GLOBAL BIOGEOCHEMICAL CYCLES, VOL. 18, GB1045, doi:10.1029/2003GB002175, 2004
Nitrous oxide emissions from temperate grassland ecosystems
in the Northern and Southern Hemispheres
Christoph Müller
Department of Plant Ecology, University Giessen, Giessen, Germany
Robert R. Sherlock
Soil, Plant and Ecological Sciences Division, Soil and Physical Sciences Group, Lincoln University, Canterbury,
New Zealand
Received 14 October 2003; revised 8 January 2004; accepted 2 February 2004; published 25 March 2004.
[1] Nitrogen (N) fertilized or grazed grasslands in temperate regions of the Northern and
Southern Hemisphere are important sources for atmospheric nitrous oxide (N2O).
Following synthetic urine applications in a New Zealand grassland ecosystem, and
ammonium (NH4+) and nitrate (NO3) applications to a German grassland ecosystem,
approximately 31, 16, and 5%, respectively, of the total emitted N2O (N2Otot) was
produced by nitrification (N2Onit) with the rest being produced by denitrification
(N2Oden). Analyses of the combined data set showed that 75% of all N2O emissions
occurred above 60% water filled porosity (WFPS) and that more than 80% of all N2O
emissions occurred at soil temperatures between 10 and 15C. N2Oden emissions were
associated with a WFPS value at around 80% at relatively low NO3 concentrations, while
N2Onit emissions only occurred at high NH4+ levels shortly after N application at soil
temperatures around 10C. To increase the accuracy of predictions with simple
mathematical models, such as the ‘‘hole-in-the-pipe-model,’’ long-term validation data
sets are needed where driving variables are related to measured N2Onit and N2Oden
data.
INDEX TERMS: 0315 Atmospheric Composition and Structure: Biosphere/atmosphere interactions;
4805 Oceanography: Biological and Chemical: Biogeochemical cycles (1615); KEYWORDS: grassland,
nitrous oxide
Citation: Müller, C., and R. R. Sherlock (2004), Nitrous oxide emissions from temperate grassland ecosystems in the Northern and
Southern Hemispheres, Global Biogeochem. Cycles, 18, GB1045, doi:10.1029/2003GB002175.
1. Introduction
[2] Grassland systems comprise approximately 30– 50%
of terrestrial ecosystems in temperate regions of the earth
[Whitehead, 1995]. In this study, N2O emissions and their
relationships to important controlling factors are presented
from temperate grassland systems in the Southern (New
Zealand) and Northern Hemispheres (Germany). While the
area for arable land is very similar in New Zealand and
Germany (approximately 51 and 50% of the total land area
respectively [Statistisches Bundesamt, 1998; Statistics New
Zealand, 2000]), there are large differences in their managements. In New Zealand (NZ) a high proportion of improved
pastures are managed under a grass-clover regime with
intermittent cropping to restore soil structural, biological,
and nitrogen fertility, which degrades under continuous
arable production. In NZ, such grassland ecosystems are
grazed throughout the year, mainly by sheep, dairy cows,
and beef cattle, with the urine patches of these animals now
recognized as the major source of NZ’s N2O emissions [de
Klein et al., 2003]. This is because in grazed pastures, large
Copyright 2004 by the American Geophysical Union.
0886-6236/04/2003GB002175$12.00
quantities of N are recycled annually in animal urine (e.g.,
280 kg N ha1) and are deposited on to the soil resulting in
small volumes of soil containing high concentrations of N
(e.g., up to 1000 kg N ha1) [Haynes and Williams, 1992].
In Germany, approximately 30% of the arable land is
managed as permanent grassland without intermittent cropping [Statistisches Bundesamt, 1998]. The grassland ecosystems receive a moderate N fertilization (approximately
50– 100 kg N ha1 yr1) and may partly be grazed. In
contrast, only high-intensity dairy pastures in NZ receive
supplementary N fertilization of this order, with the bulk of
NZ’s pastureland receiving little, if any, fertilizer-N [de
Klein et al., 2001].
[3] Nitrous oxide (N2O) qualifies as a greenhouse gas
with a lifetime of 120 years and a global warming potential
over a 100-year timeframe of 310 times that of CO2
[Intergovernmental Panel on Climate Change (IPCC),
1996]. Nitrous oxide is also involved in the catalytic
depletion of stratospheric ozone [Crutzen, 1970]. Nitrous
oxide emissions mainly result from microbiological processes in soil principally via autotrophic nitrification and
heterotrophic denitrification [Ambus, 1998]. Key factors
which influence N2O emissions from soil are its aeration
status, which is inversely related to the soil moisture and
GB1045
1 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
precipitation, the soil temperature, and the available mineral
N (ammonium, NH4+; nitrate, NO3, nitrite, NO2) [Conrad et
al., 1983; Granli and Bøckman, 1994; Wrage et al., 2001].
Additional factors influencing N2O emissions are easily
metabolizable carbon [Burford and Bremner, 1975] and soil
pH [Nägele and Conrad, 1990]. However, it is not a single
factor but the interaction between several factors which
ultimately controls N2O emissions from soil [Wrage et al.,
2001]. Furthermore, the emissions arising from nitrification
(N2Onit) are driven by combinations of factors which differ
from those responsible for denitrification (N2Oden), due
largely to the different ecological habitats of the various
organisms responsible [Conrad, 1996]. The ‘‘hole-in-thepipe model’’ (HIP) has been proposed to explain N2O
emissions from nitrification and denitrification in relation
to mineral N and water filled porosity (WFPS) [Davidson
and Verchot, 2000]. This conceptual model assumes that
N2O arising from these two processes is related to the N flow
rate and the ‘‘leak’’ from those gross rates. Furthermore, it is
assumed that below and above 60% WFPS, N2O is predominantly produced by nitrification and denitrification, respectively [Bouwman, 1998]. However, so far, only a few studies
with small numbers of observations have determined N2Onit
and N2Oden separately over entire seasons. In addition, N2O
emissions typically increase with increasing soil temperature
displaying an approximate Q10 value of 2 [Whitehead,
1995]. Thus the combined effects of soil moisture with
temperature and mineral N concentrations determine the
temporal variations of N2O across the seasons.
[4] The most commonly used method to separate N2Otot
into N2Onit and N2Oden is to incubate soil in vitro in
acetylene (C2H2) concentrations of 5 – 10 Pa to inhibit just
the nitrification process [Klemedtsson and Hansson, 1990].
This method has so far been applied in experiments on
temperate grasslands with only a few incubations over
entire seasons [Ambus, 1998; Kester et al., 1997; Koops et
al., 1997].
[5] Here, we present total N2O emissions (N2Otot) and
N2O from nitrification (N2Onit) and denitrification (N2Oden)
from annual experiments in both New Zealand and Germany. A range of soil and environmental parameters were
monitored and related to the N2Otot, N2Onit, and N2Oden
emissions to derive general relationships for temperate
grassland ecosystems.
2. Materials and Methods
2.1. Experimental Set Up
2.1.1. New Zealand
[6] A field experiment was carried out near Lincoln,
Canterbury, New Zealand (172300E, 43380S). The site
was sown in a ryegrass (Lolium perenne) and white clover
(Trifolium repens) pasture 4 years prior to the initiation of
the experiment. The soil is classified as Templeton silt loam
whose top 5 cm has a sand, silt, and clay content of 59, 21,
and 19% respectively; organic C of 3.3%, pH (H2O) of 6.0,
and dry bulk density of 1.14 g cm3.
[7] The experiment was a randomized block design with
four replicates. Single urination events were applied on
days 1, 114, 184, and 281 days after the start of the
experiment on different plots.
GB1045
[8] Synthetic urine was applied, comparable to sheep
urination events, at a rate of 4.073 L m2. The composition
of the synthetic urine was the same as that employed by
Fraser et al. [1994] and gave individual elemental application rates equivalent to N: 500, K: 400, Cl: 100, and S:
15 kg ha1, respectively. The circular gas measuring plots
had a size of 0.0491 m2. To avoid artifacts due to soil
disturbance, plots were divided into gas and soil sampling
areas. All soil analyses were performed on the top 5 cm.
2.1.2. Germany
[9] The experiments were carried out at the semi-natural
grassland site at the Environmental Monitoring and Climate
Impact Station Linden located at 50320N and 841.30E near
Giessen, Germany [Jäger et al., 2003]. The grassland had
not been ploughed for the last 100 years and had been
fertilized at a rate of 50– 80 kg N ha1 yr1. The vegetation
consisted of an Arrhenaterum elatoris Br.Bl. Filipendula
ulmaria sub-community and was dominated by 12 grass
species, 2 legumes, and 15 other dicotyledon species. The
soil, a stagno-fluvic gleysol on loamy-sandy sediments over
gley (FAO), has an Ap horizon (0 – 12 cm) with a sand, silt,
and clay content of approximately 10, 58, and 32%, respectively, a pH(H2O) of 6.2, total organic carbon content of
6.6%, and dry bulk density of 0.85 g cm3. A full description
of the German site is given by Jäger et al. [2003].
[10] To investigate the effect of various N forms on N2O
emissions, three treatments were installed: control, NH4+
fertilized, and NO3 fertilized (2 repetitions per plot), each at
a rate of 100 kg N ha1 (using NH4Cl or KNO3). The
fertilizer was applied in liquid form (10 mm) on days 1 and
74 after the start of the experiment on the same plots. The
square-shaped gas measurement plots had a size of 0.16 m2.
2.2. N2O Flux Measurements
[11] Vented and insulated closed chambers designed
according to Hutchinson and Mosier [1981] were used in
both experiments. The cover period was typically 20 min
with headspace samples extracted with 60-mL polypropylene syringes via needles through a rubber septum in the
chamber top at 0, 10, and 20 min after coverage.
[12] Gas samples were analyzed within 24 hours on gas
chromatographs (Varian Aerograph Series 2800 in NZ;
Perkin Elmer Autosystem XL B5902 in Germany) equipped
with 63Ni electron capture detectors (Pye Unicam) and two
manual switching valves (Valco Instruments Co., Inc.)
[Mosier and Mack, 1980]. Integration of the gas chromatograph output was performed on a computer fitted with an
analogue-to-digital interface board running Peaksimple software (SRI Instruments).
[13] Nitrous oxide fluxes were calculated using the nonlinear equation given by Hutchinson and Mosier [1981] and
expressed in g N2O-N ha1 d1. For a cover period of
20 min the method was capable of resolving the N2O flux to
a precision of ±0.2 g N2O-N ha1 d1. Gas samples in New
Zealand were collected daily at 1400 hours except during
periods when the emissions were below 2 g N2O-N ha1 d1.
Low emissions typically occurred during prolonged
periods of no rainfall during which samples were collected
every 3 to 5 days. For control plots, samples were taken
every 1 to 2 days for the first 4 weeks of the experiment.
2 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
However, the sampling frequency was reduced to once a
fortnight and periods following rainfall after finding that the
emissions were consistently low and showed little response
to changing soil and environmental conditions. In Germany,
samples were collected at 5 times throughout each sampling
day (800, 1200, 1400, 1600, 2000 hours) on day 2, 5, 8, 10,
19, 24, 34, 69, 74, 79, 86, 95, 109, 151 after the start of the
experiment. From the five measurements, one integrated
daily N2O flux was calculated assuming a linear change
from one sampling time to the next.
2.3. Determination of N2O via Nitrification and
Denitrification
[14] Total N2O emissions were separated into N2O emissions from nitrification (N2Onit) and denitrification (N2Oden)
based on the inhibition of nitrification by 5 – 10 Pa acetylene
using separate soil core incubations in the field [Müller et
al., 1998]. For the data set in New Zealand a separate
experiment was used to derive relationships between N2Onit,
N2Oden, and soil moisture, soil temperature, NO3, and NH4+
which were then applied to the data set where only total
N2O (N2Otot) was determined [Müller et al., 1998]. In
Germany, at each sampling day, soil cores from the experimental plots were incubated with and without 5 –10 Pa
acetylene in the field under the prevailing environmental
conditions according to the procedure described by Müller
et al. [1998]. Briefly, soil cores (each D = 2.5 cm; H = 5 cm)
were taken from an area adjacent to the N2Otot flux site and
incubated in glass jars under field conditions for approximately 5 hours. There were control jars and jars where the
headspace concentration was adjusted to approximately
10 Pa acetylene (C2H2) [Müller et al., 1998]. From the soil
incubations, ratios of N2Onit/N2Otot and N2Oden/N2Otot were
derived and multiplied by N2Otot from the flux measurement to obtain the separate N2Onit and N2Oden fluxes.
Therefore each daily N2Otot flux was partitioned into N2Onit
and N2Oden flux, assuming that other N2O production
processes were negligible. This procedure is different than
the commonly used method where only laboratory incubations and no additional N2Otot flux measurements are
conducted [Ambus, 1998; Kester et al., 1997]. To obtain
yearly sums of N2Onit and N2Oden, the daily observations
were time-integrated over the observation period.
2.4. Soil Moisture
[15] The soil water content was determined gravimetrically at each time of gas analysis from the top 5 cm in New
Zealand and Germany. The soil moisture was converted to
water-filled pore space (WFPS) using bulk density and
porosity values.
2.5. Mineral Nitrogen (NH4+ ; NO3 )
[16] Soil samples from N applied areas in the two experiments were collected 1, 2, 3, 5, 7, and 10 days after N
application and then at 5- to 20-day intervals. The soil
inorganic N content was extracted immediately after sampling with 2 M KCl and analyzed colorimetrically on an
autoanalyzer (Tector Flow Injection Analyzer in NZ; Technicon continuous flow Analyzer, Braan and Luebbe in
Germany).
GB1045
Table 1. Maximum Coefficient of Variance CV (%) of Total N2O
Emissions, NH4+, and NO3 Concentrations of the New Zealand
(NZ) and the German (DE) Data Set (NH4+ Plots and NO3 Plots)
NZ data (urine plots)
DE data NH+4 plots
DE data NO
3 plots
N2Otot
NH+4
NO
3
113
79
100
17
45
55
26
64
60
2.6. Meteorological Measurements
[17] In New Zealand, soil temperatures from 2, 4, 8, and
16 cm soil depth were measured with thermistors (Campbell, Inc.) and logged at 30-min intervals throughout the
experiment on a data logger (21 X, Campbell, Inc.). Rainfall
was collected in a rain gauge (Nylex) and recorded every
day at 1400 hours. In Germany a full set of meteorological
data including soil temperatures and volumetric water contents from the top 15 cm of soil were recorded and stored as
half hourly averages [Grünhage et al., 2000].
2.7. Calculations and Statistical Analysis
[18] Nitrous oxide emissions are presented as log transformed averages (NZ) or arithmetic averages (Germany).
The lognormal transformation was used on the NZ data after
inspection showed that most of the time one particular plot
was consistently higher than the rest. For the German data
with two replications, such a procedure could not be
justified and arithmetic means were calculated. Past experience with the German permanent grassland site showed
that N2O emissions were less spatially variable than in the
New Zealand field site, thereby allowing a reduction in the
numbers of replicates and the use of an arithmetic mean
calculation. The values are presented in the graphs as area
plots. Coefficients of variation (%CV) in daily N2O fluxes
and soil NH4+ and NO3 concentrations were determined for
each sampling occasion. The highest individual daily %CV
values observed are shown in Table 1.
[19] In a final step the two data sets were combined in
order to derive general relationships for N2Otot, N2Onit, and
N2Oden with soil moisture, soil temperature, and mineral N
(NH4+ and NO3). Combining data sets in such a way is a
common practice to analyze the driving variables for the
observed N 2 O tot emissions [Bouwman et al., 2002a,
2002b].These relationships are presented in 3D graphs after
transforming the data with the 3D smoothing tool of
SigmaPlot (version 8.02, SPSS Inc.). This procedure gives
an equal weight to each individual observation and interpolates between observations. Therefore the aim of this
procedure was not to calculate exact N2O emissions for
each factor combination but rather to show the underlying
relationships with the driving variables.
3. Results
3.1. N2Otot, N2Onit, and N2Oden Emissions
3.1.1. New Zealand
[20] On an annual basis, N2O emissions from urineaffected pasture soil were 1.5 (first) to 7 times (second
application) higher (P < 0.05) than N2O emissions from
nontreated control plots. The N2O emissions from the
3 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
GB1045
control plots were always below 1.9 and on average 0.7 g
N2O-N ha1 d1. Average daily N2O emissions over the
entire sampling period of the four N applications were
11.8 N2O-N ha1 d1 corresponding to a total loss of
approximately 0.23% of the applied N (500 kg N ha1),
indicating that although urine patches are major sources of
N2O emissions, the relative amounts lost are quite small.
Subsequent experiments using real urine on the same soil
and pasture type across three different seasons showed
similar total N2O losses (R. R. Sherlock, unpublished data,
2003). The maximum (Table 1) and average %CV for total
N2O emissions were 113 and 41%, respectively. Over the
entire experiment, on average, 31% of the total N2O flux
was due to nitrification and, by difference, 69% was
therefore due to denitrification (Figure 1). Highest N2Onit
fractions were observed shortly after synthetic urine application when NH4+ concentrations were high (Figure 1). By
50 days after synthetic urine application, when most of the
applied NH4+ had been consumed, N2O was almost exclusively produced by NO3 reduction.
3.1.2. Germany
[21] Highest N2O emissions were recorded shortly after N
fertilizer application (Figures 2a and 2b) with peak values of
approximately 50 g N2O-N ha1 d1 (Figure 2). N2O
emissions from NH4+ and NO3 treated plots were on
average 11.8 and 12.3 times higher than the emissions from
nontreated plots (P < 0.05). The average emission from
control plots was 0.8 g N2O-N ha1 d1. Background
emissions were reached approximately 60 days after N
application (Figure 2). The measured N2Otot values for the
NH4+ and NO3 plots had maximum %CV values of 79 and
100%, respectively (Table 1). In the NH4+ treatment the
N2Onit and N2Oden amounted on average to 16 and 84%,
while in the NO3 treatment they were 5 and 95% of the
total N2O emissions, respectively (Figure 2).
Figure 1. Nitrous oxide emission via nitrification (N2Onit)
and denitrification (N2Oden) (the total nitrous oxide
emission (N2Otot) is the sum of the two areas N2Onit +
N2Oden), mineral N (NH4+ and NO3) concentrations and
water-filled porosities (WFPS), and precipitation and soil
temperature from a temperate grassland system in New
Zealand over an entire year (arrows indicate times of N
applications).
3.2. Soil NH4+ and NO3 Concentration
3.2.1. New Zealand
[22] Highest N2O emissions were observed shortly after N
application (Figure 1) showing that inorganic N substantially elevates N2O emissions. In urine patches, applied N
was mainly in the form of urea which hydrolyzed rapidly
to NH4+, yielding concentrations of approximately 500 mg
NH4+-N g1 (Figure 1). The N treated plots showed higher
NH4+ and NO3 than the control treatment (P < 0.05) for
approximately 60– 100 days after N applications (Figure 1).
The highest %CV values were 17 and 26% for NH4+ and
NO3 concentrations, respectively (Table 1). Once nitrification began, soil nitrate concentrations increased to approximately 150 mg NO3-N g1 at 20 – 50 days after each
synthetic urine application (Figure 1).
3.2.2. Germany
[23] Highest N2O emissions were observed within 25 days
after NH4+ and NO3 application (Figures 2a and 2b). In the
NH4+ treatment the soil NH4+ concentrations peaked at 70 and
120 mg N g1 following the two applications while NO3
concentrations peaked in the NO3 treatments at approximately 120 and 200 mg N g1. Mineral N concentrations
declined to background concentrations (P > 0.05) within
40 days after N application (Figure 2). The highest %CV for
4 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
GB1045
Figure 2. Nitrous oxide emission via nitrification (N2Onit) and denitrification (N2Oden) (the total nitrous
oxide emission (N2Otot) is the sum of the two areas N2Onit + N2Oden), mineral N (NH4+ and NO3)
concentrations, water-filled porosities (WFPS), and precipitation and soil temperature from a temperate
grassland system in Germany. (a) NH4+ fertilized. (b) NO3 fertilized. (Arrows indicate times of N
applications).
NH4+ and NO3 concentrations in the two N treatments
ranged between 45 and 64% (Table 1).
3.3. Soil Moisture
3.3.1. New Zealand
[24] Rainfall events of 15.9 mm and 46.5 mm on day 20
and day 155 (40 days after the second N application) caused
sudden increases in WFPS (Figure 1) and stimulated N2O
emission peaks separate from the first N-fertilizer related
N2O peak (Figure 1). However, high rainfall events approximately 10 weeks after the fourth urine application (Figure 1)
did not lead to emissions as high as those earlier in the
season, showing that soil moisture status is an important
factor for N2O emission but cannot be used as the sole
predictor of high N2O emissions. Overall, 85% of the total
N2O emissions from the N-treated grassland in New Zealand were observed at WFPS values above 50%.
3.3.2. Germany
[25] The precipitation intensity at the German field site
was more evenly distributed (Figure 2) than in the New
Zealand experiment. Therefore N2O emissions related to
sudden soil moisture increases were not as prominent as in
5 of 11
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
GB1045
Table 2. Percentages of N2Otot, N2Onit, and N2Oden Emitted at
Various Soil Temperatures in the New Zealand (NZ) and German
(DE) Grassland Ecosystem
N2Otot
N2Onit
N2Oden
Ecosystem
<5C
5 – 15C
>15C
NZ
DE
NZ
DE
NZ
DE
10
6
13
6
9
6
81
92
84
84
79
93
9
2
3
10
12
1
New Zealand. The WFPS was on average 62%, with 66% of
all N2O emitted at WFPS higher than 50% (Figure 2).
[26] In the combined data set (see later), 75% of all N2O
emissions occurred above 60% WFPS. Of these N2O
emissions, 37 and 63% were produced by nitrification and
denitrification, respectively.
3.4. Soil Temperature
[27] In both agricultural ecosystems the soil temperatures
in the top 5 cm did not exceed 20C (Figures 1 and 2).
Highest N2O emissions were observed after the fourth urine
application in New Zealand (Figure 1) and the second N
fertilization in Germany (Figure 2) at times when soil
temperatures had increased to about 15C. The percentages
of N2Otot, N2Onit, and N2Oden emitted at soil temperatures
below 5C, 5 – 15C, and above 15C are presented in
Table 2. More than 80% of N2Otot, N2Onit, and N2Oden
emissions occurred at times when the soil temperature was
between 5 and 15C (Table 2) with only small N2O
emissions during other times.
GB1045
applications, will stimulate the processes for N2O production. Fertilizer applications of 450 kg N ha1 as urea have
resulted in small but significant N2O emissions similar in
magnitude to the observed N loss via N2O in the current
New Zealand study [Mosier and Hutchinson, 1981; Parton
et al., 1988]. Furthermore, the observed N-induced N2O
loss from the German field site is within the range of the
N2O losses observed from similar managed grassland systems [Bouwman et al., 2002a]. Coefficients of variations
(CV) (Table 1) for N2O emissions are in the range of CVs
reported for N fertilized grasslands (CVs quoted are from 5
to 225%) [de Klein, 1994; Kester et al., 1997; Ruz-Jerez et
al., 1994]). Measurements from areas which have received
known nitrogen applications and unfertilized areas generally
show lowest spatial variability [Denmead et al., 1979]. The
N-induced N2O emissions lasted in the two studies for
approximately 30– 60 days, which is in the range of the
reported 5 – 8 weeks of fertilizer-induced N2O emissions
[Bouwman et al., 2002a; Granli and Bøckman, 1994]. The
3.5. Factor Combinations of the Combined Data Set
[28] Figures 3 – 6 present relationships of two factors on
N2O emission visualized in three-dimensional plots for the
entire data set. The figures are divided into two parts: Part a
shows the height of the N2O emissions as related to the
factor combinations while part b shows a view from above
to better visualize the exact relationships of the two factors
on N2O emissions.
[29] Almost all N2O emissions in the two agricultural
ecosystems occurred at WFPS above 60% and soil temperatures between 5 – 15C (Figure 3). Furthermore, high N2O
emissions occurred over the entire mineral N range provided
that WFPS was higher than 60% (Figure 4). Figure 5
investigates in more detail the relationship of WFPS in
combination with NO3 on N2Oden. Highest values occur
at around 80% WFPS and moderate NO3 concentrations
(50 mg N g1) (Figure 5). Highest N2Onit emissions
occur between 5 and 10C at high NH4+ concentrations
(400 mg N g1) (Figure 6). At lower NH4+ concentrations,
N2Onit emission rates were negligible.
4. Discussion
4.1. Nitrous Oxide Emissions and Their Relationship
to Mineral N
[30] N2O emissions from terrestrial ecosystems predominantly originate from the oxidation of NH4+ and reduction of
NO3. Therefore an NH4+-forming fertilizer such as urea
which undergoes nitrification, or direct NH4+ or NO
3
Figure 3. Relationship of WFPS and soil temperature on
N2Otot emissions (combined New Zealand and German data
set). (a) View from the side. (b) View from above. See color
version of this figure in the HTML.
6 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
GB1045
ratios which were then multiplied by independent N2Otot
emission measurements to obtain N2Onit and N2Oden. We
believe this procedure produced more realistic results than
the usual procedure in which the resulting flux, determined
solely by incubation, is not scaled by actual N2Otot emission
measurements. Incubations often suffer from problems due
to high spatial variability and artifacts during the incubation
period [Kester et al., 1997; Koops et al., 1997; Müller et al.,
1998]. For example, in field incubations it is important to
use intact soil cores rather than homogenized soil to keep
the internal structure intact [Kester et al., 1997; Müller et
al., 1998]. Furthermore, the diffusion of acetylene to the
sites where N2O is produced is inversely related to the soil
moisture status. Best results are obtained at soil moistures
below field capacity [Ryden and Dawson, 1982]. Diffusion
constraints in poorly drained heavy textured soils with a
high WFPS are usually overcome by the soil core technique
where only short diffusion pathways are present [Ryden et
al., 1987]. Most studies which report N2Onit and N2Oden via
the acetylene method have been carried out only for a few
Figure 4. Relationship of WFPS and mineral N on N2Otot
emissions (combined New Zealand and German data set).
(a) View from the side. (b) View from above. See color
version of this figure in the HTML.
application of urine in New Zealand and NH4+ in Germany
resulted in higher and more prolonged N2O emissions
compared to those plots receiving NO3 (Figure 2), which
again is consistent with other observations [Bouwman et al.,
2002a; Clayton et al., 1997]. On the basis of the soil texture
(the NZ grassland soil had a coarser texture), it is surprising
that the New Zealand grassland soil supported higher N2Otot
emissions. However, apart from the soil texture, the age of
the ecosystem is an important indicator for the N2Otot
emission potential. While the grassland in New Zealand
had been ploughed 4 years prior to the onset of the
investigations, the German soil had not been ploughed for
at least 100 years [Jäger et al., 2003]. Old ecosystems are
characterized by a ‘‘tight’’ nutrient cycle and a high capacity
for N retention and do not support high gaseous N losses
[Müller et al., 2002; Stark and Stephen, 1997].
4.2. N2Onit and N2Oden Emissions
[31] The current in-field incubation method was used
exclusively to derive N2Onit/N2Otot and N2Oden/N2Otot
Figure 5. Relationship of WFPS and NO3 on N2Oden
emissions (combined New Zealand and German data set).
(a) View from the side. (b) View from above. See color
version of this figure in the HTML.
7 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
Figure 6. Relationship of soil temperature and NH4+ on
N2Onit emissions (combined New Zealand and German data
set). (a) View from the side. (b) View from above. See color
version of this figure in the HTML.
discrete observations and not over entire seasons as reported
here. Therefore we believe the data reported here to be more
representative of actual N2Onit and N2Oden emissions than
much of the data reported previously.
[32] Approximately 31% of the overall N2O emission
from the New Zealand grassland was produced by nitrification. Highest N2Onit emissions were observed shortly after
urine applications, which is consistent with observations that
N2O emissions closely followed the pattern of nitrification
shortly after urine application [Clough et al., 2003] or after
slurry applications [Merino et al., 2001]. After NH4+ application on the German grassland site the contribution of
nitrification to the overall N2O flux was on average only
16%. This provides evidence that high N2O emissions after
NH4+ application may not be specifically due to nitrification.
Rather, the NH4+ may actually stimulate a bigger and more
active denitrifier population and hence facilitate N2O emissions via denitrification [Azam et al., 2002].
[33] The main driving variable for the division of N2Otot
into N2Onit and N2Oden is considered to be WFPS [Davidson,
GB1045
1991]. Below 60% WFPS nitrification and above 60% WFPS
denitrification are considered to be the predominant N2O
producing processes [Bouwman, 1998]. However, this arbitrary division could not be confirmed with this current data
set in which, at WFPS greater than 60%, 37 and 63% of the
total N2O emissions were produced by nitrification and
denitrification, respectively. Furthermore, the absolute value
of WFPS at which nitrification and denitrification dominate
with respect to N2Otot production are also site specific (i.e.,
they depend on soil texture). In finer grained soils it can be
expected that anaerobic microsites can develop at much
lower WFPS values than in coarser soil [Davidson, 1991].
Shortly after the fourth urine application in the New Zealand
study the predominant process leading to N2O emission was
nitrification while the soil itself was near saturation, a
condition usually known to favor denitrification but not
nitrification [Arah et al., 1991]. This highlights the fact that
nitrification makes a high contribution, or even is the dominant N2O producing process, during high soil moistures.
Even under near-saturated conditions it can still be important,
as observed in several other studies on N fertilized temperate
grassland soil [Ambus, 1998; Clough et al., 2003; Davidson,
1993; Koops et al., 1997; Robertson and Kuenen, 1991].
Nitrous oxide emissions via nitrification are most likely
produced under coinciding aerobic and anaerobic conditions
as a nitrite-reducing side reaction (‘‘nitrifier-denitrification’’)
[Payne, 1991; Wrage et al., 2001]. On the other hand, even
during summer periods under low soil moisture it was found
in a subsequent in-field 15N study on the German grassland
field site that denitrification was the exclusive N2O production process [Müller et al., 2004].
[34] Therefore the conceptual model that N2Onit and
N2Oden can be related to the WFPS of the soil [Bouwman,
1998] may in many instances be incorrect and can lead to
erroneous results because there does not seem to be such a
clear-cut division between WFPS where predominantly
N2Onit or N2Oden occurs. Furthermore, the ‘‘hole-in-thepipe model’’ (HIP) is often used to predict N2O from
nitrification and denitrification assuming that N 2 O nit
and N2Oden are related to the underlying process rates
[Bouwman, 1998]. However, in practice the N2Otot emissions are often related to the mineral N pool sizes and not
gross N transformation rates, which provides only ‘‘broadbrush’’ accuracies for biogeochemical models [Davidson
and Verchot, 2000]. A more accurate prediction requires
knowledge of the gross N transformations of nitrification
and denitrification and the relationships of these N rates to
N2O production under various soil temperature-moisture
conditions [Müller, 2000].
[35] The analysis of N2Oden and N2Onit with closely related
factors, i.e., N2Oden with NO3 and WFPS (Figure 5) and
N2Onit with NH4+ and soil temperature (Figure 6), shows that
more accurate relationships can be derived for the processrelated N2O emissions. These kinds of analyses will also help
to derive more accurate functions for model developments.
4.3. Soil Moisture-Precipitation
[36] There is a general trend that N2O emissions do
increase with soil moisture, in particular above 60% WFPS,
over the entire mineral N range (Figure 4) [Clayton et al.,
8 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
1997; Dendooven and Anderson, 1994; Dendooven et al.,
1994]. For the combined data set, 75% of the total N2O was
emitted at WFPS >60% WFPS. Above this, soil moisture
level is considered to be the regime where rapidly increasing denitrification promotes the onset of anaerobic conditions and denitrification [Arah et al., 1991]. Transient
increases in WFPS due to large rainfall events stimulate
high N2O emissions even at times when the initial fertilizerinduced N2O emission has subsided (e.g., days 20 and 155
after start of experiment, Figure 1), which again is in line
with other studies on temperate grassland [Tilsner et al.,
2003]. One explanation for large N2O peaks, in particular in
the New Zealand study, after sudden soil moisture changes
may be an imbalance between NO and N2O reductase
promoting transient N2O buildup and release [Cates and
Keeney, 1987].
4.4. Soil Temperature
[37] Highest N2O emissions coincide with times when
both the soil moisture and soil temperature are high
(Figure 3). This is not surprising, since increasing soil
temperature positively influences the rates of both nitrification and denitrification [Goodroad and Keeney, 1984] and
also the N2O emissions [Cates and Keeney, 1987]. The
temperature maximum where the highest N2O emissions
occurred ranged in this study between 10 and 15C
(Table 2). However, this is lower than the maximum N2O
emissions at 20C reported in other studies [Clayton et al.,
1997]. This apparent discrepancy is related to the timing of
fertilizer application. While in the Clayton study [Clayton et
al., 1997] the fertilizer was applied at times of maximum
soil temperature (early and mid-summer), in the study
reported here the fertilizer was applied when the soil
temperature was lower (Figures 1 and 2). Since N availability is one of the most important N2O-driving variables,
the soil temperature at the time of fertilization has to be
considered when deriving temperature relationships. For the
derivation of conceptual N2O production/emission models
it should be stressed that the soil temperature is only a
key variable under conditions when nutrient levels are
adequate and microbial activities are limited by enzyme
rates rather than by the transport of substrate to the
membranes [Conrad, 1996].
[38] Freezing-thawing cycles are not included in the data
because these conditions did not occur in the New Zealand
study and would have influenced the overall relationships.
However, N2O emission during freezing-thawing does occur in the German grassland system and can cause large
N2O emissions [Müller et al., 2003, 2002].
4.5. Overall Relationships
[39] We were able to derive detailed relationships because
of the high sampling frequency with a total of 252 measurements together with accompanying data. This is several
times more than from other experimental data sets on
temperate grassland (e.g., Tilsner et al. [2003] presented
only 50 measurements over 1 year). In other studies
the often only weak relationships are related to the high
CVs associated with the few N2O emission measurements
[Kester et al., 1997; Tilsner et al., 2003]. Furthermore,
GB1045
correlations of N2O emissions with single factors are
usually weak [Davidson and Verchot, 2000]. This highlights
the fact that combinations of factors are required for the
prediction of N2O emissions from soil, which leads to the
development of simple mathematical models [Bouwman et
al., 2002b]. The three most important factors which influence N2O emissions from grassland soils are inorganic N
concentrations, soil moisture, and soil temperature. The
interactions of these factors on N2O emissions are well
documented for temperate grassland [Granli and Bøckman,
1994; Ryden, 1981] and subtropical pasture [Brams et al.,
1990]. This is also demonstrated here for N2Otot and its
relationship to WFPS and soil temperature (Figure 3) and
N 2 O tot and its relationship to WFPS and mineral N
(Figure 4). N transformations, and therefore the buildup of
mineral N (NO3 and NH4+), are related to soil moisture and
soil temperature, and the combination of all three can
promote N2O emissions from soils under pasture [Monaghan
and Barraclough, 1993]. The relationships of N2O emissions
with the underlying variables can be visualized very well
with 3D-Mesh plots (Figures 3 – 6) [Clayton et al., 1997].
This new analysis of process-related N2Oden with WFPS and
NO3 and N2Onit with soil temperature and NH4+ should help
in the development of more accurate relationships for the
prediction of N2O emissions.
[40] A promising new method to analyze the complex
interactions of factors on N2O emissions is the application
of artificial neural networks (ANN). The NZ data set
presented here was included in an ANN study. The ANN
model was able to predict 92% of the variability of N2O
emissions from temperate grassland soil in NZ from relationships with daily rainfall, soil moisture, soil temperature,
soil NH4+, soil NO3, and total mineral N [Ryan et al., 2004].
Furthermore, the NZ data set presented was also used in
a validation study of the DayCent model [Parton et al.,
1998]. DayCent overestimated the measured N 2 O tot
emission by more than three times [Stehfest and Müller,
2004]. The validation study with the detailed data set
highlighted specific areas where DayCent needs to be
further developed.
4.6. Other Factors
[41] Other factors which influence N2O emissions are soil
pH and easily metabolizable carbon [Granli and Bøckman,
1994]. However, no significant correlation between soil pH
and N2O was observed (data not presented). Concentrations
of water soluble carbon were high enough at both field sites
that they did not appear to limit N2O production by
denitrification [Burford and Bremner, 1975]. The lack of
correlation between pH, WSC, and N2Otot is not surprising
because the data were within the published ranges where
they should have no influence on denitrifier or nitrifier
activity [Conrad, 1996]. Plant N uptake may have had a
short-term effect on N2O emissions when the soil inorganic
N pool was small and was therefore not consistent over the
whole year.
5. Conclusions
[42] Detailed measurements of the process-based N2O
emission, N2Onit, and N2Oden, together with the influencing
9 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
variables, enhances the understanding of N2O emissions
from temperate grassland soils. Despite the totally different
management of the grassland sites in the Southern (New
Zealand) and Northern (Germany) Hemispheres, the relationships of the influencing variables to N2Otot, N2Onit, and
N2Oden emissions appear to be uniform. To develop processbased models, relationships of the most important factors
should be based on actual data. In a second step, detailed
studies are required which determine the gross N transformations in soil and the related N2O emission via nitrification and denitrification. These requirements are best met
by 15N-labeling studies [Müller et al., 2004] where not only
the underlying N transformations but also the process related
N2O emissions are determined under field conditions.
[43] Acknowledgments. We thank J. C. G. Ottow for his support
during the experimental period in Giessen. The projects were funded by
Crop and Food, New Zealand, and the German Science Foundation (DFG).
References
Ambus, P. (1998), Nitrous oxide production by denitrification and nitrification in temperate forest, grassland and agricultural soils, Eur. J. Soil Sci.,
49, 495 – 502.
Arah, J. R. M., K. A. Smith, I. J. Crichton, and H. S. Li (1991), Nitrous
oxide production and denitrification in Scottish arable soils, J. Soil Sci.,
42, 351 – 367.
Azam, F., C. Müller, A. Weiske, G. Benckiser, and J. C. G. Ottow (2002),
Nitrification and denitrification as sources of atmospheric nitrous oxide:
Role of oxidizable carbon and applied nitrogen, Biol. Fertil. Soils, 35,
54 – 61.
Bouwman, A. F. (1998), Nitrogen oxides and tropical agriculture, Nature,
392, 866 – 867.
Bouwman, A. F., L. J. M. Boumans, and N. H. Batjes (2002a), Emissions of
N2O and NO from fertilized fields: Summary of available measurement
data, Global Biogeochem. Cycles, 16(4), 1058, doi:10.1029/
2001GB001811.
Bouwman, A. F., L. J. M. Boumans, and N. H. Batjes (2002b), Modeling
global annual N2O and NO emissions from fertilized fields, Global Biogeochem. Cycles, 16(4), 1080, doi:10.1029/2001GB001812.
Brams, E. A., G. L. Hutchinson, W. P. Anthony, and G. P. Livingston
(1990), Seasonal nitrous oxide emissions from an intensively-managed,
humid, subtropical grass pasture, in Soils and the Greenhouse Effect,
edited by A. F. Bouwman, pp. 481 – 487, John Wiley, Hoboken, N. J.
Burford, J. R., and J. M. Bremner (1975), Relationships between the denitrification capacities of soils and total, water-soluble and readily decomposable soil organic matter, Soil Biol. Biochem., 7, 389 – 394.
Cates, R. L., and D. R. Keeney (1987), Nitrous oxide emission from native
and reestablished prairies in southern Wisconsin, Am. Midland Nat.,
117(1), 35 – 42.
Clayton, H., I. P. McTaggart, J. Parker, L. Swan, and K. A. Smith (1997),
Nitrous oxide emissions from fertilised grassland: A 2-year study of the
effects of N fertiliser from and environmental conditions, Biol. Fertil.
Soils, 25, 252 – 260.
Clough, T. J., R. R. Sherlock, M. N. Mautner, D. B. Milligan, P. F. Wilson,
C. G. Freeman, and M. J. McEwan (2003), Emission of nitrogen oxides
and ammonia from varying rates of applied synthetic urine and correlations with soil chemistry, Aust. J. Soil Res., 41, 421 – 438.
Conrad, R. (1996), Soil microorganisms as controllers of atmospheric trace
gases (H2, CO, CH4, N2O, and NO), Microbiol. Rev., 60(4), 609 – 640.
Conrad, R., W. Seiler, and G. Bunse (1983), Factors influencing the loss of
fertilizer nitrogen into the atmosphere as N2O, J. Geophys. Res., 88(C11),
6709 – 6718.
Crutzen, P. J. (1970), The influence of nitrogen oxides on the atmospheric
ozone content, Q. J. R. Meteorol. Soc., 96, 320 – 325.
Davidson, E. A. (1991), Fluxes of nitrous oxide and nitric oxide from
terrestrial ecosystems, in Microbial Production and Consumption of
Greenhouse Gases: Methane, Nitrogen Oxides, and Halomethanes,
edited by J. E. Rogers and W. B. Whitman, pp. 219 – 235, Am. Soc.
for Microbiol., Washington, D. C.
Davidson, E. A. (1993), Soil water content and the ratio of nitrous oxide to
nitric oxide emitted by soil, in Biogeochemistry of Global Change, edited
by R. S. Oremland, pp. 369 – 386, Chapman and Hall, New York.
GB1045
Davidson, E. A., and L. V. Verchot (2000), Testing the hole-in-the-pipe
model of nitric and nitrous oxide emissions from soils using the
TRAGNET database, Global Biogeochem. Cycles, 14(4), 1035 – 1043.
de Klein, C. A. M. (1994), Denitrification in grazed grasslands in
The Netherlands, Ph.D. dissertation, 120 pp., Utrecht Univ., Utrecht,
Netherlands.
de Klein, C. A. M., R. R. Sherlock, K. C. Cameron, and T. J. van der
Weerden (2001), Nitrous oxide emissions from agricultural soils in New
Zealand-A review of current knowledge and directions for future
research, J. R. Soc. N. Z., 31, 543 – 574.
de Klein, C. A. M., L. Barton, R. R. Sherlock, Z. Li, and R. P. Littlejohn
(2003), Estimating a nitrous oxide emission factor for animal urine from
some New Zealand pastoral soils, Aust. J. Soil Res., 41, 381 – 399.
Dendooven, L., and J. M. Anderson (1994), Dynamics of reduction
enzymes involved in the denitrification process in pasture soil, Soil Biol.
Biochem., 26, 1501 – 1506.
Dendooven, L., P. Splatt, J. M. Anderson, and D. Scholefield (1994),
Kinetics of the denitrification process in a soil under permanent pasture,
Soil Biol. Biochem., 26, 361 – 370.
Denmead, O. T., J. R. Freney, and J. R. Simpson (1979), Studies of nitrous
oxide emission from a grass sward, Soil Sci. Soc. Am. J., 43, 726 – 728.
Fraser, P. M., K. C. Cameron, and R. R. Sherlock (1994), Lysimeter study
of the fate of nitrogen in animal urine returns to irrigated pasture, Eur. J.
Soil Sci., 45, 439 – 447.
Goodroad, L. L., and D. R. Keeney (1984), Nitrous oxide production in
aerobic soils under varying pH, temperature and water content, Soil Biol.
Biochem., 16, 39 – 43.
Granli, T., and O. C. Bøckman (1994), Nitrous oxide from agriculture,
Norw. J. Agric. Sci. Suppl., 12, 1 – 128.
Grünhage, L., K. Hanewald, H. J. Jäger, and W. Ott (2000), Auswirkungen
dynamischer Veränderungen der Luftzusammensetzung und des Klimas
auf terrestrische Ökosysteme in Hessen: II. Umweltbeobachtungs- und
Klimafolgenforschungsstation Linden: Jahresbericht 1995, Umweltplanung Arb. Umweltschutz Heft 274, 195 pp., Hessisches Landesamt für
Umwelt und Geol. (HLUG), Wiesbaden, Germany.
Haynes, R. J., and P. H. Williams (1992), Changes in soil solution composition and pH in urine-affected areas of pasture, J. Soil Sci., 43, 323 –
334.
Hutchinson, G. L., and A. R. Mosier (1981), Improved soil cover method
for field measurement of nitrous oxide fluxes, Soil Sci. Soc. Am. J., 45,
311 – 316.
Intergovernmental Panel on Climate Change (IPCC) (1996), Nitrous oxide
and carbon dioxide in agriculture OECD/IPCC/IEA phase II development
of IPCC guidelines for national greenhouse gas inventory methodology,
report, 47 pp., Geneva.
Jäger, H.-J., S. W. Schmidt, C. Kammann, L. Grünhage, C. Müller, and
K. Hanewald (2003), The University of Giessen Free-Air Carbon Dioxide
Enrichment Study: Description of the experimental site and of a new
enrichment system, J. Appl. Bot., 77(6), 117 – 127.
Kester, R. A., M. E. Meijer, A. Libochant, W. de Boer, and H. J. Laanbroek
(1997), Contribution of nitrification and denitrification to the NO and
N2O emissions of an acid forest soil, a river sediment and a fertilized
grassland soil, Soil Biol. Biochem., 29, 1655 – 1664.
Klemedtsson, L., and G. I. Hansson (1990), Methods to separate N2O
produced from denitrification and nitrification, Mitt. Dtsch. Bodenk.
Gesell., 60, 19 – 24.
Koops, J. G., M. L. van Beusichem, and O. Oenema (1997), Nitrous oxide
production, its source and distribution in urine patches on grassland on
peat soil, Plant Soil, 191, 57 – 65.
Merino, P., J. M. Estavillo, G. Besga, M. Pinto, and C. González-Murua
(2001), Nitrification and denitrification derived N2O production from a
grassland soil under application of DCD and Actilith F2, Nutr. Cycl.
Agroecosyst., 60, 9 – 14.
Monaghan, R. M., and D. Barraclough (1993), Nitrous oxide and dinitrogen
emissions from urine-affected soil under controlled conditions, Plant
Soil, 151, 127 – 138.
Mosier, A. R., and G. L. Hutchinson (1981), Nitrous oxide emissions from
cropped fields, J. Environ. Qual., 10(2), 169 – 173.
Mosier, A. R., and L. Mack (1980), Gas chromatographic system for
precise, rapid analysis of nitrous oxide, Soil Sci. Soc. Am. J., 44,
1121 – 1123.
Müller, C. (2000), Modelling Soil-Biosphere Interactions, 342 pp., CAB
Int., Wallingford, UK.
Müller, C., R. R. Sherlock, and P. H. Williams (1998), Field method
to determine N2O emission from nitrification and denitrification, Biol.
Fertil. Soils, 28, 51 – 55.
Müller, C., M. Martin, R. J. Stevens, R. J. Laughlin, C. Kammann, J. C. G.
Ottow, and H.-J. Jäger (2002), Processes leading to N2O emissions in
10 of 11
GB1045
MÜLLER AND SHERLOCK: N2O EMISSIONS FROM GRASSLAND ECOSYSTEMS
grassland soil during freezing and thawing, Soil Biol. Biochem., 34,
1325 – 1331.
Müller, C., C. Kammann, J. C. G. Ottow, and H.-J. Jäger (2003), Nitrous
oxide emission from frozen grassland soil and during thawing periods,
Z. Pflanzenern. Bodenk., 166(1), 46 – 53.
Müller, C., R. J. Stevens, R. J. Laughlin, and H.-J. Jäger (2004), Microbial
processes and the site of N2O production in a temperate grassland soil,
Soil Biol. Biochem., 36, 453 – 461.
Nägele, W., and R. Conrad (1990), Influence of pH on the release of NO
and N2O from fertilized and unfertilized soil, Biol. Fertil. Soils, 10, 139 –
144.
Parton, W. J., A. R. Mosier, and D. S. Schimel (1988), Rates and pathways
of nitrous oxide production in a shortgrass steppe, Biogeochemistry, 6,
45 – 58.
Parton, W. J., M. D. Hartman, D. S. Ojima, and D. S. Schimel (1998),
DAYCENT and its land surface submodel: Description and testing,
Global Planet. Change, 19(1 – 4), 35 – 48.
Payne, W. J. (1991), A review of methods for field measurements of
denitrification, For. Ecol. Manage., 44, 5 – 14.
Robertson, L. A., and J. G. Kuenen (1991), Physiology of nitrifying and
denitrifying bacteria, in Microbial Production and Consumption of
Greenhouse Gases: Methane, Nitrogen Oxides and Halomethanes, edited
by J. E. Rogers and W. B. Whitman, pp. 189 – 199, Am. Soc. for Microbiol., Washington, D. C.
Ruz-Jerez, B. E., R. E. White, and P. R. Ball (1994), Long-term measurement of denitrification in three contrasting pastures grazed by sheep, Soil
Biol. Biochem., 26, 29 – 39.
Ryan, M., C. Müller, H. J. Di, and K. C. Cameron (2004), The use of
Artificial Neural Networks (ANNs) to simulate N2O emissions from a
temperate grassland ecosystem, Ecol. Modell., doi:10.1016/j.ecolmodel.
2003.10.010, in press.
Ryden, J. C. (1981), N2O exchange between a grassland soil and the atmosphere, Nature, 292, 235 – 237.
GB1045
Ryden, J. C., and K. P. Dawson (1982), Evaluation of the acetylene-inhibition technique for the measurement of denitrification in grassland soils,
J. Sci. Food Agric., 33, 1197 – 1206.
Ryden, J. C., J. H. Skinner, and D. J. Nixon (1987), Soil core incubation
system for the field measurement of denitrification using acetylene-inhibition, Soil Biol. Biochem., 19, 753 – 757.
Stark, J. M., and S. C. Stephen (1997), High rates of nitrification and nitrate
turnover in undisturbed coniferous forests, Nature, 385, 61 – 64.
Statistics New Zealand (2000), New Zealand Official Yearbook 2000, Wellington, N. Z.
Statistisches Bundesamt (1998), Statistisches Jahrbuch, Wiesbaden.
Stehfest, E., and C. Müller (2004), Simulation of N2O emissions from
an urine-affected pasture in New Zealand with the ecosystem model
DayCent, J. Geophys. Res., 109, D03109, doi:10.1029/2003JD004261.
Tilsner, J., N. Wrage, J. Lauf, and G. Gebauer (2003), Emission of gaseous
nitrogen oxides from an extensively managed grassland in NE Bavaria
Germany: I. Annual budgets of N2O and NOx emissions, Biogeochemistry, 63, 229 – 247.
Whitehead, D. C. (1995), Grassland Nitrogen, 397 pp., CAB Int., Wallingford, UK.
Wrage, N., G. L. Velthof, M. L. van Beusichem, and O. Oenema (2001),
Role of nitrifier denitrification in the production of nitrous oxide, Soil
Biol. Biochem., 33, 1723 – 1732.
C. Müller, Department of Plant Ecology, University Giessen, HeinrichBuff-Ring 26-32, 35392 Giessen, Germany. (christoph.mueller@bot2.
bio.uni-giessen.de)
R. R. Sherlock, Soil, Plant and Ecological Sciences Division, Soil and
Physical Sciences Group, Lincoln University, P.O. Box 84, Canterbury,
New Zealand.
11 of 11