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Processes regulating nitric oxide emissions
from soils
Kim Pilegaard
rstb.royalsocietypublishing.org
Review
Cite this article: Pilegaard K. 2013 Processes
regulating nitric oxide emissions from soils.
Phil Trans R Soc B 368: 20130126.
http://dx.doi.org/10.1098/rstb.2013.0126
One contribution of 15 to a Discussion Meeting
Issue ‘The global nitrogen cycle in the twentyfirst century’.
Subject Areas:
environmental science, ecology, microbiology
Keywords:
nitric oxide, emission, soil
Author for correspondence:
Kim Pilegaard
e-mail: [email protected]
Department of Chemical and Biochemical Engineering, Technical University of Denmark,
Kgs. Lyngby 2800, Denmark
Nitric oxide (NO) is a reactive gas that plays an important role in atmospheric
chemistry by influencing the production and destruction of ozone and thereby
the oxidizing capacity of the atmosphere. NO also contributes by its oxidation
products to the formation of acid rain. The major sources of NO in the atmosphere are anthropogenic emissions (from combustion of fossil fuels) and
biogenic emission from soils. NO is both produced and consumed in soils as
a result of biotic and abiotic processes. The main processes involved are
microbial nitrification and denitrification, and chemodenitrification. Thus,
the net result is complex and dependent on several factors such as nitrogen
availability, organic matter content, oxygen status, soil moisture, pH and
temperature. This paper reviews recent knowledge on processes forming
NO in soils and the factors controlling its emission to the atmosphere. Schemes
for simulating these processes are described, and the results are discussed with
the purpose of scaling up to global emission.
1. Introduction
Exchange of trace gases between the terrestrial ecosystems and the atmosphere
plays an important role in the regulation of atmospheric composition and climate.
Therefore, there is a growing need for quantification of trace gas exchange and
for mechanistic descriptions that can be used in models for prediction of future
climate changes. Obviously, the greenhouse gases such as CO2, N2O and ozone
(O3) are of prime interest, but also other gases such as volatile organic carbons
and nitrogen oxides (NO and NO2), that are much more reactive in the
atmosphere, are important [1].
Nitrogen oxides are an integral part of the Earth system and are constantly
exchanged between the atmosphere and ecosystems. The nitrogen cycle has a
pronounced effect on ecosystem productivity and affects climate in several
ways. Both nitrous oxide (N2O) and nitric oxide (NO) are emitted from the
soil, and whereas N2O is a strong greenhouse gas by itself, NO acts indirectly
by contributing to the formation of O3, the third largest contributor to positive
radiative forcing [2]. The deposition of N compounds to ecosystems has a fertilizing effect and might stimulate primary production and thus CO2 uptake from
the atmosphere, whereas O3 is phytotoxic and thus will reduce primary production. Davidson & Kingerlee [3] estimated the amount of NO emitted from
soils to the atmosphere globally to be between 13 and 21 Tg N yr – 1, depending
on the strength of the adsorption onto plant canopy surfaces.
NO reacts rapidly with O3 in the atmosphere and creates NO2; the sum of
NO and NO2 is called NOx. The amount of NOx originating from soil emission
is comparable in source strength with the anthropogenically emitted NOx from
the burning of fossil fuels which amounts to 20–24 Tg N yr – 1 [2]. NO emitted
from the soil is a significant contributor to the NOx mixing ratio in the atmosphere, and NO may directly be involved in the production of OH, thus
influencing the oxidizing capacity of the atmosphere [4,5]. The relative role of
soil-emitted NO is highest in areas with the lowest anthropogenic emission,
and in forested areas, a significant amount of the soil-emitted NO might be
captured as NO2 by the canopy [6].
NO emission from soils has been studied in numerous experiments both in the
field and in the laboratory, often together with N2O. The knowledge on rates of
& 2013 The Author(s) Published by the Royal Society. All rights reserved.
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2
NO
NO−3
NH2OH
NO−2
N2O
N2
denitrification
nitrification
NH3
NO
N2O
N2
nitrifier denitrification
Figure 1. Transformations of mineral nitrogen in soil. The boxes for nitrification and nitrifier denitrification overlap, as nitrifier denitrification is a pathway of
nitrification, but separate into the different branches from NO2
2 onwards. Adapted from Wrage et al. [12].
emission is thus quite comprehensive, but the knowledge on the
mechanisms that control the emission still needs improvement
[7–9]. The intention of this paper is to give a short overview of
the current knowledge of NO emission from soils with emphasis on new knowledge gained during recent years.
2. Nitric oxide formation in soil
The production and consumption of NO in soil is a result of
both microbial activity and chemical reactions. Many processes and micro-organisms are involved; the two most
important groups of micro-organisms are nitrifiers and denitrifiers. Generally, both NO and N2O are produced by the
same processes; however, the exact ratios of the two products
are not yet clearly known. Recently, there has been a much
stronger focus on N2O emission from soil rather than on
NO, because N2O is a greenhouse gas by itself, whereas
NO only indirectly contributes to global warming. However,
generally processes producing N2O also produce NO.
The following overview of processes involved in NO production and consumption is mainly based on Conrad [10].
(a) Nitrification
NO and N2O are by-products of nitrification, the oxidation of
ammonium to nitrate. The so-called nitrosobacteria that carry
out the first part of this process require oxygen. The production
mechanism for NO by these bacteria is unknown but might
follow the sequential pathway in equation (2.1) [11]:
NHþ
4 ! NH2 OH ! HNO ! NO "! NO2 :
ð2:1Þ
The nitrobacteria oxidize nitrite to nitrate, using oxygen as
the terminal electron acceptor:
NO
2 ! NO3 :
ð2:2Þ
Under anoxic conditions, these bacteria reduce nitrate to
nitrite and further to NO.
Nitrosobacteria and nitrobacteria are autotrophic. Heterotrophic nitrifiers also exist (both bacteria and fungi); they
produce nitrate by either an inorganic or an organic pathway:
NHþ
4 ! NH2 OH ! NO2 ! NO3 ;
ð2:3Þ
and
R NH2 ! R NHOH ! R NO ! R NO2 ! NO
3:
ð2:4Þ
Many of the heterotrophic nitrifiers seem to denitrify
under aerobic conditions. They might be especially important
as producers of NO and N2O in forest soils.
(b) Denitrification
The process where nitrogen oxides are reduced by microorganism (mainly bacteria but also fungi) to gaseous products is called denitrification. Both NO and N2O are
produced as part of the process that reduces nitrate to the
end product N2:
NO
3 ! NO2 ! NO "! N2 O "! N2 " :
ð2:5Þ
Denitrification can take place both under aerobic and
anaerobic conditions, but it is believed that anaerobic
denitrification is the most important for NO production
in soil.
Wrage et al. [12] described a pathway where the oxidation
2
of NH3 to NO2
2 is followed by the reduction of NO2 to N2O
and N2. They called this pathway nitrifier denitrification
(figure 1). The process is carried out by autotrophic NH3oxidizers. Only nitrifiers carry out nitrifier denitrification,
whereas both nitrifiers and denitrifiers are involved in
coupled nitrification–denitrification. The quantitative importance of the nitrifier denitrification pathway is not yet certain,
but Wrage et al. [12] estimate that it can be an important
source of N2O (and NO) under certain circumstances, i.e.
high N content, low organic C content, low O2 pressure
and maybe also low pH. Isotope tracing has shown that the
process can actually occur in soils, and may in fact be responsible for the greater proportion of total nitrifier-induced N2O
production [13]. Recently, Kool et al. [14] studied a poor
sandy soil and found that nitrifier denitrification could be
a major contributor to N2O emission from the soil, when
moisture conditions were suboptimal for denitrification.
However, the study did not include analysis of NO emission.
Baggs [15] has shown that it is possible to quantify some of
the processes involved in NO and N2O production in soil
by applying stable isotope enrichment techniques. However,
the methods are still only usable in the laboratory, and
further technical advances are needed to quantify the
processes in natural systems.
New insights into the composition, density and activity of
the denitrifying community have been gained from advanced
molecular techniques [16]. Of special interest for the NO formation in soil is nitrite reductase, which catalyses the
Phil Trans R Soc B 368: 20130126
N2O
NO
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aerosols
NO
NH3
NO
OH
HONO
NO2
HNO2
NO2
OH
HNO3
atmosphere
soil
H+
NH+4
NO–2
N(–III)
N(II)
N(III)
HNO3
NO–3
N(IV)
N(V)
Figure 2. Coupling of atmospheric HONO with soil nitrite. Red arrows represent the multiphase processes linking gaseous HONO and soil nitrite (acid – base reaction
and phase partitioning), green arrows represent biological processes, orange arrows represent heterogeneous chemical reactions converting NO2 and HNO3 into HONO
and blue arrows represent other related physico-chemical processes in the N cycle. Adapted from Su et al. [18]. (Reprinted with permission from AAAS).
reduction of soluble nitrite into gaseous nitric oxide. Thus, for
example, it has become possible to measure the abundance and
structural community composition of the functional group
involved in nitrite reduction by analysing the nirK gene
coding for the enzyme nitrite reductase [17].
Other micro-organisms than the true denitrifiers can
reduce nitrate and produce NO. The nitrate respirers produce
nitrite as their end product, and other micro-organisms carry
out dissimilatory reduction of nitrate to ammonium (DNRA).
DNRA is an anaerobic process reducing nitrate via nitrite to
ammonium. Thus, DNRA can play an important role in
retaining N in the ecosystem. DNRA is of highest significance
in wetland ecosystems, but can also be an important process
in tropical forest soils with high clay content as well as in
temperate grassland soils. The role of DNRA in aerobic
soils is not yet clear [9].
(c) Chemodenitrification
The chemical decomposition of nitrite (chemodenitrification)
can be important at low pH. Nitrite is normally only present
in small amounts in soil and is mainly of microbial origin.
Nitrite can be produced from ammonium (by nitrifying
microbes) as well as from nitrate (by denitrifying microbes;
figure 2). High concentrations of nitrite can be found in
water films where Hþ is also present due to microbial activity
and can lead to NO production:
þ
3NO
2 þ 2H ! 2NO " þNO3 þ H2 O.
ð2:6Þ
If ferrous iron or other reduced metals are available, then
nitrite can be reduced chemically to NO:
2þ
þ 2Hþ ! NO " þFe3þ þ H2 O.
NO
2 þ Fe
ð2:7Þ
A further possible chemical reduction pathway for nitrite
is by hydroxylamine. However, this process mainly produces
N2O:
þ
NH2 OH þ NO
2 þ H ! N2 O " þ2H2 O.
ð2:8Þ
Recently, a new pathway for soil nitrite has been
shown [18]:
þ
NO
2 þ H $ HNO2 $ HONO "
ð2:9Þ
The release of HONO from soil nitrite can be especially
large from fertilized soils with low pH. The process is,
however, reversible as also shown by Venterea et al. [19].
(d) Nitric oxide consumption
NO is highly reactive and may therefore easily be decomposed either chemically or biologically. Chemical oxidation
plays a minor role in soil owing to the generally low concentrations of NO in the soil atmosphere. NO can be consumed
by denitrifiers because they can use it as an electron acceptor
in the step that produces N2O (equation (2.5)). This process is
stimulated by anoxic conditions. Other micro-organisms in
the soil are able to oxidize NO to N2O under oxic conditions.
3. Nitric oxide emission from soil
Firestone & Davidson [11] presented a conceptual model for
microbiological and ecological factors controlling soil emissions of NO and N2O. The so-called hole-in-the-pipe (HIP)
model [20] linked the two gases through their common processes of microbial production and consumption. Thus, the
HIP model relates the sum of NO and N2O production to
availability of nitrogen in the soil and to abiotic factors. The
complex effects of soil moisture on gaseous N emission
could be described by relating the ratio NO : N2O to soil
moisture. The HIP model can be explained as nitrogen flowing through two leaky pipes, representing nitrification and
denitrification. NO and N2O ‘leak’ out of the pipes, and the
rate of leaking is determined by the soil moisture. Soil
water both controls oxygen transport in the soil and transport
of gaseous N out of the soil. In dry well-aerated soils, nitrification is the dominant process resulting in NO emission from
the soil because it can diffuse out of the soil before being consumed. In wet soils, denitrification dominates and much of
the NO is consumed before it can leave the soil; thus, N2O
is the dominating gas emitted from the soil. In soils that are
even more wet and mostly anaerobic N2O is reduced to N2
[20], which is subsequently emitted.
(a) Nitrogen availability
The most important factor for NO emission is the availability
þ
of N in the soil, mainly in the form of NO2
3 and NH4 as the
sources for denitrification and nitrification. The pool sizes of
þ
NO2
3 and NH4 are a net result of N input to the ecosystem
and N output and the processes involved. Basically, there
are three major forms of nitrogen input: nitrogen fixation,
nitrogen deposition and input as fertilizer/manure, and
two forms of nitrogen output: gaseous emission and leaching.
Phil Trans R Soc B 368: 20130126
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H+
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3
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þ
Soil water acts as a transport medium for NO2
3 and NH4 and
influences the rate of O2 supply and thereby controls whether
aerobic processes such as nitrification or anaerobic processes
such as denitrification dominate within the soil. In general,
gaseous N
N2
N2O
NO
0
20
40
80
60
100
WFPS (%)
Figure 3. Proposed relative contributions of nitrification (solid grey shading)
and denitrification (hatched shading) to gaseous N emissions as a function of
water-filled pore space (WFPS). Adapted from Davidson et al. [20].
NO emission (% of maximum)
100
sandy loam
silty loam
sandy clay loam
loam (1)
loam (2)
80
60
40
20
0
0
20
40
60
WFPS (%)
80
100
Figure 4. The relationship between NO emission and water-filled pore space
(WFPS) from different forest soils in the NOFRETETE project (based on data in
Schindlbacher et al. [26]).
nitrification dominates at values of water-filled pore space
(WFPS) below 60 per cent and denitrification dominates at
values above 60 per cent. Thus, at a WFPS of 60 per cent, the
ratio of NO : N2O is often close to 1 (figure 3). Owing to limited
substrate diffusion at very low water content and limited gas
diffusion at high water content, maximum NO emission generally occurs at intermediate soil moisture. Because NO is highly
reactive, it will more readily be consumed at high soil moisture
where the residence time is longer.
In a laboratory study with soil cores from European forest
soils, Schindlbacher et al. [26] found that soil moisture and
temperature explained 74 per cent of the variability in NO
emission. NO was emitted from all the soils except from a
boreal pine forest soil in Finland, where the laboratory experiment showed net NO consumption. NO emissions from
a German spruce forest ranged from 1.3 to over 600 mg
NO–N m – 2 h – 1 and greatly exceeded emissions from other
soils. Average N2O emissions from this soil tended also to
be the largest (170 + 40 mg N2O-N m – 2 h – 1), but did not
differ significantly from other soils. The optimal soil moisture
for NO emission differed significantly between the soils, and
ranged between 15 per cent WFPS in sandy Italian floodplain
soil and 65 per cent in loamy Austrian beech forest soils
(figure 4). Thus, each soil had its own optimum probably
owing to differences in other soil characteristics.
Goldberg & Gebauer [27] studied the effect of soil moisture on NO emission by experimental induced drought
Phil Trans R Soc B 368: 20130126
(b) Soil moisture
4
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Leaching is mostly in the form of NO2
3 and to a lesser extent
dissolved organic nitrogen.
The transformation of atmospheric N2 to NH3 (nitrogen
fixation) is an important pathway for nitrogen, because N2
normally cannot be directly used by organisms for their metabolism. Biological fixation can be carried out by certain symbiotic
and heterotrophic bacteria in the soil. Fixation by leguminous
symbiotic bacteria has an especially large potential and these
bacteria can fix up to 200 kg N ha – 1 yr – 1, whereas fixation
by heterotrophic bacteria is generally in the order of
1–5 kg N ha – 1 yr – 1 [9]. High NO emission has been observed
from soils with legumes capable of symbiotic nitrogen fixation
[21].
In most agricultural systems, nitrogen input as fertilizer
(either natural in the form of livestock manure or as synthetic
fertilizer) is the most important source of N in the soil. The
mean national input to European agricultural soils varies
from 42 in Portugal to 243 kg N ha – 1 yr – 1 in the Netherlands
[22]. A rapid increase in NO emission is normally observed
immediately after fertilizer application. The effect of fertilizer
input on soil NO emission is very variable and ranges from
0.003 to 11 per cent with an average of approximately 0.5 per
cent of the N applied as fertilizer [7].
Nitrogen can be deposited from the atmosphere as
both wet deposition (dissolved in rain water) and dry deposition (as gases or particles). Deposition to open land with
short vegetation is mainly in the form of wet deposition
and amounts to 3–30 kg N ha – 1 yr – 1 over Europe. Forest
canopies act as efficient sinks for gases and particles, and
deposition to forest is therefore often twice as high as to
open land (5–60 kg N ha – 1 yr – 1). The lowest deposition is
found in northern Europe and the highest in central and
western Europe with high industrialization and intensive
agriculture [9].
Pilegaard et al. [23] found significant positive correlations
between deposition of nitrogen to forests and NO emission.
Similarly, elevated fluxes of NO were observed after N
addition (þ50 and þ150 kg N ha – 1 yr – 1) to coniferous forest
soils [24], but only the highest amount had an effect on deciduous forest soil. It was concluded that atmospheric deposition
may result in increased NO emission from forest soils by
promoting nitrification, and that the response may vary significantly between forest types under similar climatic regimes.
However, increased nitrogen input does not always lead to
enhanced microbial activity. Burton et al. [25] found that
forest soil N availability was enhanced following simulated
chronic NO2
3 deposition, but after an initial increase, soil respiration was reduced, probably owing to reduced decomposition
activity of the microbial community.
Measurements of nitrification potential have shown the
highest correlation with NO (and N2O) emission [20], but
other indexes such as the litterfall C : N ratio have also
shown to be a reasonable proxy for nitrogen availability.
However, because many diverse processes lead to NO formation in the soil, it will be difficult to identify a single
index for the prediction of soil NO emission.
36
50
150
30
28
50
26
150
soil moisture (vol%)
0
20
0
24
22
NO flux
(µg N m–2 h–1)
0
15
2
10
32
0
4
34
0
–5
0
250
0
8
12
16
20 24 28 32 36 40 44
water-filled pore space (%)
48
Figure 5. Mean daily NO fluxes in throughfall exclusion and control plot
dependent on the water-filled pore space in the organic layers (6 cm depth).
(Reprinted from Goldberg & Gebauer [27] with permission from Elsevier.)
(throughfall exclusion) in a Norway spruce forest followed by
re-wetting. They found a maximum NO emission for this soil
at 33 per cent WFPS in the organic layer (figure 5). They
observed decreased NO emission during natural rain
events, but a large NO emission after re-wetting of the soil
following drought. The high emission following drought
might be due to accumulation of nutrients during the
drought period and re-activation of the micro-organisms
immediately after re-wetting.
(c) Soil temperature
As long as other factors such as substrate availability and soil
moisture are not limiting, NO emission increases with soil
temperature owing to the positive effect of temperature on
enzymatic processes and microbial turnover rates. Thus,
temperature is not a primary control factor for the magnitude
of soil emission, but rather a modulating factor of short-term
variations [7]. In general, it has been found that NO emission
increases exponentially with soil temperature [26] with Q10 1
values in the range of 2–3 [28,29]. Some soils, however,
have much higher activation energies, resulting in Q10 of up
to 10 which could be due to strong chemodenitrification [26].
Based on a 5 year dataset of continuous measurements
of soil– atmosphere exchange of N2O, NO and CO2 at the
temperate, nitrogen-saturated Norway spruce forest site
Höglwald, Wu et al. [28] found that NO emissions were positively correlated with WFPS up to a soil temperature of 158C,
but at soil temperatures above 158C, highest NO emissions
were found at lowest WFPS values. The correlation of trace
gas fluxes with soil temperature was stronger than that
with soil moisture. However, soil moisture could become
the crucial regulator for N2O emission during freeze/thaw
periods. The effects of freeze/thaw events on NO emission
were negligible, but an increased NO emission was observed following soil re-wetting after long drought periods. The
NO : N2O ratio was determined by WFPS rather than by soil
temperature. A significant positive correlation between soil
temperature and NO : N2O ratio was observed only when
WFPS was below 45 per cent. The highest NO : N2O ratio
was found under conditions favourable to nitrification (soil
temperature around 158C; WFPS less than 40%). A recent
analysis of soil flux measurements over the period 1994–2010
at the Höglwald site [30] confirmed these findings, specifying
5
15
10
soil temperature (°C)
20
Figure 6. Effects of soil moisture (10 cm depth) and temperature (5 cm depth)
on monthly means of soil NO fluxes. Results from NO emission measurements in
the Höglwald forest during 1994–2010 (adapted from Luo et al. [30]).
that NO fluxes were highest when the temperature was high
(more than 158C), but the soil moisture was in the range of
24–30 vol% (figure 6).
(d) pH
A high pH generally favours nitrification and thus NO emission. Decreasing pH values lead to increased NO production
by denitrification, and chemodenitrification (NO production from NO2
2 ) increases at a pH less than 4 [29]. Because
different NO producing processes are favoured by different
pH values, there is often no direct relationship between the
amount of NO emitted and the pH.
(e) Vegetation
Vegetation type seems to have an influence on NO emission.
Both the immediate vegetation cover of the soil and the ecosystem as such can influence the emission. Thus, moss cover
seems to reduce NO emission [31]. This was confirmed by laboratory measurements of nitric oxide from a spruce forest soil
by Bargsten et al. [32], who found the lowest emissions for
soil samples taken under moss and grass and highest emissions
from soil samples taken under blueberry and spruce.
In the NOFRETETE project [23] of nitrogen oxide emission from soils at 15 forest sites across Europe, it was found
that coniferous forest soils had much higher NO emissions
than deciduous forest soils. This is probably due to differences in soil and litter properties in the two types of
forests. Thus, Finzi et al. [33] found large differences in C
and N pools and in net N mineralization in the soil under
six different tree species. Similarly, from studies in a species
trial, Brüggemann et al. [34] found the highest rates of soil respiration, gross N mineralization and gross nitrification in the
organic layer under spruce, followed by beech . larch .
oak . pine. Nitrification and thus NO emission is favoured
by a coniferous forest floor because of the aerobic conditions
in the litter and the lower water content. Another explanation
of the large difference in NO emission from spruce and beech
forest might be that the filtering capacity of the much denser
spruce forests is higher than that of beech forests and thus the
throughfall carries a higher amount of deposited N from the
atmosphere to the forest floor [35].
Once emitted from the soil, NO might react with O3 to
form NO2 that can be taken up by the canopy and thus eventually return to the forest soil. This so-called canopy
reduction is important for the estimation of NO emission to
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–50
0
50
100
150
200
250
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6
0
0
8
5
–5
100
50
throughfall exclusion 2006
throughfall exclusion 2007
control 2006
control 2007
10
NO flux (µmol m–2 h–1)
10
50
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vegetation, input type
6
(b)
N input/availability
soil type
temperature
(d) chemodenitrification
nitrification
denitrification
soil water content
pH
Figure 7. Overview of main factors affecting NO emission from the soil: (a) linear response of NO emission versus N input or N availability, the slope is dependent on
vegetation type and type of input (e.g. fertilizer application, wet deposition); (b) temperature sensitivity with a Q10 of approximately 2; (c) maximum NO emission at
intermediate soil water content, moderated by soil type; (d) highest NO emission at acid conditions (chemodenitrification) and basic conditions (nitrification).
the free atmosphere, especially from forest soils. On the other
hand, foliar uptake of NO2 might be an important source of
N for the forest ecosystems [36].
Figure 7 gives an overview of the main factors controlling
NO emission.
temperature and precipitation (as a proxy for soil moisture)
into account:
(f ) Range of nitric oxide emission
where fw/d is some function of temperature (constant, linear,
exponential), Aw/d (biome) a coefficient to distinguish
between biomes (11 classes), P ( precipitation) a scalar function to adjust for pulses (wetting events, four different
classes) and CR(LAI, SAI) a scalar reduction factor that
accounts for canopy uptake of NOx. The annual estimate of
soil emission for Europe was 0.74 and 5.5 Tg N yr – 1 for the
Globe with a range of 3.3– 7.7 Tg N yr – 1. The same algorithm,
but with different database sources, was used by Ganzeveld
et al. [6] who estimated the global soil emission to be 12 Tg N
yr – 1.
Stehfest & Bouwman [40] compiled information from several hundred measurements of NO emission from soils (189
from agricultural fields and 210 from soils under natural vegetation). Based on statistical models of the factors controlling
NO emission (mainly vegetation type and soil C content),
they estimated the NO emission from soils globally to be
1.8 Tg N yr – 1 (1.4 Tg from fertilized cropland and 0.4 Tg
from grassland). A similar statistical approach was used by
Yan et al. [41] to estimate global NOx emission from soils
based on organic carbon content, soil pH, land-cover type,
climate, nitrogen input, soil temperature, soil moisture and
vegetation fire. The annual NOx emission from global soils
was calculated to be 7.43 Tg N, decreasing to 4.97 Tg N
after canopy reduction. The fertilizer emission factor was calculated to be 1.16 per cent above soil and 0.70 per cent above
canopy, which is somewhat higher than the factor applied by
Skiba et al. [37] and Simpson et al. [38].
To estimate future climate effects on N2O and NO emissions from European forest soils, Kesik et al. [42] used the
model PnET-N-DNDC (a combination of the photosynthesisevapotranspiration model (PnET), the denitrification–
decomposition (DNDC) model and a nitrification module).
The model was tested against data from the forest soils in
Ludwig et al. [7] summarized a large number of soil NO
emission measurements made in different ecosystems
throughout the globe. The mean annual emission ranged
from less than 0.01 to 30 kg N ha – 1 yr – 1. Generally, agricultural fields receiving fertilizer showed the highest emissions
followed by grasslands, forests and other natural ecosystems.
Some of the lowest values in forests are found in nitrogenpoor forest soils with low N input from the atmosphere
such as the Hyytiälä forest in Finland, whereas the highest
emission is found in nitrogen-saturated forests in areas with
a high N deposition like Höglwald in Germany and Speulderbos in the Netherlands [23].
4. Modelling and upscaling
Owing to the many biotic and abiotic factors controlling soil
emission of NO, there is a substantial uncertainty in the
scaling up to regional and global estimates. Several attempts
have been made to provide modelling schemes for this task.
Skiba et al. [37] presented an approach based on a simple
relationship of soil NO emissions as a factor of fertilizer-N
input. The fraction emitted was set to 0.3 per cent of the
added fertilizer N. To account for non-agricultural areas,
two additional assumptions were made by Simpson et al.
[38]: a background emission of 0.1 ng NO–N m – 2 s – 1,
and the fraction of applied N released as NO was applied to
all inputs of N whether as fertilizer, animal manure or
as atmospheric deposition. This approach resulted in an
estimate of an annual NO emission from European soils of
0.14–1.5 Tg N.
A slightly more complicated and widely used model is
the one by Yienger & Levy [39]. This model takes both
Flux ¼ fw=d ðsoil temperature; Aw=d ðbiomeÞÞ
P ð precipitationÞ CRðLAI, SAIÞ
ð4:1Þ
Phil Trans R Soc B 368: 20130126
NO emission
(c)
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NO emission
(a)
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model has been successful in simulating CO2 and N2O emission from the Höglwald forest. It remains, however, to be
demonstrated how well it simulates NO emission.
5. Outlook
Endnote
1
Rate of change with a temperature increase of 10.
References
1.
2.
Arneth A et al. 2010 From biota to chemistry and
climate: towards a comprehensive description of
trace gas exchange between the biosphere and
atmosphere. Biogeosciences 7, 121–149. (doi:10.
5194/bg-7-121-2010)
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in the climate system and biogeochemistry. In
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Davidson EA, Kingerlee W. 1997 A global inventory
of nitric oxide emissions from soils. Nutr. Cycling
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NOx emissions and the role of canopy processes.
Phil Trans R Soc B 368: 20130126
Although more focus has been placed on N2O emission, many
new field studies have been carried out to quantify emissions
of NO from soils, giving us a comprehensive knowledge of
NO emission from various ecosystems, soil types and climatic
conditions. However, most field studies were short-term, and
to elucidate the temporal variation there is a need for continuous long-term (multi-year) measurements.
Recent years have also provided an improved mechanistic
understanding of NO formation and consumption in the soil,
partly because of the application of new tools from molecular
biology. The many laboratory and field studies have provided
increased knowledge of the controlling factors for NO emission.
NO emission from soils is the result of many processes with
many types of micro-organisms involved. Abiotic factors in the
soil influence the processes to different extents and simulation
of NO emission is therefore complicated. Models of NO emission generally fall into two categories: very simple models with
few factors or very complicated models, including mechanistic
processes in the soil. The simple models have the advantage of
being more easy to upscale, because of a lower demand on
input information, whereas the advanced process models are
able to simulate plot-scale measurements quite accurately.
Recently, intermediate models have been developed with the
hope that more precise estimates of regional and global NO
emission can be provided.
The present global or regional estimates are, however,
quite far from converging and show a range of values with
about a factor of 10 in difference between the lowest and
highest estimates. Clearly, there is a need for more field
and laboratory experiments to elucidate the mechanisms controlling NO emission from the soil, and especially long-term
continuous measurements are needed because of a high temporal variation. Model development should be continued
both with respect to models requiring few input parameters
(for estimating global and regional emission) and models
that can accommodate the detailed knowledge of all the processes and factors controlling NO emission from the soil to be
used in areas where sufficient input data are available.
7
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the NOFRETETE project [23] and combined with climate
scenarios and GIS information. According to the scenario,
mean annual surface temperatures in Europe in 2031–2039
will be approximately 1.88C higher (from 7.6 to 9.48C)
compared with the period 1991–2000. The average precipitation over Europe is predicted to be almost unchanged but
with large regional differences such as increases along the western coasts by up to 30 per cent, but decreases in many inland
regions and especially in the Mediterranean area by up to 80
per cent. Using this scenario, the forest soil NO emissions
were predicted to increase by 9 per cent from 0.068 to
0.074 Tg NO–N yr – 1.
The same approach was used to calculate NO emissions
from both agricultural and forest soils [43]. Total forest soil NO
emission from EU15 countries was estimated at 0.075 Tg
NO–N yr – 1 and total agricultural soil NO emission at
0.102 Tg NO–N yr – 1 which amounts to 4–6% of the total
anthropogenic emission from Europe. This model estimate was
compared with the approaches described above by Yienger &
Levy, Skiba et al., Simpson et al., and Stehfest & Bouwman,
and it was found that the estimates for agricultural soils varied
by a factor of 4 with the Yienger and Levy approach giving the
highest estimate (0.190 Tg NO–N yr – 1) and the Skiba/Simpson
approach giving the lowest estimate (0.049 Tg NO–N yr – 1). In
summary, estimates of global soil NO emission ranges from
1.8 Tg NO–N yr – 1 [40] to 12 Tg NO–N yr – 1 [6] and European
soil NO emission from 0.14 to 1.5 Tg NO–N yr – 1 [38].
It was recognized by de Bruijn et al. [44] that the data
requirements of the process-based models are very high and
therefore make their application for regional and global scaling
up difficult. They tested a simplified model (DecoNit) for
describing biogeochemical processes of C and N in combination with a modular simulation environment where it is
combined with soil water balance and forest process submodules. The modelling approach was tested with data from the
NOFRETETE forest sites. The model performed better than
the PnET-N-DNDC model [45] by providing a more precise
simulation of the annual emission rates, and also a somewhat
more precise prediction of the variation on shorter time scales.
A new model of medium complexity, MiCNiT, for simulation of soil air NO, N2O and N2 concentrations and net
exchange of these gases at the soil–atmosphere interface has
recently been published [46]. The MiCNiT model calculates
decomposition of soil organic matter, dynamics of microbial biomass, denitrification, autotrophic and heterotrophic
nitrification by applying the microbial activity concept, as
well as transport of gases and solutes between anaerobic and
aerobic soil fractions and through the soil profile. So far, the
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