Bovine urine and dung deposited on Brazilian savannah pastures

Agriculture, Ecosystems and Environment 190 (2014) 104–111
Contents lists available at ScienceDirect
Agriculture, Ecosystems and Environment
journal homepage: www.elsevier.com/locate/agee
Bovine urine and dung deposited on Brazilian savannah
pastures contribute differently to direct and indirect soil nitrous
oxide emissions
Ana Carolina R. Lessa a , Beata E. Madari b , Debora S. Paredes a , Robert M. Boddey c ,
Segundo Urquiaga c , Claudia P. Jantalia c , Bruno J.R. Alves c,∗
a
Soils Department, Universidade Federal Rural do Rio de Janeiro, BR 465 km 7, Ecologia, 23890-000 Seropédica, RJ, Brazil
Embrapa Arroz e Feijão, Rodovia GO-462, km 12 Zona Rural, 75375-000 Santo Antônio de Goiás, GO, Brazil
c
Embrapa Agrobiologia, BR 465, km 7, Ecologia, 23891-000 Seropédica, RJ, Brazil
b
a r t i c l e
i n f o
Article history:
Received 23 April 2013
Received in revised form
19 December 2013
Accepted 6 January 2014
Available online 13 February 2014
Keywords:
15
N balance
Cattle excreta
Greenhouse gases
NH3 losses
a b s t r a c t
Cattle ranching is one of the most important agricultural activities in Brazil. The impact of livestock on
soil N2 O emissions in Brazil has only been assessed using a Tier 1 approach of the IPCC guidelines, as there
are no data available from field studies. Apart from the need for accumulating data for the development
of proper direct N2 O emission factors, we tested for possible differences between urine and dung as N2 O
sources and the difference in emissions between the dry and wet season. An area of Brachiaria brizantha at
the Embrapa Rice and Bean Centre in the Cerrado (central savannah) region (Goiás state) was subdivided
into plots where fresh cattle urine and dung were monitored for three consecutive periods (two in the
rainy and one in the dry season) for N losses, principally N2 O emissions and NH3 volatilization. 15 Nlabelled urine N was used in the first monitoring period for an N balance study which indicated that
denitrification and NH3 volatilization were the most important processes for N loss. Percentages of N lost
as N2 O and as volatilized NH3 were greater for urine than for dung. In addition, N losses as N2 O in the
rainy season were much greater than during the dry season. Representing the Cerrado region and the
extensive pasture systems common in this region, direct emission 0.007 g N2 O–N g−1 (0.7%) excreta N,
well below the EF3PRP of 0.020 g N g−1 (2%) used by IPCC for cattle N in excreta. The fraction of excreta N
lost as NH3 of ∼15% was in line with the IPCC guidelines. Disaggregation of emission factors for excreta
type is recommended.
© 2014 Elsevier B.V. All rights reserved.
1. Introduction
Anthropogenic emissions of greenhouse gases (GHGs) in Brazil
are dominated by emissions of enteric methane from cattle, and
nitrous oxide derived from the excreta they deposit on pastures. It is
estimated that enteric methane contributes 56% of the emissions in
the agricultural sector and nitrous oxide 23% (Ministério de Ciência,
Tecnologia e Inovação (MCTI), 2013). Together they constitute 28%
of the total Brazilian national inventory.
In Brazil, approximately 37% of the 150 million hectares under
cultivated pastures are located in the Cerrado area (Bustamante
et al., 2012a). These pastures are dominated by Brachiaria species
and are principally used for extensive beef production systems
(Ferraz and Felício, 2010) with approximately 80 million cattle
∗ Corresponding author. Tel.: +55 21 3441 1516/+55 21 8111 2463(mob);
fax: +55 21 2682 1230.
E-mail addresses: [email protected], [email protected] (B.J.R. Alves).
0167-8809/$ – see front matter © 2014 Elsevier B.V. All rights reserved.
http://dx.doi.org/10.1016/j.agee.2014.01.010
or 40% of the national herd (Instituto Brasileiro de Geografia e
Estatística (IBGE), 2013).
The annual amount of N excreted by grazing cattle depends
on the protein content of the diet but average values for the
dominant pasture systems of Latin America were estimated at
40 and 70 kg N head−1 yr−1 for beef and dairy cattle, respectively
(Intergovernmental Panel on Climate Change (IPCC), 2006). Estimates for Zebu steers grazing on Brachiaria humidicola pastures in
southern Bahia state (Brazil), varied from 91% to 95% of ingested N,
or 30 to 43 kg N head−1 yr−1 depending on stocking rates (Boddey
et al., 2004).
Following IPCC guidelines, a direct N2 O emission factor of
2% is the default for total excreted N on pastures. In addition,
factors of 20% and 30% are used to estimate N losses by ammonia volatilization/NOx emissions and N losses by leaching/runoff,
respectively. From these N losses the indirect (off-site) soil emissions of N2 O are computed (Intergovernmental Panel on Climate
Change (IPCC), 2006). While, in the absence of specific measurements, this methodological approach is of value for estimating
A.C.R. Lessa et al. / Agriculture, Ecosystems and Environment 190 (2014) 104–111
GHG emissions, the use of default data may lead to large errors
in the GHG inventory. For livestock, the available N2 O data used
for emission factors comes predominately from a few countries of
temperate climate (van Groenigen et al., 2005; Smith et al., 2004)
as there is a lack of research in other environments.
Edaphoclimatic conditions in the Cerrado region contrast
greatly with most temperate and even sub-tropical regions. In the
Cerrado, it is estimated that 61% of the soils are highly weathered
Oxisols or Entisols, which are very freely draining (Lopes, 1996).
Rainfall is generally between 1200 and 1600 mm and approximately 90% occurs during the warm summer season from October
to April (Lopes, 1996). Daytime temperatures at this time of year
range from 25 to 35 ◦ C although extremes over 40 ◦ C may occur
(Bustamante et al., 2012b). The high rainfall coinciding with high
temperatures would likely result in rapid formation of anoxic
microsites in the soil, which would favour N2 O emissions (Smith
et al., 2003), but rapid drainage and high evapotranspiration rates
would suggest that these conditions would be transitory (Skiba and
Ball, 2002; Dobbie and Smith, 2003).
The dry season in the Cerrado is extremely severe with often
more than 100 days without rain. Thus nitrous oxide emissions
from excreta would be expected to be much lower in this period
of the year (Yamulki et al., 1998). However, according to Saarijärvi
et al. (2006) ammonia volatilization losses, especially from urine,
are likely to be higher.
The excreta type could also influence N2 O emissions (van der
Weerden et al., 2011). Considering the contrasting characteristics
of urine and dung, it is likely that their contributions to N2 O and
NH3 losses differ greatly. In the UK, Yamulki et al. (1998) reported
that 1% of cattle urine N and 0.53% of dung N were lost as N2 O
and higher emissions from urine than dung were also observed in
Germany (Flessa et al., 1996). Large differences in NH3 volatilization rates between excreta types have been reported, the highest
rates registered for urine (Petersen et al., 1998). Cattle ingesting
low quality diets excrete a greater proportion of N in dung than
cattle ingesting higher quality diets. For cattle grazing unfertilized
Brachiaria pastures in the Atlantic forest region of Brazil, the ratio
of faecal N to urine N was between 0.56 and 1.1 at a site in the South
of Bahia (Boddey et al., 2004) and as high as 3 in a hillside site near
Juiz de Fora (Minas Gerais) (Xavier et al., 2013).
The vast pasture area in Brazil localized in the Cerrado region
is contributing to the large impact of the livestock sector on the
nation’s GHG emissions, which generates an urgent demand for the
development of regional emission factors to improve the evaluation
of the impact of different management practices on GHG mitigation
strategies.
Therefore, the objective of this study was to quantify ammonia
volatilization and N2 O emissions from urine and dung artificially
deposited on a pasture area of the Brazilian Cerrado during both
the wet and dry seasons with the aim of developing regionally
appropriate emission factors.
2. Material and methods
2.1. Site description
The study was carried out on a grass pasture site of the Embrapa
Rice and Bean Centre experimental station (16◦ 28 S–49◦ 17 W,
823 m a.s.l.) located in the Municipality of Santo Antonio de Goiás,
State of Goiás. The climate is Aw, tropical savannah, megathermic,
according to the Köppen’s classification (Köppen, 1936). A characteristic of this region is that rainfall is practically absent from June
to September. The original vegetation of the region was a forest
type with a closed canopy (Cerradão) one of the sub-biomes of the
Brazilian Cerrados (Bustamante et al., 2012b).
105
Approximately two decades before this study a Brachiaria
brizantha cv Marandu pasture was established on a clay loam
soil (Ferralsol—FAO classification, Oxisol—US Soil Taxonomy) with
a texture of 43% clay and 44% sand in the top 20 cm. Soil
samples taken from the area presented the following fertility data: 10.4 g C kg−1 , 0.91 g N kg−1 , 3.6 mg P kg−1 , 90 mg K kg−1 ,
1.62 cmol Ca+2 dm−3 , 0.71 cmol Mg+2 kg−1 and pH 5.7 in water
(1:2.5). To comply with the standard low-input grazing in this
region neither liming nor basic fertilization were practiced in the
area for the study.
Three experiments were set up to study the N losses from cattle
excreta, two of them during the rainy season and one in the dry
season.
2.2. Preliminary trial on linearity of N2 O emissions
A preliminary study was performed to investigate the response
of N2 O emissions in closed static chambers during a period of
50 min. For this trial, five of the static chambers described below
(Section 2.6) were positioned on the pasture within a radius of 5 m
of each other over an area that had been amended with the equivalent of 60 kg N ha−1 as ammonium sulphate. Even though the soil
was moist from recent rainfall, the day before sampling 2 L of water
were distributed uniformly in each chamber (equivalent to 8 mm
of rainfall). The chambers were sealed and gas samples were taken
at approximately 09.00 h from each chamber approximately every
10 min up to 50 min after closure, the exact times being noted as
the samples were taken. The samples were taken and analysed as
described in Section 2.6.
2.3. Experiment 1
The experiment was performed on an area where a grazing simulation had established sward height at 15 cm. Plots of 1.5 × 1.5 m
were delimited in the area in order to accommodate the following
treatments: (1) a control without excreta; (2) cattle urine addition;
and (3) cattle dung addition. The three treatments were applied in a
randomized complete block design with six replications (18 plots).
In the centre of each plot, the base of a static chamber of
40 × 60 cm dimension was inserted into the soil to an average depth
of 5 cm. The details of the chambers are described in Section 2.6.
Urine and dung were collected fresh from crossbred dairy
(Nelore/Friesian) cows during milking at dawn on the day the
experiment was set up. The animals were kept in the pasture but
supplemented with soybean and corn meal. Approximately 15 kg
of fresh dung were well mixed in a container until visually homogeneous. A sample was taken for chemical analysis and the remainder
used in the experiment. Dung patches were artificially prepared by
pouring the dung (1.6 kg fresh weight, total N 4.2 g) into a 24 cm
diameter steel ring of 3 cm height in the centre of the static chamber
base. The final dung area was 0.045 m2 , which was close to the average area of 0.047 m2 dung−1 quantified by Braz et al. (2003) after
a 10-week period of monitoring a Brachiaria decumbens pasture
under grazing in Brazil.
One litre of urine labelled with 15 N was prepared by mixing
950 mL of fresh urine with 50 mL of urea solution of 17.6 mg N mL−1
containing 9.7 atom% 15 N in excess. The analysis of samples
from fresh and labelled urine revealed N concentrations of
9.8 mg N mL−1 and 10.2 mg N mL−1 , respectively. The labelled urine
ended up with 0.835 atom% 15 N excess and 1 L of the final solution
(10.2 g N chamber−1 ) was poured onto the soil surface delimited by
the walls of the static chamber base taking care to wet the whole
area inside the chamber limits. This volume of urine applied was in
the range of 0.8 to 1.7 L event−1 taken from the inventory data of
Whitehead (1995).
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The same volume of urine and mass of dung were equally placed
in a similar area close to the chamber in the respective treatment
plots, using an extra chamber base as a mould. This area was used
for ammonia volatilization measurements and also for soil sampling to determine soil moisture, NH4 + and NO3 − .
Gas sampling for N2 O started on 25 November 2009 and continued until 02 January 2010. In this same period, soil samples were
taken to monitor moisture and mineral N. In the dung area, samples
were carefully taken from below dung pats. Ammonia volatilization
was monitored over a period of 21 days starting at the same time
as N2 O measurements.
Plant and soil sampling for 15 N-urine balance study was performed on 11 February 2010.
2.4. Experiments 2 and 3
A second experiment was set up later in the rainy season.
Another area in the same pasture previously submitted to simulated grazing as before was divided into plots as in the first
experiment, and the same treatments were deployed following the
same experimental design. In this study, the amount of dung used
represented 4.2 g N chamber−1 , while the applied urine resulted in
6.4 g N chamber−1 . Gas sampling for soil N2 O flux determination
was done from 08 January to 12 April 2010. Ammonia volatilization
was monitored for 21 days from 08 January onwards.
This same procedure was repeated again for a third experiment carried out during the dry season. In this case, the added
dung was equivalent to 4.5 g N chamber−1 , and in the case of urine
9.5 g N chamber−1 . Soil N2 O measurements were taken from 15 July
to 13 August 2010 and ammonia volatilization was monitored for
21 days as before. For this experiment, a simulated rainfall of 8 mm
was applied on 01 August (2 L of water sprinkled over the internal
area of each 40 × 60 cm chamber) and again on 03 August when
20 mm was applied (5 L for each chamber).
2.6. Quantification of N2 O emissions
Nitrous oxide fluxes were measured every day from the application of cattle excreta until towards the end of each measurement
period when the sampling interval increased to every three days
or weekly, depending on the experiment. Gas sampling was performed using closed static chambers as described by Alves et al.
(2012). Each chamber was composed of a rectangular hollow
metal frame, 40 cm wide × 60 cm long × 17 cm in height which was
inserted about 5 cm into the soil and left for the whole experimental
period. Chambers tops were made of the same material as the base
and a soft rubber ring was fixed in its rim in order to ensure the seal
after coupling the top to the chamber base. The top of each chamber
was fitted with a three-way valve for gas sampling. At each sampling time, the top coupled to the chamber resulted in a headspace
height from 10 to 12 cm on average, but which was determined for
each chamber after 9 measurements with a ruler.
Gas samples were taken between 08.30 and 10.30 h (Alves et al.,
2012). Sampling time was 30 min, one sample being taken immediately after closure and another at the end of incubation time. The
gas accumulated in the headspace of each chamber was sampled
using polyethylene syringes and transferred immediately to 20 mL
chromatographic vials evacuated to −80 kPa just before by using a
hand vacuum-pump.
Analyses of N2 O concentrations were performed using a Perkin
Elmer Auto System XL gas chromatograph equipped with an electron capture detector and a back-flush system with a packed
Poropak Q column (Jantalia et al., 2008).
Soil N2 O fluxes were calculated as described in Jantalia et al.
(2008) and the emissions per experimental period were estimated
by the integration of the corresponding fluxes. The fraction of N as
urine or dung lost as N2 O was calculated by the ratio between the
emitted N2 O–N of the excreta deduced from that of the control and
the total N applied as excreta.
2.7. Ammonia volatilization
2.5. Urine-N balance by 15 N technique
For the first experiment (rainy season, starting 29 November
2009) a 15 N-aided N balance was performed on the added labelled
urine. All the aerial tissue including the standing dead material
was harvested from the chamber area. The existing litter was also
collected. The external area around the chamber (10 cm from the
chamber walls) had the aerial tissue and existing litter collected
and pooled. All this material was oven dried at 65 ◦ C for >72 h.
The soil from inside the area delimited by the chamber was
totally removed in 10 cm layers to 40 cm depth. Samples for soil
bulk density determination were also taken. The total soil mass of
each sampled layer was weighed and sieved to separate the root
material, which was also oven-dried at 65 ◦ C as for the other plant
material. The remaining soil was subsampled and air-dried in a
shaded area.
The dry soil and plant material were weighed and powdermilled for total N and 15 N analysis as described by Ramos et al.
(2001).
Urine-N recovered in plant or soil (%Rur) was determined as
follows:
% Rur =
% 15 NxsT × M × N
% 15 NxsU × UN
× 100
where % 15 NxsT is the atom % 15 N in excess of plant or soil material;
M is the plant or soil dry matter; N is the N fraction of plant or soil
material; %15 NxsU is the atom % 15 N in excess of urine; and UN is
the total N applied as urine.
Quantification of N volatilized was performed according to the
methodology of Araujo et al. (2009) as described by Jantalia et al.
(2012). For this technique, the NH3 is captured by a semi-open
chamber made of 2 L plastic (PET) bottles (10 cm diameter). Each
chamber was placed on the area affected by the excreta immediately after deposition. Following the protocol of the technique,
initially each two days and then each three days from the 4th
day, the acid-embedded foam strips were replaced with fresh ones.
Analysis of ammonium in the foam strips was performed by steam
distillation as described in De Morais et al. (2013).
The total volatilized NH3 in the 21 days period was calculated
from the addition of the amounts determined for each sampling
interval. The fraction of the N of the excreta lost as volatilized NH3
was calculated by the ratio between the N volatilized from the dung,
corrected for the volatilization from the control area, expressed as a
fraction of the N added as excreta. Adjustments of the total amount
lost for the affected area by each excreta type were performed.
2.8. Supporting variables
During the experimental period, rainfall and air temperature
were recorded by an automatic weather station situated 200 m
from the experiment.
On every day of gas sampling, soil samples were taken from
the 0–10 cm layer and oven-dried (105 ◦ C) to determine the water
content. Soil samples for bulk density calculations were also taken
from the area in order to calculate volumetric water content and
total soil porosity, and hence, water filled pore space (WFPS) as
described in Jantalia et al. (2008).
A.C.R. Lessa et al. / Agriculture, Ecosystems and Environment 190 (2014) 104–111
107
Fig. 1. Accumulation of soil N2 O in a static closed chamber during 50 min and the
goodness of fit to a linear function. Three asterisks indicate a significance level of
P < 0.001.
Twenty grams of the fresh soil were used to determine the soil
mineral N content. The fresh soil mass was extracted with 60 mL
2 M KCl after 1 h on a rotary shaker at 220 rpm. The supernatant was
filtered and the NO3 − and NH4 + concentrations were determined in
the resultant solution, respectively, by an automated flow injection
(FIA) system using Cd reduction and nitrite analysis (Giné et al.,
1980) and by the salicylate reaction (Alves et al., 1993).
The patterns of N2 O fluxes and volatilized ammonia during the
experimental period and also the 15 N recovery data were displayed
by using means and standard error of means. Integrated data for
each experimental period were submitted to ANOVA after testing
for normality and equal variance tests by using SAS Institute (1985),
and means were separated by Scott–Knott test at 5% probability.
3. Results
Results of the preliminary trial to investigate linearity of the emissions of N2 O
over a 50 min period showed that, while emission rates varied by more than a factor of three (0.50 to 1.64 ␮L N2 O L−1 h−1 ), none showed any consistent tendency to
deviate from a linear emission rate (Fig. 1).
Urine application to soil under the pasture dramatically increased N2 O fluxes
to >10 mg N m−2 h−1 in the first experiment. Response to urine application was also
observed in the second experiment conducted in the rainy season, but N2 O fluxes
were lower (Fig. 2A).
The N applied in dung was approximately half of that in urine but N2 O fluxes
were proportionately much lower; on most days ≤50 ␮g N m−2 h−1 with highest
flux of 316 ␮g N m−2 h−1 . For the second experiment, relative effects did not change
with N2 O fluxes of dung treated areas rarely exceeding 100 ␮g N m−2 h−1 (Fig. 2A).
Comparatively, soil N2 O fluxes in the control plots were very low ranging from
(apparently) slightly negative to a maximum of 23 ␮g N m−2 h−1 , considering both
experimental periods during the rainy season. For both experiments, the period of
high soil N2 O fluxes was restricted to a period of from application of treatments to
30 days after, which was better perceived taking into consideration the extended
period of gas sampling of the second experiment when induced N2 O fluxes by the
treatments ceased completely.
Rainfall events were frequent from the beginning of the first experimental
period with daily events frequently surpassing 20 mm. As a result, WFPS was maintained at 60% or above, with higher values under the dung patches occurring in
the first experiment than in the second (Fig. 2B). High soil moisture was accompanied by increased levels of soil NH4 + in the treatments receiving urine and dung
(Fig. 2C) although the urine-affected area presented the highest concentrations for
both experiments. Even though soil NO3 − had also been at higher concentrations
in the urine treatment, there was a clear difference between the two experimental periods when increased concentrations were much more apparent only in the
second experiment (Fig. 2D). A common trend captured in the second experimental period was the increased soil NO3 − concentration in the periods of diminishing
WFPS, when rainfall was not registered.
In the dry season measurable soil N2 O emissions were not induced by the
placement of urine and dung onto soil but only after the simulated irrigation
(Fig. 3A). Again the induced N2 O fluxes were greater for the areas treated with
urine, even though the magnitude of fluxes was far lower than those registered
Fig. 2. Nitrous oxide (A) fluxes from urine and dung patches artificially deposited on
a Brachiaria pasture on an Oxisol of the Cerrado region in Brazil during two consecutive experimental periods within the rainy season. Rainfall (bars) and water filled
pore space (WFPS—symbols) data during the same period (B) are presented along
with soil NH4 + (C) and NO3 − (D) availability. Bars are standard error of mean.
in the rainy season. Rainfall was practically absent during the dry season, which
brought about low WFPS levels, which were increased to close to 50% only after the
rainfall simulation (Fig. 3B). Soil NH4 + and NO3 − remained at low levels but NH4 +
increased after the first addition of water in all treatments and NO3 − only at the
end of the monitoring period when the soil started to dry again (Fig. 3C and D).
The net emission of N2 O during the 37 days duration of the first experiment
amounted to 1046 mg N m−2 for urine and 24 mg N m−2 for dung. For the second experiment, which lasted for 94 days, net emissions were 353 mg N m−2 and
25 mg N m−2 for urine and dung, respectively. The third experiment presented the
lowest net emissions for urine and dung of 4 and <1 mg N2 O–N m−2 , respectively.
Considering the total N applied as excreta, the fractions emitted as N2 O from urine
were 0.026 g N g−1 N urine for the first period and 0.013 g N g−1 N urine for the second
period of the rainy season and <0.001 g N g−1 N urine for the dry season (Table 1). In
the case of dung, the emitted fraction for the rainy season was 0.001 g N g−1 N dung
for the first period and 0.002 g N g−1 N for the second period of the rainy season and
for the dry season it was <0.001 g N g−1 N.
Ammonia volatilization was intense after urine deposition on soil, 80% occurring
within the first 2 days with the process ceasing within a week during the rainy
period (Fig. 4A and B). This behaviour was different for the dung-treated soil as NH3
volatilization increased after the first two to four days and ceased after 10 days or
later. There was also a trend of losses to remain at lower levels but for longer time
during the dry season (Fig. 4C).
The percentage of N lost as NH3 from urine-treated soil was 30.4% and 16.8%
of the N in the excreta, respectively, for the first and second periods of the rainy
season (Table 2). For the dry season, the percentage of N lost as NH3 was 20.8% of
the added urine N. In the case of dung, the proportion of N lost as NH3 percentages
were estimated at 2.3% and 2.6% for the first and second periods of the rainy season,
respectively, and 4.3% of dung N for the dry season.
Approximately 65% of the N added as urine was recovered in the soil–plant
system, plant material responding for approximately half of this total (Fig. 5). The
aerial tissues of Brachiaria accumulated 17.4% of the urine-N and the root system
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Table 1
Amount of N in cattle urine and dung used as soil treatment of the two experimental periods of the rainy season and one in dry season, and respective fraction of added N
emitted as N–N2 O.
Treatment
Amount of N in applied excreta (g N chamber−1 )
Rainy season
Urine
Dung
*
Fraction of added N emitted as N–N2 O (g N g−1 N excreta)
Dry season
Rainy season
Dry season
Nov/09
Jan/10
Jul/10
Nov/09
Jan/10
Mean
Jul/10
10.1
4.1
6.4
4.2
9.5
4.5
0.0255a*
0.0011b
0.0131a
0.0016b
0.0193
0.0014
0.0001a
0.0000a
Mean N data followed by a same letter did not differ in the column according to the Scott–Knott test at 5% probability.
Table 2
Amount of N in cattle urine and dung used as soil treatment of the two experimental periods of the rainy season and one in dry season, and respective percentages of added
N lost as volatilized NH3 .
Treatment
Urine
Dung
*
Amount of N in applied excreta (g N chamber−1 )
Volatilized N–NH3 (%)
Rainy season
Nov/09
Jan/10
Dry season
Jul/10
Rainy season
Nov/09
Jan/10
Mean
Dry season
Jul/10
10.1
4.1
6.4
4.2
9.5
4.5
30.4a*
2.3b
16.8a
2.6b
23.6
2.5
20.8a
4.3b
Mean N data followed by a same letter did not differ in the column according to the Scott–Knott test at 5% probability.
was responsible for another 10.9% of the recovered N. The existing litter contained
only 0.6% of the urine-N, and shoot and litter of plants around the chamber contained
4.2% of this N.
The upper soil layer (0–10 cm) retained 23.0% of the urine-N, almost 72% of the N
recovered from the soil profile of 40 cm depth. The urine-N recovered in the 10–20,
20–30 and 30–40 cm layers were, respectively, 4.5%, 2.8% and 1.8% of the total added
to the pasture.
Fig. 3. Nitrous oxide (A) fluxes from cattle urine and dung patches artificially
deposited on a Brachiaria pasture on an Oxisol of the Cerrado region in Brazil during
the dry season. Rainfall (bras) and water filled pore space (WFPS—symbols) data
during the same period (B) are presented along with soil NH4 + (C) and NO3 − (D)
availability. Bars are standard error of mean.
4. Discussion
The preliminary study on the linearity of emission of N2 O from
the static chambers indicated that rates remained constant up to
50 min which justified our use of just two sampling times over a
period of 30 min used throughout this study. The chambers were
all within a radius of 5 m where ammonium sulphate had been
uniformly distributed, but there was more than a three-fold difference in emissions rates. These results indicate our chamber system
Fig. 4. Ammonia volatilization from cattle urine and dung patches artificially
deposited on a Brachiaria pasture on an Oxisol of the Cerrado region in Brazil during
two 21-day periods in the rainy season (A and B) and one in the dry season (C). Bars
are standard error of mean.
A.C.R. Lessa et al. / Agriculture, Ecosystems and Environment 190 (2014) 104–111
Fig. 5. Recuperation of urine-15 N in shoot, litter and roots of a Brachiaria pasture
and from the soil profile to 40 cm depth. Bars are standard error of mean.
was well insulated from external temperature changes and that the
chamber seal of the top to the base, and the depth of insertion of the
base into the soil, were sufficient to avoid gas escaping under the
chamber walls (Conen and Smith, 2000). This suggests that investment in greater replication of sampling, in terms of space and time,
rather than in the number of gas samples taken from each chamber,
was under our conditions the most efficient strategy to optimize the
determination of mean emission rates.
After the application of excreta on pastures, similar patterns of
N2 O fluxes were observed, with increased fluxes during the first 20
days that followed urine and dung, which practically ceased after a
month. This relatively short period of response was also observed
by Galbally et al. (2010) in Australia under more arid climatic conditions and also in colder regions by van Groenigen et al. (2005) in
The Netherlands, and by Flessa et al. (1996) in Germany. The only
study carried out in Brazil, but under a cooler climatic regime than
that of the Cerrado, showed the same patterns of emissions from
dung and urine but emissions continued to be greater than those
of the control (soil without excreta) for 30 to 40 days, which was
attributed to a combination of low temperatures and late rainfall
(Sordi et al., 2013).
Most studies on soil N2 O fluxes from cattle excreta have been
conducted in temperate environments, where soil temperature
is lower and evapotranspiration is considerably slower than in
tropical environments. This implies that the gas sampling periods
adopted in this study were sufficient to cover the effects of the
deposition of excreta on gas fluxes. Data presented in Fig. 2 confirms the decreasing response of soil N2 O fluxes with time from
excreta treatments to rainfall events, which was more evident in
the second experimental period.
The combination of high soil mineral N availability and high
WFPS is considered to be a trigger for the induction of soil N2 O
fluxes (Smith et al., 2003), provided no other major limiting factor
operates on the system. This is the most direct explanation for the
steep increase in soil N2 O emission after urine application onto soil
observed during the rainy season in the present study (Fig. 2A and
B). Cattle urine N is constituted mainly of urea (∼70–90%—Bristow
et al., 1992; Kool et al., 2006) that is usually rapidly hydrolysed
by soil urease, which explains the increased concentrations of soil
NH4 + shortly after the urine addition (Fig. 2C). Nitrate formation in
the first experimental period where WFPS was frequently over 60%
(Fig. 2B) was not significant (Fig. 2D), which could be explained by
intense denitrification that governed the high N2 O losses in that
case. On the other hand, the second experimental period in the
rainy season presented periods of high nitrate accumulation under
the urine treatment when WFPS decreased to below 60%, coinciding
with reduced N2 O fluxes.
109
Dung pats cover the soil and hence reduce evaporation losses.
This effect was noticeable especially in the first experimental period
of the rainy season (Fig. 2B). It is reasonable to assume that if dung
is deposited by cattle on areas of high soil mineral N content, for
example urine-affected areas, this could increase N2 O emissions,
as was observed by van Groenigen et al. (2005).
While urine was a massive inducer of soil N2 O emissions during
the rainy season, the presence of dung resulted in emissions of one
or two orders of magnitude lower than those registered with urine
application, even though the N present in the dung was between
40% and 64% of that in urine (Table 1). These results are in agreement with those found by Flessa et al. (1996) where the fraction
of N lost as N2 O from urine was almost 10 times greater than that
from dung. In the case of Sordi et al. (2013), the results of the study
carried out in Southern Brazil are in agreement with our findings
but the magnitude of differences were smaller, principally because
of the relatively lower emissions from cattle urine. Only a relatively
small fraction of the N in dung is in a labile condition, and this is
affected by animal diet (Lovell and Jarvis, 1996). As reported by
van Vliet et al. (2007) the dung produced by animals on a highfibre, low-protein diet had lower concentrations of both organic
and inorganic N than that of animals on a low-fibre, high-protein
diet. In the case of the animals fed on extensive pasture systems
where liming and fertilization are rarely practiced, there is a trend
of increased recalcitrance of the dung and a decrease in N content of
the excreted dung and urine. The low N contents in urine and dung
used in this study can be considered as representative of those in
the excretions deposited in the extensive grazing systems of most
of Brazil.
During the dry season, the application of urine or dung did not
induce significant soil N2 O fluxes. Only after an artificial rainfall of
25 mm, almost 30 days after urine application, were N2 O fluxes registered, but then at a relatively low intensity (Fig. 3). Under dry soil
conditions (WFPS ∼20%—Fig. 3B) urea hydrolysis slows down and
the NH3 formed is continuously, though not intensely, lost through
volatilization (Sommer and Hutchings, 2001). After the first 8 mm
of applied rainfall, NH4 + increased not only in the soil receiving
urine and dung but also in the control treatment, indicating water
dramatically limited soil microbial activity. The following artificial
rainfall of 20 mm two days later increased WFPS to the point where
N2 O emissions were only marginally induced, only in the urine
treatment, which was not enough to bring about an emission factor
much different from zero (Table 1).
Apart from differences in N content as a function of excreta type
and period (Table 1), large differences in N2 O emissions between
seasons were evident. The calculated emission factor for urine was
significantly greater than that for dung, except in the case of the
dry season when both fluxes were almost zero. Considering the
results obtained in this study, a direct N2 O emission factor (EF) for
the rainy season would be 0.02 g N g−1 urine (2%) on average, which
matches the IPCC EF3PRP used for cattle excreta. However, this factor would not apply to the dry season, as a specific EF was too low to
be estimated. In the case of N excreted in dung the presented data
indicates an EF of 0.001 g N g−1 for the rainy season and practically
zero for the dry season as for urine. These results were considerably
different to those obtained by Sordi et al. (2013) working in southern Brazil. They found emissions from urine almost one eighth of
those registered in this present study, but for dung their emissions
were somewhat higher. The wetter and warmer conditions in the
Cerrado region during the rainy season could explain the higher
N2 O fluxes in our study (Uchida et al., 2011). For dung, the difference in the results between the two studies was not so great, with
the exception of the dry season N2 O emissions in our experiment
when they were almost undetectable for both urine and dung.
Differences in N lost by NH3 volatilization between the rainy
and dry seasons were only detected for dung, although in both
110
A.C.R. Lessa et al. / Agriculture, Ecosystems and Environment 190 (2014) 104–111
cases losses were low (2.5% and 4.3%, respectively). During the
rainy season NH3 losses from excreta were restricted to the first
6 to 10 days after deposition (Fig. 4A and B). This pattern was also
observed in several investigations realized in diverse environments
using different techniques (Lockyer and Whitehead, 1990; Petersen
et al., 1998; Saarijärvi et al., 2006; Mulvaney et al., 2008). However, the magnitude of losses varied enormously especially when
urine was the N source under evaluation. In this study, our estimate
of losses varied from 30% of the added N in the first experiment
in the rainy season to 17% in the second experiment (Table 2),
which are within the large range of NH3 –N losses from urine
(Lockyer and Whitehead, 1990; Petersen et al., 1998; Saarijärvi
et al., 2006; Mulvaney et al., 2008). Losses from dung were much
smaller (almost negligible) which is in accordance with previous
research (e.g. Petersen et al., 1998; Mulvaney et al., 2008). During
the dry season, NH3 losses were not so intense in the first days after
the application of excreta, but they persisted for a longer period;
losses from urine being greater than for dung. The absolute magnitude of the estimates of the losses of N through NH3 volatilization
should be treated with some caution as the factor determined by
Araujo et al. (2009) may vary somewhat with different conditions
of temperature, soil moisture, pH and wind speed.
Nitrogen in dung is in part recalcitrant, which would be one of
the explanations for the lower percentage of N losses compared to
that in urine. Moreover, a crust can be formed on dung (Petersen
et al., 1998), which can act as a physical barrier with chemical and
biological implications hindering NH3 formation as discussed by
Mulvaney et al. (2008).
The fraction of added N volatilized from urine was not different in the dry season compared to the rainy season and NH3 loss
was approximately five-times greater for urine compared to dung
(Table 2). Whether these results showing similar NH3 losses in
the wet and dry seasons can be generalized is not clear, especially in view of the considerable number of edaphoclimatic factors
which may affect this loss mechanism (Sommer and Hutchings,
2001).
Even though volatilization losses during the rainy season were
adequately monitored (Jantalia et al., 2012), the denitrification
process could not be fully accounted as only N2 O was measured.
However, the use of 15 N-labelled urine in the first experiment
revealed almost 65% of the added N remained in the system, half
in the above- and below-ground plant material and half in the soil,
mostly in the first 10 cm (Fig. 5). If the estimate of 30% of the added
N lost as NH3 is accepted, the remaining 5% would be accounted
for by non-N2 O denitrification losses and nitrate leaching. The root
system of Brachiaria was abundant and accumulated near half of
the N recovered in shoots and litter (data not shown). Soils of the
Cerrado region are usually N limited which brings about increased
rooting density (Oliveira et al., 2004) contributing to the increased
soil- and excreta-N uptake.
5. Conclusion
Data on N losses from cattle excreta are rare in Brazil despite the
large impact of N2 O emissions by cattle on national inventory of
greenhouse gases. Our results showed, that for the Cerrado region,
the fraction of the N lost as N2 O was approximately 0.012 g N g−1 N
in urine and 0.001 g N g−1 N in dung, considering a rainy season of
7 months duration in this region (Bustamante et al., 2012b). Under
conditions of extensive grazing, rarely more than 60% of the N is
excreted as urine so that the weighted emission factor for the whole
year would be around 0.007 g N g−1 excreted N, which is at the
lower end of the uncertainty range used by the Intergovernmental
Panel on Climate Change (IPCC) (2006), but well below the central
value of 0.02 g N g−1 excreted N.
In relation to volatilized NH3 the results also suggest much lower
losses from dung, amounting to a mean of 2.5% of total N in the rainy
season and 4.3% in the dry season. So although losses of NH3 –N from
urine were considerably greater (22% of added N, considering the 7
months of rainfall per year) than would be expected from the IPCC
Tier 1 estimate (FracGASM = 20% added N), on average adding losses
from dung and urine (14.8% assuming 60% excreted N goes through
urine) the IPCC value seems to be adequate.
For the rainy season in the Cerrado region, NH3 volatilization
and denitrification are the most important processes of N losses
from cattle excreta, which should also be true for the dry season
when NO3 − leaching/run-off losses are not to be expected.
Even though dairy cow excreta is more enriched in N than that
of beef cattle, and for this reason more liable to N losses, the results
obtained indicate that an annual excretion by cattle (beef and dairy,
respectively) of 40 to 70 kg N head−1 would imply an emission of
0.59 to 1.03 kg N2 O head−1 yr−1 , assuming 1% of volatilized N is lost
as N2 O (Intergovernmental Panel on Climate Change (IPCC), 2006)
and no significant leaching/run-off losses occur. Calculations using
IPCC guidelines (including the indirect N2 O emissions) would result
in emissions of 1.52 to 2.67 kg N2 O head−1 yr−1 between two and
three times our estimates.
The results presented here indicate that the emission factor for
urine N cannot be considered the same as for dung, as has been
adopted for the Tier 1 of IPCC guidelines. This disaggregation was
also suggested by van der Weerden et al. (2011) for excreted N by
ruminants in New Zealand, which indicates it has a much wider
purview than a local adjustment.
Acknowledgements
The authors express their gratitude to the team of Embrapa
Arroz e Feijão and Embrapa Agrobiologia for their diligent assistance in the field and for the laboratory analyses. The authors
ACdeRL and DSP gratefully acknowledge the Federal Agency of Support and Evaluation of Postgraduate Education (CAPES) for MSc
Research Fellowships, and the authors RMB, SU and BJRA for “productivity” fellowships from CNPq and from the program “Cientista
de Nosso Estado” of the Rio State Research Foundation (FAPERJ). The
work was funded by Embrapa, CNPq, FAPERJ and the Universidade
Federal Rural do Rio de Janeiro.
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