NH3 volatilization was carried out according to
the methodology of Araujo et al. (2009) as described by Jantalia et al.
(2012). Using this technique, the NH3 was captured in a semi-open
chamber made of 2 l plastic bottles (PET bottles; 10 cm diameter), lined
with acid-embedded foam strips. The chamber was placed on the area
affected by the excreta or fertilizer immediately after deposition. Foam
strips were collected and replaced with fresh strips after 1, 3, 5, 9, 14,
and 21 DAA. Quantification of the ammonium captured in the foam
strips was performed by steam distillation (Kjeldahl method) following
the method of De Morais et al. (2013). The minimum detection limit
was 0.1mg N chamber−1.
Total volatilized NH3 was calculated for the experimental period
(three weeks) by summing the amounts measured in each sampling
interval. Volatilized NH3 was expressed as a fraction of N added, and it
was calculated by dividing the N volatilized from the excreta or ferti-
lizer treatment plots, corrected for NH3 lost from the control treatment,
by the applied N. The total amount of volatilized NH3 was corrected for
the affected area by each excreta type, and the calibration factor (1.74)
as determined by Araujo et al. (2009).
2.4. N2O and CH4 flux measurements and emission factors
The static closed chamber technique (Mosier, 1989) was used to
collect air samples. The headspace of the chamber was 15 cm high
rectangular polyurethane (0.4× 0.6m) covered with a thermal in-
sulation mantle. The headspace was deployed on rectangular metal
bases at the beginning of each sampling event, between 9:00–10:00 am,
which represented the daily mean flux as found by Alves et al. (2012).
The volume of each chamber was 0.036m3. Chambers were equipped
with a rubber belt to seal the chamber base, and an output valve for
sample removal. The linearity of gas accumulation in the chamber was
successfully tested in a preliminary experiment with an intensive
sampling routine (every 10min for one hour), and the deployment
period was determined to be 30min. Two samples were taken; T0,
immediately after the chamber was closed, and T30 at the end of the
incubation period. We analyzed 2300 samples from T0; both N2O and
CH4 concentrations were found to be the same as the background air
during the entire experimental period for all treatments. This suggests
that collecting ambient air samples is adequate for determining T0
concentration, as practiced, for example, by Dobbie and Smith (2003).
Air samples were taken with 50ml polypropylene syringes. Air
temperatures outside and inside the chambers were recorded using a
digital thermometer. Each air sample was transferred to 20ml pre-
evacuated vials (Shimadzu flasks). Samples were analyzed by gas
chromatography (GC-2014, Shimadzu, Kyoto, Japan), which analyzed
the gases simultaneously. Samples were analyzed under the following
conditions: to measure N2O, the injector was 250 °C, the column was
80 °C, the carrier gas was N2 (30ml min−1), and electron capture de-
tector was set at 325 °C; to measure CH4 the flame gas was H2 (30ml
min−1), and the flame ionization detector was set at 280 °C. The
minimum detection limit was 0.004 and 0.01 ppb for N2O and CH4,
respectively.
The N2O fluxes (μg m−2 h-1) or CH4 fluxes (μg m−2 h-1) were cal-
culated assuming a linear increase of gas concentration during the de-
ployment period, the air temperature and pressures, the chamber
Table 1
Amount of N in cattle urine, dung, dung+ urine, and urea used as soil treat-
ment for the two rainy season and two dry season experimental periods.
Amount of N in applied excreta and fertilizer (g N chamber−1)
Rainy season Dry season
Treatment 2013 2014 2012 2013
Excreta type
Urine 10.56 (0.12) 10.56 (0.12) 10.56 (0.12) 10.56 (0.12)
Dung 6.73 (0.23) 6.24 (0.25) 3.97 (0.18) 3.93 (0.29)
Dung+urine 8.65 (0.73) 8.40 (0.47) 7.26 (0.58) 7.25 (0.54)
Fertilizer
Urea 1.92 (0.02) 1.92 (0.02) 1.92 (0.02) 1.92 (0.02)
Within parentheses the standard error of the means (SEM;± ). Dry season 2012
(July 8-October 16) and 2013 (July 3 -October 17). Wet season 2013 (January
9- April 17) and 2014 (December 17 – March 31).
Table 2
Dung characteristics. Amount of dry matter (%), carbon (% of DM), nitrogen (%
of DM), and C/N ratio. (n= 5).
DM carbon nitrogen C/N
Trial (%)
Dry season 2012 15.4 (1.2) a 42.3 (2.1) b 2.91 (0.4) a 14.5 b
Rainy season 2013 14.1 (0.9) a 44.9 (1.9) ab 2.70 (0.4) a 16.6 b
Dry season 2013 16.8 (1.3) a 49.1 (2.3) a 1.72 (0.4) b 28.5 a
Rainy season 2014 15.5 (1.1) a 38.6 (2.7) b 1.70 (0.5) b 22.7 a
Within parentheses is presented standard error of the means (SEM;± ). In the
column means followed by the same letter did not differ (Tukey test; α=5%).
Fig. 1. Experimental schema of 3 batch to evaluate greenhouse gases, NH3 volatilization and soil mineral N content. The distance between batches was 5m and
between plot 1.5 m.
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
3
volume, and area of the metal bases (Cardoso et al., 2018). The cu-
mulative emissions (g m2) for each 106-day experiment was calculated
by integrating the hourly fluxes over time using linear interpolation.
For each experiment, the N2O-N EF was calculated according to Eq.
(1);
EF3PRP or EF1 (%) = [N2O-N treatment - (N2O-N control)] / applied-N
× 100) ((1)
where EF3PRP is the emission factor (percentage of the urine, dung,
dung plus urine), and EF1 is the percentage of fertilizer applied-N
emitted as N2O. N2O-N treatment is the cumulative N2O-N emissions
from urine, dung, dung plus urine, or urea treated plots during the
study period (g m−2). N2O-N control is the cumulative N2O-N emissions
from the control plot (g m−2), and applied-N is the N application rate (g
m−2) from the treatments.
The CH4 emission factor was calculated for the dung treatment (kg
CH4 head−1). We estimated the annual production of feces based on the
assumption that one animal defecates 10 kg (wet weight) of feces per
day (on average 1 kg, ten times), which was based on values observed
in previous research carried out in tropical pasturelands (Gonzalez-
Avalos and Ruiz-Suarez, 2001; Orr et al., 2012; Mazzetto et al., 2014).
During the dry season, we multiplied the fecal production over five
months by the average CH4 cumulative emissions from dung treatment
measured in the dry season, which were from 1.5 kg of wet dung. Thus,
we corrected for the size of the treatment divided by 1.5. During the
wet season, the CH4 EF was obtained for seven months. Annual CH4 EF
for cattle dung was obtained by summing the emissions from the dry
and wet seasons (kg CH4 head−1 year−1).
2.5. Soil and meteorological parameters
At each air sampling event, soil samples from the 0–10 cm layer
were collected from each treatment to measure gravimetric water
content (soil samples were oven-dried at 105 °C), and determine the
water filled pore space (WFPS), NH4+-N, and NO3−-N contents. Soil
bulk density in the 0–5 cm layer was also measured, using a 50mm
diameter, 50mm height cylinder. WFPS was calculated using the
gravimetric water content, bulk density, and a particle density of 2.65 g
cm-3.
For mineral N analysis, extraction with 2M L−1 KCl was performed
on moist field samples. The correction of water content was done after
105 °C drying. Ammonium-N was determined using a Berthelot
reaction, measured with spectrometry at 647 nm (Kempers and Zweers,
1986). Nitrate-N quantification was carried out using ultraviolet ab-
sorption spectrometry at 220 nm (Miyazawa et al., 1985;Olsen, 2008).
The minimal detection limit for NH4+ and NO3- was 0.1mg N kg−1 in
dry soil. Data describing daily maximum, average, and minimum
temperature, and daily rainfall were obtained from a meteorological
station located 1.5 km away.
2.6. Statistical analysis
The patterns of volatilized NH3, and N2O and CH4 fluxes during the
experimental period were displayed using means and standard error of
means. Integrated data for each experimental period were subjected to
ANOVA after testing for normality, and equal variance tests using R
version 3.1.2 (2014) following the randomized blocks design. The sta-
tistical model included the effects of treatments, season of year and
treatments as follow:
Statistical model: μ + ßi+Yj+Sl Tj + (AB)kl + εijkl
Where μ is the overall means, the parameters ßj are the block effects,
the parameters Yk+ Sl+ Tj are the years, seasons and treatments ef-
fects and εklj are random errors, Means were separated using a Tukey-
HSD test at 5% probability.
The Pearson correlation analysis was run to test for relationships
between transformed N2O or CH4 fluxes and temperature, rainfall,
WFPS, NO3-N, and NH4-N using data from each sampling event (n=46
for each treatment). Single and multiple linear regression (backward)
analyses were used to create explanatory models using the variable to
account for variation in seasonal N2O emissions.
3. Results
3.1. Temperature and precipitation
Temperature and precipitation were relatively consistent during
first and second years of the experiment. However, during the wet
season of 2014 the region was under a severe drought. During the dry
season, the maximum, average, and minimum air temperatures were
38.3, 20.9, and 5.9 °C in 2012 and 35.9, 20.5, and 4.6 °C in 2013
(Fig. 2). In the wet season, the maximum, average and minimum
temperatures were 34.4, 23.1, and 12.7 °C in 2013 and 35.9, 25.0 and
15.8 °C in 2014 (Fig. 2). There was no rain between 10–73 DAA in the
Fig. 2. Daily air temperature (minimum, mean, and maximum; T; ºC) and daily rainfall (P; mm). Data from Agrometeorological Station, Department of Exact Science,
FCAV/UNESP,
located 1.5 km away from the experiment site. (a) dry season 2012, (b) wet season 2013, (c) dry season 2013, and (d) wet season 2014.
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
4
2012 dry season and in 2013, there was no rain between 20–70 DAA. In
both years, rain was observed at the end of the dry season experiments.
The accumulated rainfall during the dry season study periods was
146.6 mm and 149.2 mm in 2012 and 2013, respectively, representing
11% and 16% of the annual precipitation. The total rainfall during the
wet season experiments was 537mm and 516.6mm in 2013 and 2014,
respectively, representing 39% and 54% of annual precipitation.
3.2. Ammonia volatilization
Volatilized N-NH3 varied according to the type of excreta
(p < 0.001) and season (p < 0.001; Table 3). The volatilized urine-N
was higher as compared to dung-N in the 2012 dry season (20.9% and
4.7%, respectively); however, they were similar in 2013 (approximately
7.5%). During the wet season, volatilized-N did not differ according the
type of excreta (7.2%, 6.4%, and 6.3% for dung, urine, and dung plus
urine, respectively); however, it did differ between years, being lower
in 2014 when a strong drop in NH3 from dung was observed. For urea
fertilizer, 17.0% and 16.9% of N applied in the dry and wet seasons,
respectively, were volatilized, with no significant difference according
to the season (Table 3). While we did not find differences in urea fer-
tilizer volatilization based on the season, annual differences were ap-
parent, especially during the wet season, when volatilized NH3 de-
creased by 50%.
3.2.1. Ammonia volatilization during the dry season
During the dry season, FracGASM differed according to the excreta
type. Urine treatment presented the highest NH3 volatilization in 2012
(a loss of 20.9% added-N), followed by dung plus urine (a loss of 12.6%
added-N), and dung (a loss of 4.7% added-N). Marked interannual
variations were observed in NH3 volatilization from urine-N; however,
dung and dung plus urine remained similar over time (Table 3).
For urine, 20.9% (± 4.0) and 7.6% (±1.9) of urine-N were vola-
tilized during 2012 and 2013, respectively (Table 3). In 2012, 87.6%,
and in 2013, 76.4% of the N-volatilization occurred within the first 5
DAA (Fig. 2). For dung, 4.7% (±1.7) and 7.4% (± 3.3) of dung-N
were lost as NH3 during 2012 and 2013, respectively (Table 3). In 2012,
the N volatilization occurred mainly during the first 5 DAA, and in 2013
it persisted until 15 DAA (Fig. 3). For dung plus urine, the amount of
applied-N volatilized in 2012 was 12.6% (±1.8), and in 2013, 10.55%
(±2.6; Table 3). In 2012, more than 50% of N-NH3 volatilization oc-
curred in the first 3 DAA. This differs from 2013, when N volatilization
was minimal during the first 3 DAA. However, for both years more than
80% of N volatilization had occurred by 9 DAA, with the process
ceasing by 11 DAA (Fig. 3).
The average FracGASF was 17.0% during the dry season for urea
fertilizer. During 2012, 19.1% (±6.4) and during 2013, 14.9%
(±5.1) of urea-N was volatilized. The timing of N volatilization dif-
fered annually; in 2012 more than 80% of volatilization had occurred
by 5 DAA and in 2013 the 80% volatilization was achieved by 14 DAA
(Fig. 3).
3.2.2. Ammonia volatilization during the wet season
The FracGASM did not vary according to the excreta type during the
wet season. On average, 6.3, 7.2, and 6.4% of applied-N was lost as NH3
for urine, dung and dung plus urine, respectively, which resulted in an
average added-N volatilization of 6.6% for excreta. However, annual
differences were apparent; FracGASM was lower in 2014, mainly for
dung, which decreased from 12.4% (±1.6) to 2.0% (± 0.7).
In 2013, 7.6% (±1.3), 12.4% (±1.6), and 8.9% (± 1.9) of ex-
creta-N was volatilized for urine, dung, and dung plus urine, respec-
tively, and in 2012, 5.0% (± 0.7), 2.0% (±0.7), and 3.8% (±0.9) of
excreta-N was volatilized, for urine, dung, and dung plus urine, re-
spectively. During the wet season, volatilization mainly occurred at 5
DAA and ceased by approximately 9 DAA.
FracGASF averaged 16.9% for urea fertilizer and differed annually.
In 2013, 22.9% (± 6.4) and in 2014, 10.8% (± 3.1) of applied-N was
volatilized. For urea, 87% and 85% of total N loss (NH3 from applied-N)
was volatilized by 5 DAA, during 2013 and 2014, respectively.
3.3. Temporal trends in N2O fluxes
3.3.1. Temporal trends during the dry season
The N2O fluxes from control plots were approximately zero during
the evaluation period. The N2O emission peak for dung averaged 696
(± 91) μg N2O-N m−2 h-1 at 20 DAA during 2012 and dropped to
background levels by approximately 64 DAA (Fig. 4 a). During 2013,
the peak flux was 128 (± 12) μg N2O-N m−2 h-1 observed at 2 DAA
with secondary peaks at 6, 29, and 64 DAA. For urine, the peak N2O
flux during 2012 was measured at 20 DAA (526 ± 91 μg N2O-N m−2 h-
1), and at 78 DAA (98 ± 35 μg N2O-N m−2 h-1) during 2013. For dung
plus urine, N2O emissions peaked in 2012 at 680 ± 61 μg N2O-N
m−2 h-1 at 20 DAA, and fell to background levels after 31 DAA, while in
2013, emissions peaked at 2 DAA (79 ± 7 μg N2O-N m−2 h-1), and
dropped to background levels after 35 DAA (Fig. 4 c). Negatives N2O
fluxes were found frequently; in 2012, negative fluxes for most treat-
ments were measured in 12 sampling events, and by 6 sampling events
in 2013.
With respect to urea fertilizer, peak N2O production was observed at
20 DAA (454 ± 160 μg N2O-N m−2 h-1) and declined to background
levels at 64 DAA in 2012. In 2013, urea fertilizer emissions peaked at 2
DAA (88 ± 9 μg N2O-N m−2 h-1) and rapidly fell to background levels
after 7 DAA (Fig. 4 c).
3.3.2. Temporal trends during the wet season
During the wet season, N2O emissions were higher as compared to
the dry season. For dung, the highest N2O fluxes (approximately 340 μg
N2O-N m−2 h-1) were recorded at 7 and 31 DAA in 2013 and they
peaked at 64 DAA (98 ± 29 μg N2O-N m−2 h-1) in 2014. During 2014,
N2O emissions were like the control treatment for most sampling
events. For urine, N2O emissions peaked at 31 DAA (772 ± 163 μg
N2O-N m−2 h-1) in 2013, which was the highest average flux observed
in this study. In 2014, the topmost urine N2O flux was recorded at 27
DAA (587 ± 59 μg N2O-N m−2 h-1); N2O emissions remained high
until 64 DAA and then dropped to background levels. For dung plus
urine, N2O emissions peaked in 2013 at 38 DAA (471 ± 87 μg N2O-N
m−2 h-1) while the lowest N2O flux was observed at 91 DAA (9 ± 3 μg
N2O-N m−2 h-1). In 2014 the highest N2O flux was observed at 27 DAA
(489 ± 75 μg N2O-N m−2 h-1) with a secondary peak at 45 DAA
(Fig. 4).
Table 3
Percentages of added N lost as volatilized NH3 from cattle urine, dung,
dung+urine, and urea used as soil treatment for the two rainy season and two
dry season experimental periods.
Volatilized N-NH3
(% of total N-applied)
Rainy season Dry season
Treatment 2013 2014 Mean 2012 2013 Mean
Excreta type
Urine 7.6 (1.3) b 5.0 (0.7)
a
6.3 b 20.9 (4.0)
a
7.6 (1.9) b 14.2 a
Dung 12.4 (1.6)
a
2.0 (0.7)
b
7.2 ab 4.7 (1.7) c 7.4 (3.3) b 6.0 b
Dung+urine 8.9 (1.9) b 3.8 (0.9)
a
6.4 b 12.6 (1.8)
b
10.5 (2.6)
a
11.5 a
Fertilizer
Urea 22.9 (6.4) 10.8
(3.1)
16.8 19.1 (6.4) 14.9 (5.1) 17.0
Mean N data followed by a same letter did not differ in the column according to
the Tukey-HSD test at 5% probability. Within parentheses is the standard error
of the means (SEM;± ).
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
5
One week after urea fertilizer application, the highest average N2O
emissions were 315 ± 97 μg N2O-N m−2 h-1 that occurred 7 DAA in
2013, and in 2014 N2O production peaked on 64 DAA (171 ± 75 μg
N2O-N m−2 h-1). During 2014, the N2O flux from urea fertilizer was like
the control treatment for most observations (Fig. 4 d).
3.4. Nitrous oxide emission factors
Nitrous oxide EF3PRP differed between excreta type and season;
however, N2O EF1 did not vary between seasons for urea fertilizer
(Table 4).
3.4.1. Effect of
excreta type and fertilizer during the dry season
The observed background emissions the control experiment were
1.2 and 1.7 mg N2O-N m−2 during 2012 and 2013, respectively. Mean
N2O EF did not differ between excreta type and year of measurement
during the dry season. The mean N2O EF during the dry season was
0.47% (±0.1) for dung, 0.32% (±0.1) for urine, and 0.34% for dung
plus urine (Table 4).
The observed mean N2O EF1 for urea fertilizer was 0.71 (± 0.2).
There was a large annual difference between EF1; the second year was
seven times lower as compared to the first year (Table 4).
3.4.2. Effect of excreta type and fertilizer during the wet season
During the wet season, N2O emissions from the control were 1.6 and
-2.6 mg N2O-N m−2 for 2013 and 2014, respectively (Table 4). For
dung, N2O EF averaged 0.36% (± 0.1); however, N2O EF was much
higher in 2013 (0.58%±0.0) as compared to 2014 (0.15%±0.1). The
mean N2O EF was 1.02% (±0.1) and 0.84% (±0.1) for urine and
dung plus urine, respectively, with no annual variation (Table 4). The
N2O EF1 estimated from urea fertilizer was 1.00% (±0.3); it was
1.20% (± 0.2) in 2013, and 0.80% (±0.1) in 2014 (Table 4).
3.4.3. Annual N2O emissions factors
The dry and wet seasons in the study region are five and seven
months long, respectively, allowing us to estimate the annual EF based
in the season length. For dung, urine, and dung plus urine, the esti-
mated EFs in the first year were 0.51, 0.83, and 0.63%, respectively,
and 0.30, 0.62, and 0.63% in the second year. For urea fertilizer, the
estimated annual EF1 was 1.22 and 0.53% for the first and second years
Fig. 3. As in Fig. 2 but for cumulative ammonia volatilization (% of N added).
Fig. 4. As in Fig. 2 but for nitrous oxide fluxes (μg N2O-N m−2 h-1).
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
6
of the study, respectively (Table 4).
3.5. Temporal trends in CH4 fluxes
3.5.1. Temporal trends in CH4 fluxes during the dry season
During the 2012 dry season, the highest CH4 fluxes were observed at
31 DAA and averaged 318 (± 143), 362 (± 153), and 394 (± 176) μg
CH4-C m−2 h-1 for dung, urine and dung plus urine, respectively (Fig. 5
a). During 2013, CH4 oxidation peaked at 45 DAA and the lowest ob-
served flux was -133(± 32) μg CH4-C m−2 h-1 in the control treatment
(Fig. 5 a). During the 2013 dry season, both CH4 fluxes and oxidation
were small; the highest CH4 emissions were observed at 27 DAA
(175 ± 75 μg CH4-C m−2 h-1) in the dung plus urine treatment. For
urea fertilizer, a peak of 75.7 μg CH4-C m−2 h-1 was observed at 2 DAA
(Fig. 5 c)
3.5.2. Temporal trends in CH4 fluxes during the wet season
During the 2013 wet season, CH4 peak emissions for dung were
1256 (± 550) μg CH4-C m−2 h-1 at 7 DAA which then declined rapidly
to background levels. For urine, the highest CH4 flux was recorded at 8
DAA (188 ± 108 μg CH4-C m−2 h-1), and for dung plus urine, peak CH4
emissions were 1004 (± 61) μg CH4-C m−2 h-1 at 3 DAA. The highest
CH4 oxidation mean was found at 7 DAA (231 ± 66 μg CH4-C m−2 h-1;
Fig. 5 b).
In 2014, the highest average CH4 flux for dung was 198 (± 78) μg
CH4-C m−2 h-1 measured at 24 DAA, which was the peak CH4 flux
observed in this study. Peak CH4 flux was observed at 27 DAA
(113 ± 42 μg CH4-C m−2 h-1) for urine and at 27 DAA (177 ± 83 μg
CH4-C m−2 h-1) for dung plus urine. The highest CH4 oxidation was
recorded in the control experiment (-60 ± 47 μg CH4-C m−2 h-1) at 27
DAA and for urea, the highest mean CH4 production was recorded at 20
DAA (154 ± 87 μg CH4-C m−2 h-1) (Fig. 5 d).
3.6. Cumulative CH4 emissions
Cumulative CH4 emissions differed seasonally (p=0.01), and with
the type of excreta (p < 0.05). Dung was shown to differ from urine,
urine plus dung, and urea fertilizer (p < 0.01; Table 5).
Dung was found to differ from other treatments during the 2013 wet
Table 4
Fraction of added N emitted as N-N2O in cattle urine, dung, dung+ urine, and
urea used as soil treatment for the two rainy season and two dry season ex-
perimental periods.
Fraction of added N emitted as N-N2O (% of N added)
Rainy season Dry season
Treatment 2013 2014 Mean 2012 2013 Mean
Excreta (EF3PRP)
Urine 1.20
(0.1) a
0.84
(0.0) a
1.02 (0.1) 0.32
(0.1) b
0.33
(0.1) b
0.32 (0.1)
Dung 0.58
(0.0) b
0.15
(0.1) b
0.36 (0.1) 0.42
(0.0) a
0.51
(0.2) a
0.47 (0.1)
Dung+urine 0.84
(0.2) a
0.84
(0.1) a
0.84 (0.1) 0.34
(0.0) b
0.34
(0.1) b
0.34 (0.1)
Fertilizer (EF1)
Urea 1.20
(0.2)A
0.80
(0.1)B
1.00 (0.3) 1.25
(0.3)A
0.16
(0.1)B
0.71 (0.2)
Mean data followed by a same letter did not differ in the column for excreta and
in the line for fertilizer according to the Tukey-HSD test at 5% probability.
Within parentheses are the standard errors of the means (± SEM).
*Fertilizer was not compared to the excreta. ANOVA significance for season
(p > 0.05) and year (p > 0.05).
Fig. 5. As in Fig. 2 but for methane fluxes (μg C−CH4m−2 h-1).
Table 5
Cumulative CH4 fluxes (mg CH4-C m−2) from treatment cattle urine, dung,
dung+urine, and urea applied to the soil for two rainy season and two dry
season experimental periods.
Rainy season Dry season
Treatment 2013 2014 2012 2013 Mean
mg CH4-C m−2
Control 56.3 (72) b 9.5 (33)
b
34.6 (28)
b
34.3 (25)
b
33.7
Excreta type
Urine 115.3 (87) b 15.2 (7)
b
48.5 (40)
b
70.3 (12)
b
15.2
Dung 331.0 (111) a 60.3 (22)
b
50.9 (26)
b
91.4 (22)
a
133.4
Dung+urine 70.3 (91) b 55.6 (26)
b
40.0 (42)
b
36.0 (26)
b
41.5
Fertilizer*
Urea 70.2 (63) 50.8 (15) −3.4
(45)
49.0 (12) 50.8
Data followed by a same letter did not differ according to the Tukey-HSD test at
5% probability.
* Fertilizer was not compared to the excreta. ANOVA significance for season
(p > 0.05) and year (p > 0.05) when analyzed urea fertilizer.
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
7
season; however, no significant difference was observed in 2014, when
the emissions decreased. Dry season CH4 emissions from dung were
higher in 2013 and did not differ from other treatments in the first year
of evaluation. Annual cumulative CH4 emission averages were 33.7,
15.2, 41.5, and 50.8 mg C−CH4m−2 for the control, urine, dung plus
urine, and urea fertilizer treatments, respectively. The highest cumu-
lative CH4 emissions were found in the 2013 wet season
(331 ± 111mg C−CH4m−2), followed by the 2013 dry season
(91 ± 22mg C−CH4m−2; Table 5).
3.7. Methane emission factors for beef cattle dung
The calculated EFs for beef cattle dung were 0.79 and 0.18 kg CH4
head−1 year−1 during the wet and dry seasons, respectively.
Annualized CH4 EF was 0.54 kg CH4 head-1 year−1.
3.8. Soil water-filled pore space
3.8.1. Soil water-filled pore space variation during dry season
During the 2012 dry season, the WFPS levels at 0–10 cm soil depth
were approximately 40%, they declined to approximately 30% at 27
DAA, increased to approximately 50% at 45 DAA, and then gradually
decreased until the end of the trial. In the first four days of observations,
WFPS was higher in the urine and dung plus urine treatments (Fig. 6 a).
During the 2013 dry season, WFPS was approximately 20% at 5 DAA,
except for in the urine treatment. WFPS then increased to 60% at 20
DAA, and gradually declined to approximately 20–25% by 65 DAA.
This level persisted until the end of the experiment (Fig. 6 c).
We used the multivariate regressions analysis to identify which
variables are driving N2O emissions. Only soil moisture was the key
driver of N2O flux during dry season evaluations. A significant Pearson
positive correlation between N2O flux and WFPS was found in the
background control, dung, and urine treatments in 2012, and with the
urine and urea treatments in 2013. However, the correlation was weak.
A positive correlation was found between CH4 fluxes and dung during
the 2012 dry season (Table 6).
3.8.2. Soil water-filled pore space variation during the wet season
The WFPS showed considerable temporal variation during the wet
season; however, it did not vary between treatments. During 2013,
WFPS
for 0–10 cm soil depth varied from 20 to 70% during the first 85
DAA. The lowest mean WFPS was recorded at 10 DAA (20%) and the
highest at 95 DAA (90%), which then decreased to 50% by the end of
the experiment (Fig. 6 b). During 2014, WFPS ranged from 40 to 60%.
WFPS was the lowest at the commencement of the experiment and at
45, 65, and 80 DAA, and the highest at 25, 50, and 95 DAA (Fig. 6 d).
The WFPS presented a significant Pearson correlation with CH4 for the
control treatment (p < 0.1; r= 0.23) in the 2013 wet season (Table 6).
3.9. Soil inorganic-N
During the dry seasons, NO3-N was similar between all treatments.
During the wet seasons, NO3-N content was similar between treatments
in 2013, and was higher for urine and dung plus urine in 2014 (Fig. 7).
Soil NH4-N content was generally higher as compared to NO3-N; it
was lower during dry season experiments and higher during the first
year of evaluation (Fig. 8). The quantity of NH4-N presented a sig-
nificant positive Pearson correlation with N2O for urine plus dung
(p < 0.05; r= 0.38) in the 2013 wet season and urine plus dung
(p < 0.05; r= 0.31) in the 2014 wet season. Furthermore, NH4-N
presented a significant positive Pearson correlation with CH4 for urine
plus dung (p < 0.1; r= 0.17) in the 2012 wet season, and urea
(p < 0.01; r= 0.53) in the 2014 wet season (Table 6). WFPS, NH4-N,
and NO3-N were the key determinants of N2O and CH4 emissions for
most treatments. N2O emissions were driven by WFPS soil mineral-N
during the dry and wet seasons, respectively (Table 7).
4. Discussion
4.1. Ammonia volatilization
Several edaphoclimatic factors influence the mechanisms of NH3
volatilization (Sommer and Hutchings, 2001). Our results showed that
FracGASF from urine-N were higher in the dry season as compared to
the wet season during study years and ranged from 5.0 to 20.9%
(Table 3). According to Saarijärvi et al. (2006), following long periods
without rain, ammonia volatilization losses may be higher in dry soil,
and ammonia losses significantly decreased after rainfall duo to in-
creases in soil moisture content (Oenema and Velthof, 1993). We found
that soil moisture optimized nitrogen incorporation into the soil. In the
Brazilian Cerrado, Lessa et al. (2014) found urine-N losses of 20.8% and
23.6% during the dry and wet seasons, respectively. Whitehead and
Raistrick (1993) studied NH3 volatilization from 22 soils from England
and Wales and found that volatilization ranged from 6.8 to 41.3% of
Fig. 6. As in Fig. 2 but for water filled pore space (WFPS) at soil depth of 0–10 cm.
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
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total urine-N, with a mean value of 26.5%. Laubach et al. (2013) stu-
died NH3 emissions from urine excreted on New Zealand pastures and
found that emissions represented 25.5% of the excreted urine-N. A large
variation (1.5–40%) in NH3 volatilized was found when urine was the N
source under evaluation in temperate grasslands soils (Petersen et al.,
1998; Bol et al., 2004; Mulvaney et al., 2008). These authors quantified
NH3 volatilization for a range of temperate grasslands and soil moisture
conditions.
A crust can form on dung, making nitrogen in the dung somewhat
recalcitrant, and thus providing an explanation for the lower N losses in
dung as compared to urine. Furthermore, N can become immobilized
during dung decomposition (Petersen et al., 1998). Depending on en-
vironmental conditions, organic dung-N may take more than a single
growing season to mineralize (Wachendorf et al., 2008). Here, we
found no differences in dung-N lost from NH3 volatilization between
the dry and wet seasons; losses were 6.0% and 7.2%, respectively
(Table 3). Our data appear to be an approximate average of the re-
ported values for N volatilization in previous studies. The dung-N loss
fraction averaged 1.5% from studies in England (Ryden et al., 1987)
and Finland (Saarijärvi et al., 2006); 2.5% during the wet season and
4.3% during the dry season in the Brazilian Cerrado (Lessa et al., 2014);
and 4.5% (Sugimoto et al., 1992) and 11.6% (Laubach et al., 2013) in
New Zealand.
In the dung plus urine treatment, the percentage of N losses did not
differ from urine, and were 11.5% and 6.4% for the dry and wet sea-
sons, respectively (Table 2). This result suggests that liquid urine could
be suppressing the mechanisms that protected dung-N from volatiliza-
tion, and the urea content in the urine may contribute to the higher NH3
volatilization rates from dung plus urine treatment.
The N volatilized from fertilizer varied markedly, and depended on
the fertilizer formulation. Sources of N such as ammonium nitrate,
calcium nitrate, and ammonium sulfate were not subject to greater
losses by NH3 volatilization in acid soils (Cantarella, 1998) as compared
to urea. The FracGASF amounted to 16.9% of applied N (Table 3),
higher than the default IPCC emission factor of 10%. In the wet season,
we found an interannual effect on NH3 volatilization. It is possible that
this variation occurred due to the diminution in precipitation and
subsequent variations in soil moisture that strongly influenced NH3
production.
Our results were near the bottom of the range (18–64%) of N lost as
Table 6
Pearson correlation coefficients (r) between N2O or CH4 fluxes from dung, urine, dung+ urine, and urea fertilizer with explanatory variables (0–10 cm of soil depth)
per season and year of evaluation.
N2O CH4
Season/year Treatment % WFPS N-NO3− N-NH4+ % WFPS N-NO3− N-NH4+
Dry 2012 control 0.48* 0.27.
dung 0.47* 0.19.
urine 0.50*
urine+ dung
Dry 2013 dung 0.28. 0.36*
urine 0.30*
urine+ dung 0.28.
urea 0.29*
Rainy 2013 control 0.23.
dung 0.38* 0.38*
urine
urine+ dung 0.38* 0.17.
Rainy 2014 urine+ dung 0.31*
urea 0.47** 0.53**
†Significance code:. p < 0.1.
* p < 0.05.
** p < 0.01.% WFPS=percentage of water filled pore space.
Fig. 7. As in Fig. 2 but for soil nitrate content (mg N-NO3− kg-1 dry soil) at a depth of 0–10.
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
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volatilized NH3 from urea fertilizer observed in a study conducted at
several sites in São Paulo, Brazil (Cantarella and Marcelino, 2007). Our
data suggests that the IPCC guidelines overestimate FracGASM and
underestimate FracGASF in tropical regions.
4.2. Effect of excreta type and season on N2O fluxes
The N2O fluxes from urine, urine plus dung, and urea followed the
typical emission peaks (within 7 DAA) reported in previous studies (de
Klein et al., 2003; Hoeft et al., 2012; Lessa et al., 2014; Sordi et al.,
2013), except for the rainfall response observed in 2014. However, it is
important to note that in the 2014 wet season, the study region was
under a severe drought that affected soil moisture, temperature, and
grass growth which in turn affected gas production.
For the dung treatment, WFPS drove N2O fluxes in the 2012 dry
season and soil NO3− in the 2013 dry and wet seasons (Table 6).
However, the highest N2O emission peak was not related to a rainfall
event (Fig. 2) or the highest WFPS (Fig. 5). Wet soil and anaerobic
conditions did not necessarily increase N2O emissions (Ball, 2013) be-
cause other factors can limit N2O production (soil ammonium and
nitrate. After precipitation, anaerobic conditions favor denitrification to
N2 over N2O production (Jiang et al., 2011). Sordi et al. (2014) sug-
gested that WFPS did not closely reflect the rainfall pattern, perhaps
due to changes in soil water content caused by evapotranspiration or
drainage between rainfall events and soil sampling. The emission peaks
after dung application occurred in the first week, except for 2014 in line
with previous studies (Fig. 2). The delay observed in 2014 can be at-
tributed to annual precipitation differences.
Emission peaks for the urine and urine plus dung treatments oc-
curred within 5–45 DAA (Fig. 4), and declined to background levels by
90 DAA in line with de Klein et al. (2003); Hoeft et al. (2012); Lessa
et al. (2014) and Sordi et al. (2013). There was an
exception during the
2013 wet season, when higher N2O peaks for urine were observed at 94
DAA; this peak may be attributed to precipitation. In our study, emis-
sions from urine peaked later (at approximately 33 DAA; Fig. 4 b,c,d),
except during the 2012 dry season when emissions peaked at 20 DAA.
This was similar to Sordi et al. (2014), who found peaks at 17 DAA for
urine and dung. The application of dung plus urine was not compared
to previous studies which applied these excreta individually. Nitrous
oxide patterns for the dung plus urine treatment were similar to that of
Fig. 8. As in Fig. 2 but for soil ammonium content (mg N-NH4+ kg−1 dry soil) at a depth of 0–10.
Table 7
Multiple and single linear regression models accounting for variation in N2O fluxes from dung, urine, dung+urine, and urea fertilizer using explanatory variables.
Gas Treatment Variable Estimate SE P value Model R2
N2O Dry 2012 control % WFPS −11.55 2.53 P=0.02 0.24
dung % WFPS −1172.46 475.4 P=0.02 0.22
urine % WFPS −993.0 370.1 P=0.01 0.26
Dry 2013 dung Nitrate −2.99 2.3 P=0.06 0.18
urine % WFPS 1.36 0.56 P<0.05 0.30
urea % WFPS 61.92 43.4 P=0.03 0.31
Rainy 2013 dung Nitrate −10.2 5.6 P=0.05 0.23
urine Nitrate 8.08 4.5 P=0.06 0.19
dung+urine % WFPS 0.27 0.14 P=0.07 0.17
Rainy 2014 dung+urine Precipitation Ammonium 0.38 −2.07 0.04 1.37 P=0.05 0.31
urea Nitrate 4.53 1.88 P=0.02 0.49
CH4 Dry 2012 control % WFPS −15.8 12.3 P=0.06 0.25
dung % WFPS −295.6 337.1 P=0.09 0.17
Dry 2013 dung Nitrate −4.42 2.5 P=0.04 0.37
dung+urine Nitrate −1.25 0.9 P=0.01 0.29
Rainy 2013 control % WFPS 94.1 53.8 P=0.09 0.14
dung Nitrate −40.2 21.4 P=0.07 0.18
Rainy 2014 dung+urine Ammonium −0.38 0.09 P=0.07 0.17
urea Ammonium 1.49 0.52 P<0.01 0.57
SE – Standard error and % WFPS=percentage of water filled pore space.
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
10
urine.
Studies have suggested that N2O production after urine or dung
application occurred both via autotrophic nitrification and hetero-
trophic denitrification (Flessa et al., 1996; Carter, 2007; Mazzetto et al.,
2014), whilst others suggest that nitrification is the main N2O produ-
cing process (Koops et al., 1997; Bol et al., 2004; Lessa et al., 2014) or
that denitrification is the principal process (Yamulki et al., 2000; van
Groenigen et al., 2005). Denitrification predominates in anaerobic
conditions and nitrification under aerobic soils. In our study, for ex-
ample, during the 2013 wet season, N2O peaked between 10 and 31
DAA (Fig. 4), coinciding with the NH4-N peaks from 200 to
400mg kg−1 soil (Fig. 8) The delay observed in nitrification could be
due to the lack of precipitation. Sordi et al. (2014) attributed lower
NO3-N contents to a higher N loss via NH3 or a higher leaching of NO3-
N. Soil NH4-N contents higher than the NO3-N content after urine ap-
plication have been reported by several studies (Yamulki et al., 1998;
Hoeft et al., 2012; Sordi et al., 2014). Our results suggest that ni-
trification was the predominant process in N2O production in well-
drained ferralsol pastureland, which was supported by the fact that
WFPS was generally 40–60% (Fig. 5).
For the dung treatment, regression modeling suggested a relation-
ship between WFPS and nitrate-N to explain variations in N2O emis-
sions (Table 7). The low temperatures and WFPS of winter reduce the
microbial processes impacting N2O production and can explain the
lowest cumulative emissions of N2O and EF for urine in the dry winter
(Sordi et al., 2013). Contrary to tropical climates, winter soils are wet in
temperate region pastures, and the highest N2O emissions rates are
reported during the winter (Uchida and Clough, 2015). Although the
effect of WFPS and nitrate-N on N2O was observed the correlation was
weak (R2 lower than 0.5).
Higher N2O emissions during the wet season from urine was found
before. Lessa et al. (2014) found a large difference in N2O emissions
between seasons, with emissions from urine being almost zero in the
dry season. Soil moisture was a key driver regulating N2O production
and possibly explains the seasonal differences. Similar results were re-
ported by Tully et al. (2017) in Kenya and by Thomas et al. (2017) in
Canada; during drier seasons, moisture is the dominant mechanism
limiting N2O production.
For dung and urea treatments the absence of season effect on N2O
emissions are in line with Mazzetto et al. (2014) who found no seasonal
difference in the accumulated N2O emissions from dung. However, our
results showed a strong interannual variation in the dung and urea
treatments; the second year of the study showed markedly reduced
emissions. This reduction was contemporaneous with a period of
drought in the study region, which can explain the interannual differ-
ences. In tropical areas, the emissions in the first week after application
for the dung treatment are very important to the total N lost as N2O. For
example, Cardoso et al. (2018) found that more than 90% of cumulative
N2O emissions were emitted by 7 DAA. Our results did not show higher
N2O emissions during the first week after application in the 2014 wet
season, which may explain the lower N2O EF found in this study.
Negative fluxes have been reported in previous studies (Ball and
Clayton, 1997; Chapuis-Lardy et al., 2007; Lessa et al., 2014; Mazzetto
et al., 2014; Cardoso et al., 2017). For example, negative EFs (-0.23%
for dung) were found by van der Weerden et al. (2011), by Krol et al.
(2016) in Scotland (-0.2% for dung), and in Japan (-0.021%) by Mori
and Hojito (2015). These values indicate that N2O emissions from the
soil background were higher as compared to that induced by the ap-
plication of excreta. While we found negative fluxes in all seasons and
for all treatments (Fig. 4), these generally occurred during the dry
season. Hence, N2O production and consumption may be regulated by
interactions between the O2 concentration and soil moisture content
(Cheng et al., 2014). Overall, the factors regulating N2O consumption in
the soil are not well understood and additional research is needed to
better understand N2O uptake.
4.3. Differences in N2O emissions factor due to the type of excreta and urea
The type of excreta can influence N2O emissions (van der Weerden
et al., 2011; Krol et al., 2016). Immediately after animal urination,
urinary urea is rapidly hydrolyzed to ammonium in the soil, aug-
menting the soil pH and stimulating the release of water soluble carbon
available as a microbial food supply for denitrifying bacteria
(Monaghan and Barraclough, 1993). Subsequently, under favorable soil
conditions, ammonium can be quickly nitrified to nitrate and then
further denitrified to N2O and N2. In contrast to urine, there is sig-
nificantly less mineral N in dung. Consequently, soil N transformation
activity beneath dung patches is lower. According to Van der Weerden
et al. (2011) interaction between the dung patches and the soil mi-
crobial community can be restricted because of the high dry matter
content of dung. This can also reduce the potential for dung-N to in-
filtrate into the soil, resulting in less available N to be emitted as N2O.
On a subtropical Brazilian pastureland, Sordi et al. (2013) found the
EF from dung (0.15%) to be lower than that of urine (0.26%). Lessa
et al. (2014) found emissions from urine-N to be 14 times greater than
dung-N during the wet season and, for both excreta, there were prac-
tically zero emissions during the dry season. Moreover, Mazzetto et al.
(2014) concluded that feces cannot be considered an N2O source under
the conditions of their experiment (they measured N2O emissions on
subtropical and tropical sites in Brazil during 30 days of a winter and a
summer season). Our findings are in line with Sordi et al. (2013) and
Krol et al. (2016); the main source of N2O is urine during the wet
season.
Unlike previous studies, our results showed that the dry season N2O
EF was higher for dung compared to urine. Wachendorf et al. (2008)
also found a higher EF
for dung as compared to urine in a temperate
region; they attributed the higher emissions to freeze-thaw events.
Urine-induced N2O emissions originate mainly from the indigenous soil
mineral N pool as opposed to applied urinary-N (Wachendorf et al.,
2008). In our study, it is possible that the lack of rain affected ni-
trification and the amount of available NO3− for N2O emissions from
urine. We included the treatment dung plus urine to contribute to the
debate of disaggregating EF3PRP. Our results illustrated that the com-
bined EF was similar to that of urine. Urine application on dung patches
could break down barriers to urea hydrolysis and N infiltration from the
dung, resulting in N2O emissions similar to urine (Table 4).
The IPCC EF3PRP guideline for cattle excreta is 2%. The EF measured
here varied from 0.32 to 1.02% The urine EF differs markedly as
compared to those obtained under subtropical conditions (0.26%) by
Sordi et al. (2013) and are similar to those measured in the Cerrado
(0.7%) by Lessa et al. (2014). This variation maybe is also due to the
pasture management and forage composition.
Grass production is seasonal and variations in the chemical com-
position of forage is expected. Animal supplementation with different
nitrogen and energy compositions can be used to improve animal per-
formance on grassland. These would result in different N rates in the
excreta and biochemical compositions of dung. Data on the impacts of
forage chemical composition, forage species and animal supplementa-
tion in tropical regions are lacking. Further research is required to
understand the effect of these variables on N2O emissions.
The EFs found in this study were 0.32% and 1.02% for urine during
the dry and wet seasons, respectively, and 0.34% and 0.84% for dung
plus urine during the dry and wet seasons, respectively. Based on the
lengths of the dry and wet seasons, the annual EF was 0.73% and 0.63%
for urine and dung plus urine, respectively.
The EFs for both urine, and dung plus urine in the tropical ferralsol
found in this study are at the bottom of the previously reported global
range (0.0–8.6%; Krol et al., 2016; Cardoso et al., 2017; Hörtnagl et al.,
2018). This can be attributed to a WFPS of 40–60% during most of the
experimental period which, combined with the available mineral N
content, created ideal conditions for N2O production via nitrification as
opposed to denitrification. Our study used synthetic urine to determine
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
11
the EF (0.73%), which was similar to that of Lessa et al. (2014; 0.7%).
Furthermore, our findings are in line with Krol et al. (2016), who found
similar EFs using synthetic urine and real urine at several sites.
Therefore, synthetic urine appears to be a reasonable proxy for real
urine.
These EFs of 0.4% for dung were higher as compared to previous
studies. For example, Sordi et al. (2014) reported an EF of 0.15% in a
subtropical region, while in the tropical Cerrado, Lessa et al. (2014)
estimated an EF of 0.1%. Furthermore, in temperate regions an EF of
0.25% was reported in New Zealand (Saggar et al., 2015) and 0.31% in
Ireland (Krol et al., 2016). The N2O EFs for dung ranged from
-0.20–1.48% in grassland (Krol et al., 2016) and achieved 5.67% in
controlled conditions (Cardoso et al., 2017). The EF for dung is lower as
compared to urine because dung patches tend to dry rapidly, tem-
porarily immobilizing the N during C decomposition. Conversely, cattle
urine is mainly comprised of urea (Spek et al., 2012), which is rapidly
hydrolyzed by soil urease, increasing the NH4-N available at the soil
surface.
We summarized the EFs from excreta published in recent years in
Table 8. Emissions from urine ranged from 0.02%, measured in a dry
region of Australia, to 4.9%, found in a tropical region of Brazil (Ward
et al., 2016; Cardoso et al., 2018). The mean EF for urine was 0.84
(± 0.2)%. Emissions from dung varied from -0.021%, in a volcanic
region of Japan, to 3.47%, in a forest region of Colombia (Mori and
Hojito et al., 2015; Rivera et al., 2018). The mean EF was 0.27
(± 0.1)% for dung and 0.63(± 0.2)% for dung plus urine. The IPCC
recommended EF3PRP of 2% is higher than the emissions reported in the
recent literature, and the results of this study.
We summarized the EFs reported from field studies over the pre-
vious three years (Table 8). The mean EF for urine calculated by us
(0.84%) from recent studies is in line with that of 0.76% as compiled by
Cai and Akiyama (2016) from 418 studies. For dung, the mean EF
(0.27%) from recent studies was also like the EF (0.28%) calculated by
Cai and Akiyama (2016), and to the EF (0.23%) calculated by Kelliher
et al. (2014) from 185 field trials conducted across New Zealand. Urine
emissions appear to be three times greater as compared to dung.
Our results further support the necessity of disaggregating N2O
EF3PRP for ruminant urine and dung deposited onto pastoral soil, as
suggested by Van der Weerden et al. (2011), Sordi et al. (2013), Lessa
et al. (2014), and Krol et al. (2016). Our findings suggest that the de-
fault 2% EF3PRP may be overestimated for tropical soils. However,
findings from other studies in Brazil indicate that EFs would need to be
adopted according to the climatic region to ensure accurate N2O
emission data for Brazilian livestock.
Table 8
A review of reported N2O emission factors (EF) for excreta on pasture soils in the last ten years in the literature (only field studies).
Country Climate Soil type Period (d) Excrete type N2O EF (%) Reference
Brazil Tropical Clay loam 48 urine 0.1-2.55 Lessa et al. (2014)
Scotland Temperate sandy loam 365 urine 0.64-1.13 Bell et al. (2015)
Scotland Temperate sandy loam 365 A. urine 0.37-1.14 Bell et al. (2015)
Brazil Tropical Sandy loam 30 urine 0.13-0.37 Mazzetto et al. (2014)
Colombia Tropical Silt clay loam 29 urine 0.07 Byrnes et al. (2017)
Brazil Tropical Sandy loam 47 urine 2.43-4.9 Cardoso et al. (2018)
Ireland Temperate sandy loam 365 urine 0.30-0.32 Krol et al. (2016)
Ireland Temperate sandy loam 365 urine 0.34-1.16 Krol et al. (2016)
Ireland Temperate Clay loam 365 urine 1.12-4.81 Krol et al. (2016)
United states Semi-arid Fine loamy 365 urine 0.11-0.13 Nichols et al. (2016)
Kenya arid Sandy 365 urine 0.0 Tully et al. (2017)
Canada Temperate Clay loam 365 urine 1.32 Thomas et al. (2017)
Canada Temperate Clay 120-365 urine 1.09 Rochette et al. (2014)
Canada Temperate Clay 120-365 urine 0.31 Rochette et al. (2014)
Brazil Subtropical Clayey 90 urine 0.10-0.45 Sordi et al. (2013)
New Zealand Temperate Silt loam 125-173 urine 0.29 Van der Weerden et al. (2011)
Ireland Temperate Sandy loam 80 urine 0.10-0.24 Selbie et al. (2014)
New Zealand Temperate Poor drained 135 A. urine 0.5-0.9 de Klein et al. (2014)
New Zealand Temperate Free drained 135 A. urine 0.03-0.3 de Klein et al. (2014)
Japan Temperate Volcanic 78-85 urine 0.24-1.14 Mori and Hojito (2015)
Australia Subtropical Sandy 90-245 urine 0.02-0.47 Ward et al. (2016)
Colombia Tropical Clay loam 102 urine 1.37-1.77 Rivera et al. (2018)
New Zealand Temperate Clay or sand 180 urine 0.16-0.57 Luo et al. (2019)
Brazil Tropical Clay 104 urine 0.32-1.20 This study
Mean 0.84(±0.2)
Brazil Tropical Clay loam 48 dung 0.0-0.16 Lessa et al. (2014)
Scotland Temperate sandy loam 365 dung 0.56-0.64 Bell et al. (2015)
Brazil Tropical Sandy loam 15 dung 0.18 Cardoso et al. (2018)
Ireland Temperate sandy loam 365 dung −0.02-0.13 Krol et al. (2016)
Ireland Temperate sandy loam 365 dung 0.06-0.24 Krol et al. (2016)
Ireland Temperate Clay loam 365 dung 0.15-1.48 Krol et al. (2016)
United states Semi-arid Fine loamy 365 dung 0.10 Nichols et al. (2016)
Kenya arid Sandy 365 dung 0.18 Tully et al. (2017)
Canada Temperate Clay loam 365 dung 0.03 Thomas et al. (2017)
Canada Temperate Sandy loam 120-365 dung 0.08 Rochette et al. (2014)
Canada Temperate Sandy loam 120-365 dung 0.15 Rochette et al. (2014)
Brazil Subtropical Clayey 90 dung 0.09-0.40 Sordi et al. (2013)
New Zealand Temperate Silt loam 125-173 dung 0.04 Van der Weerden et al. (2011)
Japan Temperate Volcanic 78-85 dung −0.021-0.086 Mori and Hojito (2015)
Australia Subtropical Sandy 90-245 dung 0.01-0.09 Ward et al. (2016)
Colombia Tropical Clay loam 102 dung 0.3-3.47 Rivera et al. (2018)
New Zealand Temperate 180 dung 0.05-0.27 Luo et al. (2019)
Brazil Tropical Clay 104 dung 0.15-0.58 This study
Mean 0.27(±0.1)
Brazil Tropical Clay 104 dung+urine 0.34-0.84 This study
Mean 0.63
A.d.S. Cardoso, et al. Soil & Tillage Research 194 (2019) 104341
12
This is the first study on N2O emissions from urea fertilizer applied
to pasturelands in Brazil. Our reported EFs (1.00%±0.3 and
0.71%±0.2) indicate that the IPCC (2006) default EF (1%) for N-fer-
tilizer is appropriate. It is widely known that during N fertilization, the
N from fertilizer exceeds that of excreta. Further research is required to
determine if N fertilization on excreta patches increases the total and/or
fertilizer-derived N2O emissions in tropical grassland soils.
4.4. Effect of season and excreta of CH4 fluxes from dung
Ideal conditions for methanogenic microorganisms were found in
the dung patch after excretion, which resulted in higher CH4 production
in the days following excretion (Jarvis et al., 1995; Sherlock et al.,
2003; Saggar et al., 2004; Mazzetto et al., 2014). In our study, CH4
initially peaked at 3 DAA with a secondary peak at 27 DAA (Fig. 5).
During the first week, dung emissions were attributed to the available C
in feces and the presence of methanogenic bacteria. We observed CH4
oxidation on most days, principally during the dry season (Fig. 5 a, c).
The high oxygen availability and low C availability in a tropical pas-
tureland contribute to methanotrophy as opposed methanogenesis.
Methanogenesis is directly related to soil water content (Le Mer and
Roger, 2001). In our study, CH4 emissions were high during the first 7
DAA in the 2013 wet season, possibly due to high carbon and moisture
content at the time of application, or higher residual archaea in the
dung. Forage chemical composition (e.g. protein and fiber content) can
differ between species (Ravetto et al., 2017), influencing the bio-
chemical composition of the dung (C/N and lignin/N ratios) and con-
sequently, the available C, which can impact CH4 production. Some
forage species have substances (e.g. tannins) that can inhibit CH4 pro-
duction in the rumen (Naumann et al., 2017). However, the con-
centrations of these substances in dung and their effect on CH4 pro-
duction of dung were not investigated in this study.
Seasonal variation in CH4 emissions was related to air temperature
and feces water content. Emissions during the wet season were 4.4, 2.1,
3.1, and 3.4 times higher as compared to the dry season for dung, urine,
dung plus urine, and urea, respectively (Table 5). Several studies have
found higher emissions during the summer (Williams, 1993; Holter,
1997; Mazzetto et al., 2014). Seasonal effects are significant im-
mediately after feces application, and negligible thereafter (Yamuki
et al., 1999). Similar variation in the magnitude of CH4 emissions
within season was found by Mazzeto et al. (2014), with emission peaks
occurring throughout their experiment, mainly influenced by rain
events.
During the wet season, higher temperatures and rainfall provide
ideal conditions for CH4 emissions. Dung remains wet, as compared to
the dry season, when the feces dries rapidly and forms a crust that re-
duces CH4 emissions (Yamulki et al., 1999). In a tropical pastureland,
the litter C/N ratio is higher (> 45) and the application of N rapidly
decomposes this material (Boddey et al., 2004). We attribute the higher
CH4 emissions from the urine and urea treatment during the wet season
to rainfall stimulated litter decomposition. Here, interactions between
moisture and temperature during the wet and warm summer appear to
be even more relevant, increasing the emissions in tropical soils as
compared to Mazzeto et al. (2014). Optimal microenvironments for
anaerobic microorganisms are created when cattle excreta are under
warm and moist conditions that favor CH4 production (Saggar et al.,
2004).
4.5. Differences in CH4 emissions by type of excreta
Methanogenic bacteria are excreted in dung. These bacteria and the
higher dung C content produce CH4 (Saggar et al., 2004). Hence, CH4
emissions from dung patches were five times higher as compared to
other treatments. Cumulative CH4 emissions showed significant differ-
ences for dung treatments only. Urine, dung plus urine, and urea fer-
tilizer cannot be considered an extra source of CH4 because they were
like control emissions (Table 5). Lin et al. (2009) reported that dung
patches were a major CH4 source, in line with our findings. However,
Jiang et al. (2012) studied dung and urine patches from sheep, and
found no difference according to the type of excreta. It is possible that
the different nutrient transformation characteristics for sheep and beef
cattle dung patches are influenced by the covered area, nutrient con-
centration, and differences in shape.
The EF for dung as determined by this study was 0.54 kg
head−1 year−1; half that of the IPCC guideline. However, it was higher
than the reported EFs (Mazzetto et al., 2014) for subtropical and tro-
pical regions; 0.02 (winter) and 0.05 (summer) kg CH4 head−1 year−1
in São Paulo, and 0.06 (winter) and 0.10 (summer) kg CH4 head-1
year−1 in Rondônia. Finally, it was lower than Cardoso et al. (2018)
who reported an EF of 0.95 kg head−1 year−1 from the dung of dairy
cattle in tropical pastureland in Rio de Janeiro.
5. Conclusion
Ammonia volatilization was affected by the type of excreta, season,
and year. Emissions from urine and urine plus dung were higher than
those from dung in the 2012 and 2013 dry seasons. However, dung
demonstrated the highest loses in the 2013 wet season. NH3 emissions
were higher during the dry season, except for dung in 2012. NH3 vo-
latilization from urea fertilizer was not influenced by the season.
Nitrous oxide and CH4 emissions differed according to the season
and type of excreta. Results from the 2014 wet season were impacted by
severe drought. N2O and CH4 emissions were higher during the wet
season. The higher source of N2O emissions during the wet season was
urine, and dung during the dry season. Overall, dung had the highest
CH4 emissions.
NH3, N2O and CH4 emissions differed from the default IPCC emis-
sion factors, which suggested that may be the default EFs do not esti-
mate well the GHGs emissions for the studied area and similar grass-
lands sites Nitrous oxide EFs were higher than IPCC EFs, indicating that
a single EF for urine and dung may be not appropriate. However, ex-
creta emission differences depend on the key drivers controlling emis-
sions. Our findings support the suggestion of disaggregation of the IPCC
EF3PRP, as suggested by van der Weerden et al. (2011); Lessa et al.
(2014) and Krol et al. (2016).
Emissions from urea fertilizer, dung plus urine, and urine treatments
were like the control, suggesting that these sources do not contribute to
net CH4 emissions. The key drivers of N2O and CH4 emissions were not
clear. WFPS and mineral-N content were correlated with wet season
N2O and CH4 fluxes.
Acknowledgments
This work was funded by the Fundação de Amparo a Pesquisa do
Estado de São Paulo “São Paulo Research Foundation” (FAPESP grants
#2011/00060-8, #2012/06718-8, #2012/04605-1, #2013/00204-5,
#2013/24782-8). The authors ASC, SCO and ESM thank FAPESP for
their scholarships. The authors ACR, LFB and ERJ are grateful to the
Conselho Nacional de Desenvolvimento Científico Tecnológico (CNPq)
and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior
(CAPES) for their scholarships. The authors would like to thank the
anonymous reviewers for their valuable comments and suggestions to
improve the quality of this paper.
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