Introduction
Nitrous acid (HONO) plays an important role in tropospheric chemistry, as it
is one of the major precursors of the hydroxyl (OH) radical, which determines
the oxidizing capacity of the atmosphere. In the early morning, HONO
photolysis has been shown to contribute up to 30 % to the local OH budget
(Alicke et al., 2002; Kleffmann et al., 2005; Ren et al., 2003, 2006;
Meusel et al., 2016). Currently, the HONO formation processes, especially
during daytime, are still not fully understood. Recent ground-based field
measurements showed unexpectedly high daytime concentrations of HONO, which
could not be solely explained by atmospheric gas-phase reactions (R1–R3)
(Kleffmann et al., 2003, 2005; Su et al., 2008a; Sörgel et al.,
2011a; Su et al., 2011; Michoud et al., 2014; Czader et al., 2012; Wong et
al., 2013; Tang et al., 2015; Oswald et al., 2015, Meusel et al., 2016).
OH+NO→HONOHONO⟶hv(300-405nm)OH+NOHONO+OH→NO2+H2O
Several studies have shown that HONO can be heterogeneously formed from
NO2 on a variety of surfaces, e.g., soot, humic acid, minerals,
proteins and organically coated particles (Ammann et al., 1998; Arens et
al., 2001; Aubin et al., 2007; Bröske et al., 2003; Han et al., 2016;
Kalberer et al., 1999; Kleffmann et al., 1999; Kleffmann and Wiesen, 2005;
Lelièvre et al., 2004; Kinugawa et al., 2011; Liu et al., 2015; Wang et al.,
2003; Yabushita et al., 2009; Meusel et al., 2017). Light can activate some
of these surfaces (humic acid, proteins and other organic compounds,
titanium dioxide, soot), which enhances NO2 uptake and HONO production
(George et al., 2005; Langridge et al., 2009; Monge et al., 2010; Ndour et
al., 2008; Ramazan et al., 2004; Stemmler et al., 2007; Kebede et al., 2013;
Meusel et al., 2017). However, NO2 uptake coefficients and the ambient
aerosol surface areas for heterogeneous reactions of NO2 were
nevertheless frequently found to be too low to account for the observed HONO
production rates (Stemmler et al., 2007; Sarwar et al., 2008; Zhang et al.,
2016). In addition to the heterogeneous NO2 reaction, Bejan et al. (2006)
observed HONO formation during irradiation of nitrophenols. Photolysis of
nitrate or nitric acid generates HONO as well (Baergen and Donaldson, 2013;
Scharko et al., 2014; Zhou et al., 2003, 2011). Contrary to the detected
missing HONO source near the ground, recent airborne measurements
(500–1200 m a.g.l., above ground level) observed HONO concentrations, which could be explained
by gas-phase reactions only (Li et al., 2014; Neuman et al., 2016). However,
vertical gradient studies showed higher HONO concentrations near the ground
than in higher altitudes, indicating a ground level source (Harrison and
Kitto, 1994; Kleffmann et al., 2003; Ren et al., 2011; Stutz et al., 2002;
VandenBoer et al., 2013; Villena et al., 2011; Zhou et al., 2011; Wong et
al., 2012, 2013; Vogel et al., 2003; Zhang et al., 2009; Young et al.,
2012). This is supported by gas exchange studies showing that HONO and NO
can be emitted from (natural) soil and biological soil crusts (biocrusts,
BSCs), even without applying atmospheric NO2 (Su et al., 2011; Oswald et
al., 2013; Mamtimin et al., 2016; Weber et al., 2015; Meixner and Yang,
2006). HONO and NO can be formed during biological processes (nitrification
and denitrification; Pilegaard, 2013), in which NH3 or NH4+
is oxidized stepwise or NO3- is reduced (Fig. 1). Depending on
soil pH and according to Henry's law, soil nitrite
(NO2-) can be converted into gaseous HONO. It was found that
sterilized soil emits lower amounts of reactive nitrogen than natural soil
(Oswald et al., 2013; Weber et al., 2015).
Nitrogen cycle at the atmosphere and pedosphere–biosphere interface
including nitrogen fixation, nitrification, denitrification and emission.
Enzymes and organisms involved are specified.
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Biocrusts grow within the uppermost millimeters to centimeters of soil in
arid and semiarid ecosystems. They are composed of photoautotrophic
cyanobacteria, algae, lichens, and bryophytes, growing together with
heterotrophic bacteria, fungi and archaea in varying proportions (Belnap et
al., 2016). Depending on the dominating photoautotrophs,
cyanobacteria-dominated biocrusts with an initial thin light-colored and
well-developed dark type, cyanolichen- and chlorolichen-dominated biocrusts
with lichens comprising cyanobacteria or green algae as photobionts, and
bryophyte-dominated biocrusts are distinguished (Büdel et al., 2009).
Many free-living cyanobacteria but also those in symbiosis with fungi
(forming lichens) and vascular plants can fix atmospheric nitrogen N2
and convert it into ammonia (Cleveland et al., 1999; Belnap, 2002; Herridge
et al., 2008; Barger et al., 2016). Globally it has been estimated that
100–290 Tg (N) yr-1 is fixed biologically (Cleveland et al., 1999), of
which 49 Tg yr-1 (17–49 %) is fixed by cryptogamic covers, which
comprise biocrusts, but also other microbially dominated biomes, like lichen
and bryophyte communities occurring on soil, rocks and plants in boreal and
tropical regions (Elbert et al., 2012). Studies have suggested that
nitrogen cycling in soil (N2 fixation, nitrification, denitrification)
and hence reactive nitrogen emission (NO, N2O, HONO) is often enhanced
by well-established biocrusts, especially by dark cyanobacteria (Cleveland
et al., 1999; Elbert et al., 2012; Belnap, 2002; Barger et al., 2013;
Johnson et al., 2005; Abed et al., 2013; Strauss et al., 2012; Weber et al.,
2015). However, much of the molecular biology and chemistry that is important for
atmosphere–land interactions likely occurs just below the crust (that
is visible at the surface).
In Cyprus, an island in the semiarid eastern Mediterranean area, biocrusts ubiquitously cover ground surfaces and hence can be anticipated to
play an important role in the local HONO budget. In the CYPHEX (CYprus PHotochemical EXperiment) campaign in 2014
the observed diel cycles of HONO ambient
air concentrations revealed strong unaccounted-for sources of HONO and NO
that were
well correlated with each other (Meusel et al., 2016). With low NO2
concentrations and high HONO / NOx ratios, direct emissions
from combustion and heterogeneous reactions of NO2 could be excluded as
significant HONO sources, leaving emissions from soil and the respective
surface cover to be the most plausible common source for both nitrogen
species (Meusel et al., 2016).
In the present study we have measured HONO and NO fluxes from soil and
biocrust samples from Cyprus by means of a dynamic chamber system. The aim
of this study was to characterize and quantify direct trace gas emissions
and demonstrate their impact on the atmospheric chemistry in the remote
coastal environment of Cyprus.
Methods
Sampling
Bare soil and biocrust samples were collected on 27 April 2016 on the
southern-southeastern side of the military station in Ineia, Cyprus
(34.9638∘ N, 32.3778∘ E), where the CYPHEX campaign took
place in 2014. It is a rural site about 600 m a.s.l. (above sea level) and
approximately 5–8 km from the coast and is surrounded by typical
Mediterranean vegetation (olive and pine trees; small shrubs like
Pistacia lentiscus, Sacopoterium spinosum and Inula viscosa). More
details about the site can be found in Meusel et al. (2016).
In an area of about 8580 m2 (southern-southeastern direction of
the station) 50 grids (25 × 25 cm) were placed at randomly selected spots for
systematic ground cover assessment. At each grid point occurrence of nine
types of surface cover (i.e., light and dark cyanobacteria-, chlorolichen-,
cyanolichen-, and moss-dominated biocrust; bare soil; stone; litter;
vascular vegetation/shrub) were assigned and quantified. Spatially
independent replicate samples of light
cyanobacteria-dominated biocrusts (light BSC), dark cyanobacteria-dominated
biocrusts with cyanolichens (dark BSC), chlorolichen-dominated biocrusts
(chlorolichen BSC I, chlorolichen BSC II), moss-dominated biocrusts (moss
BSC) and of bare soil were collected (Fig. S1 in the Supplement). Each sample was collected
in dry state in a plastic petri dish (diameter 5.5. cm, height 1 cm), sealed
and stored in the dark at room temperature until further analysis (storage
time less than 15 weeks). Storage of biocrust samples under dry and dark
conditions at room temperature is the most widely spread method and has
been used in many other studies on N cycling in which samples have been
stored even up to 6 months before measurements were performed (Abed et al.,
2013; Strauss et al., 2012; Johnson et al., 2007; Brankatschk et al.,
2013).
Overview of the samples, distribution of replicates of soil–biocrust
type and the different analyses.
Type
Only nutrient
Flux measurements, followed by
Sum
analysis
nutrient and chlorophyll analysis
Bare soil
3
3
6
Dark BSC
3
5
8
Light BSC
3
4
10
Light BSC + cyanolichen
3
Chlorolichen BSC I
3
3
12
Chlorolichen BSC II
6
Moss BSC
3
4
7
Sum
18
25
43
In total 43 samples were collected (Table 1) of which 18 samples, i.e., three
replicates of each HONO-emitting surface cover type, were used directly
(upfront) for nutrient analysis, while all others were first used for trace
gas exchange measurements prior to nutrient and chlorophyll content
analysis.
Meteorological data
During CYPHEX the meteorological parameters were measured at
about 5 m a.g.l., considered not representative for the microhabitat of the soil
ground surface. Hence, we placed three humidity (and temperature) sensors
(HOBO Pro v2) just on top of the soil surface about 4 weeks prior to sample
collection. Reference meteorological data (air temperature, humidity and
precipitation) from Paphos airport (about 20 km south of the sample area, 12 m a.s.l.) and
Prodromos (about 40 km east of the sampling area, 1380 m a.s.l.)
during the sampling period as well as the precipitation data from the last 4 years (2013–2016)
were provided by the Department of Meteorology, Cyprus
(http://www.moa.gov.cy/moa/ms/ms.nsf/DMLmeteo_reports_en/MLmeteo_reports_en?opendocument; last access: December 2016).
Soil characteristics: nutrient, chlorophyll and pH
Soil characteristics (nutrient, pH) have an effect on soil emission, e.g.,
higher nutrient level and lower pH would enhance emission according to
Henry's
law (Su et al., 2011). Nutrient analysis was conducted on samples without
gas exchange measurements (n = 3) and on replicate samples after gas
exchange measurements in order to analyze potential effects of the applied
“wetting–drying” cycle. Nitrate (NO3-), nitrite (NO2-)
and ammonium (NH4+) were analyzed via flow injection analysis with
photometric detection (FIAstar 5000, Foss, Denmark). Prior to that, the
samples comprised of soil and its biocrust cover were gently ground and an
aliquot of 7 g was dissolved in 28 mL of 0.0125 M CaCl2. After shaking for
1 h the mixture was filtered on a N-free filter. The detection limits
were 0.014, 0.046 and 0.047 mg kg-1 for NO2--N,
NO3--N and NH4+-N, respectively.
Chlorophyll analysis, as an indicator of biomass of photoautotrophic
organisms, was performed according to the dimethyl sulfoxide (DMSO) method (Ronen
and Galun, 1984). Ground samples were extracted twice with CaCO3-saturated DMSO (20, 10 mL) at 65 ∘C for 90 min. Both extracts
were combined and centrifuged (3000 G) at 15 ∘C for 10 min. The
light absorption at 648, 665 and 700 nm was detected with a spectral
photometer (Lambda 25 UV/VIS Spectrometer, PerkinElmer, Rodgau). The amount
of chlorophyll a (Chla)
was calculated according to Arnon et al. (1974).
Chlorophyll a+b (Chla+b) content was calculated according
to O. L. Lange, W. Bilger, and H. Pfanz (personal communication with B. Weber, 1995; Weber et al., 2013):
Chla+bµg=20.2⋅E648-E700+8.02⋅E665-E700⋅aChlaµg=12.19⋅E665-E700⋅a,
where Chla+b[µg], Chla[µg] is the chlorophyll content of
the sample; E648, E665, and E700 are light absorption at the
given wavelength; and a is the amount of DMSO used (in milliliters).
The pH was determined for each surface cover type (n = 3–4) according to
Weber et al. (2015, Supplement). Here, 1.5 g of the ground sample was mixed with
3.75 mL of pure water and shaken for 15 min. Then the slurry was centrifuged
(3000 G, 5 min) to separate the solid phase from the liquid solution. The
latter was used for pH determination by means of a pH electrode (InLab
Expert Pro-ISM, Mettler Toledo).
Trace gas exchange measurements
The dynamic chamber method for analyzing NO and HONO emissions from soil
samples was already introduced before (Oswald et al., 2013; Weber et al.,
2015; Wu et al., 2014) and in general showed good agreement with flux
measurements in the field (van Dijk et al., 2002; Rummel et al., 2002).
Under the prevailing dry and hot conditions in Cyprus, macropores and cracks
are likely to be present in the soil layer. It is assumed that during the
sampling and sample treatment the number and sizes of soil cracks was not
significantly increased so that the diffusivity of gases in the soil samples
is comparable to the one in soil in the natural environment. Intact soil and
biocrust samples (25–35 g in a plastic petri dish with 5.5 cm diameter and
about 1 cm height) were wetted with 8–13 g of pure water (18.2 MΩ)
up to full water holding capacity and placed into a dynamic Teflon film
chamber (≈ 47 L) flushed with 8 L min-1 dry pure air (PAG 03,
Eco Physics, Switzerland). Intact (biocrust) samples consist of a few millimeters of
the biocrust and the underlying soil. Typical drying cycles lasted between 6
and 8 h. A Teflon-coated internal fan ensured complete mixing of the
chamber headspace volume. During the experiments the chamber was kept at a
constant temperature (25 ∘C, the mean daytime air temperature
during CYPHEX) and in darkness to avoid photochemical reactions. At the
chamber outlet the emitted gases HONO, NO and water vapor were quantified.
HONO was analyzed with a commercial long path absorption photometer (LOPAP,
Quma GmbH; Wuppertal, Germany) with a detection limit of ∼ 4 ppt
and 10 % uncertainty (based on the uncertainties of liquid and gas
flow, concentration of calibration standard, and regression of calibration).
To avoid any transformation of HONO in the tubing, the sampling unit
including the stripping coil from LOPAP was directly connected to the
chamber. NOx (NO + NO2) was detected with a commercial
chemiluminescence detector (42i-TL, Thermo Scientific; Waltham, USA) modified
with a photolytic converter with a detection limit of ∼ 50 ppt
(NO) and ∼ 200 ppt (NO2). An infrared CO2 and
H2O analyzer (Li-840A, Li-cor; Lincoln, USA) was used to log the drying
and to calculate the soil water content (SWC) of the samples as follows:
SWC(WHC)=mH2O,t=nmH2O,0⋅100mH2O,t=n=mH2O,t=n-1-SLicor,t=n∑t=0t=NSLicor⋅mH2O,0,
with t= 0 denoting the measurement start (wetted sample inserted into
chamber), t= n any time between 0 and N, t= N the time when the sample had dried
out and measurement was stopped, SLicor the absolute H2O signal at a
given time, mH2O,0 the mass of water added to the sample (water-holding
capacity, WHC) and SWC the soil water content in % WHC.
Data analysis
Measured data of NO2-, NO3-, NH4+,
Chla+b, Chla, NO and HONO optimum flux and NO and HONO integrated
flux did not follow a normal distribution. Rather, log-transformed data were
normally distributed (Shapiro–Wilk) and therefore used for statistical
analysis (Pearson correlation, ANOVA including a Tukey test with a significance
level of p = 0.05) executed with OriginPro (version 9.0; OriginLab
Corporation, Northampton, Massachusetts, USA).
Precipitation data from the last 4 years (2013–2016), provided by the
Department of Meteorology of Cyprus, indicating about 30 rain events per
year (precipitation > 1 mm with following one or more dry days)
were used to estimate annual emissions of total nitrogen in terms of HONO
and NO.
Results and discussion
Meteorological conditions
About 1 month before sampling, three sensors measuring temperature and relative
humidity were installed directly above the soil surface in the field to
represent the microclimate of the ground surface. Reference air
temperature, humidity and precipitation measurements at Paphos airport and
Prodromos showed one rain event on 11–12 April, which is reflected by higher
soil humidity (80–100 %) and lower temperatures on these days (see Fig. S2).
As a consequence, the biological soil crusts were activated and went
through one full wetting and drying cycle before sample collection.
Temperature above the soil ranged from 10 ∘C at night to
50 ∘C during the day when solar radiation was most intense. Air
temperature was similar at night but not as hot during the day,
ranging between 20 and 30 ∘C. Humidity above the ground
was low during the daytime (< 30 % rH) and increased during the night
up to 80 %, while the atmospheric relative humidity (at Paphos airport)
ranged between 47 and 73 % (without rain event). Thus, there were only
little variations in humidity with height above the soil surface. Above the
ground surface the relative humidity was somewhat lower during the day
(mainly caused by higher temperatures) but somewhat higher at night,
compared to respective weather station data. During and shortly after the
main rain event humidity at ground level was higher (80 and 100 % rH)
compared to ambient air humidity (70–85 % rH). Ambient air temperatures
were somewhat lower during sample collection of this study as compared to
the CYPHEX field campaign in 2014. During CYPHEX, nighttime temperatures
(3 m a.g.l.) did not drop below 18 ∘C. Relative
humidity (3 m a.g.l.) was mostly between 70 and 100 % with
only two short periods with humidity between 20 and 60 % rH. Hence, we can
assume that soil surface temperatures were higher and ground relative humidity in the same
range during CYPHEX compared to sampling period.
Cyprus soil and biocrust characteristics
The different biocrust types were distinguished in the field based on the
dominating phototrophic compound but which provides no information about the
microbial community below or about the magnitude of (de)nitrification
processes. The microbial community could not be determined using
nondestructive methods. Systematic mapping of surface covers revealed that
moss-dominated biocrusts are the most frequent in the investigated Cyprus
field site area (21.3 %), followed by light (10.4 %) and dark BSC
(6.5 %), whereas chlorolichen- (3.2 %) and cyanolichen-dominated BSC
(1.8 %) only played a minor role (Figs. 2 and S1). The soil surface was
partially covered by litter (26.3 %), stones (19.5 %) and vascular
vegetation (8.5 %), whereas open soil was rarely found (2.5 %). It was
previously established that soil and biocrusts emit HONO and NO (Weber et
al., 2015; Oswald et al., 2013), jointly accounting for 45.6 % of surface
area in our studied region. To the best of our knowledge, no data on
reactive nitrogen emissions from vascular vegetation and plant litter have
been published yet.
Distribution of different types of ground surfaces in the studied
area. Information derived from 50 grids.
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Nutrient and chlorophyll contents as well as pH values of bare soil
and biocrust samples of different types. (a) Nitrate, nitrite and ammonium
content of all replicates. The red star indicates an outlier; (b) chlorophyll a
and chlorophyll a+b contents of samples after flux measurements and (c) pH
values of samples without and after flux measurements (bare soil and moss
BSC: n = 4; light, dark and chlorolichen BSC: n = 3). For the number of
replicates for a and b, see Table 1. In all three plots error bars indicate
standard error of the mean and different letters indicate significant
differences (of log-transformed data; p = 0.05).
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Nutrient analysis revealed large variations in concentrations of nitrogen
species ranging from 0 to 6.48, 0 to 0.57 and 0 to 22.2 mg (N) kg-1 of
dry soil and crust mass for NO3-, NO2- and NH4+,
respectively (Fig. 3a, Table S1 in the Supplement). In general, no
significant change in reactive nitrogen contents was found before and after
the trace gas exchange experiments, indicating no significant impact of one
wetting–drying cycle on the nutrient content. Bare soil samples had
significantly higher levels of NO3- and NO2- content
compared to dark, chlorolichen and moss BSC. Among the latter three, no
significant differences in nutrient levels were observed. Light BSC had
NO2- contents similar to bare soil. The NH4+ content was very similar in all samples, except for one outlier in
the group of light BSC with strongly elevated NH4+. Higher nitrate
and ammonium levels in bare soil compared to crust-covered samples were also
reported recently for a warm desert site in South Africa (Weber et al.,
2015), indicative of nutrient consumption–integration by the biocrusts.
Nitrite, however, was lower for bare soil samples compared to
biocrust samples. While NO3- was slightly higher, NH4+
and NO2- contents (especially of bare soil samples) were lower in
the South African arid ecosystem compared to Cyprus.
Chlorophyll was only determined in the samples used for flux measurements.
Chla ranged from 4.1 (bare soil) to 144.2 mg m-2 (moss BSC) and
Chla+b from 9.3 (bare soil) to 211.3 mg m-2 (moss BSC),
respectively (Fig. 3b, Table S1). From bare soil, via light BSC and
chlorolichen BSC II to dark BSC the chlorophyll content increased, but not
significantly (p > 0.2). Nevertheless, Chla and Chla+b
contents of chlorolichen BSC I and moss BSC were significantly higher than
those of bare soil, light BSC and chlorolichen BSC II (p < 0.05, Fig. 3b).
The range of chlorophyll contents is comparable to previous arid
ecosystem studies (Weber et al., 2015).
The pH of soil and biocrusts ranged between slightly acidic (6.2) and
slightly alkaline (7.6; Fig. 3c). The mean pH of 17 samples was 7.0, i.e.,
neutral. Only the pH of moss BSC samples was significantly lower than that
of bare soil, light BSC and chlorolichen BSC samples (p = 0.05). Soil and
biocrust samples from South Africa were slightly more alkaline (7.1–8.2)
with no significant difference among biocrust types (Weber et al., 2015).
HONO and NO emission fluxes as a function of soil water content.
Dotted lines are the mean fluxes. Shaded areas indicate the standard
deviation.
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NO and HONO flux measurements
All samples showed HONO and NO emissions during full wetting and drying
cycles. The calculations of the emission or flux rates are shown in the
Supplement. Maximum emission rates of HONO were observed at about 17–33 %
WHC and of NO at 20–36 % with no significant differences among all soil
cover types (Fig. 4). Emissions declined to zero at 0 % WHC and to very
small rates for > 70 %. Emission maxima strongly varied between
soil cover types but also between samples of the same cover type (see Figs. 4
and 5 and Table S1). The highest emissions of both HONO-N and NO-N were detected
for bare soil (175 ± 50.4 and 92.2 ± 20.0 ng m-2 s-1;
values indicate mean ± standard error), followed by light
(48.6 ± 24.3 and 44.0 ± 22.4 ng m-2 s-1) and dark BSC
(27.1 ± 16.1 and 26.5 ± 15.9 ng m-2 s-1). Both types
of chlorolichen- and moss-dominated biocrusts showed very low emission rates
of reactive nitrogen (on average < 10 ng m-2 s-1). Maximum
HONO emissions were somewhat higher than maximum NO emissions, especially for
bare soil. Integrating full wetting and drying cycles (6–8 h), 0.04–1.9 mg m-2
HONO-N and 0.06–1.6 mg m-2 NO-N was released (Fig. 5b). While the maximum fluxes of reactive nitrogen emission were higher
for HONO than NO, especially from bare soil, the integrated emissions were
similar or even larger for NO, which is released over a wider range of SWC.
Emission of HONO and NO from bare soil and biocrusts.
Panel (a) shows
maximum HONO-N and NO-N fluxes (ng m-2 s-1) at optimum water
conditions. Panel (b) shows emissions integrated over a whole wetting–drying
cycle (mg (N) m-2); letters show significant difference (p = 0.05, of
log-transformed data); error bars indicate standard error of the mean of
replicates (bare soil n= 3; light BSC n= 4; dark BSC n= 5; chlorolichen
BSC I n= 3; chlorolichen BSC II n= 6; moss BSC n= 4).
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In general, it is difficult to compare chamber flux measurements of different
studies due to different experimental configurations, such as chamber
dimension, flow rate, residence time, drying rate, etc. Here, we compared
our results to studies that applied the same method (with the same or very
similar conditions). The emission rates were consistent with the studies
in which HONO-N or NO-N emissions from soil between 1 and 3000 ng m-2 s-1
were found (Su et al., 2011; Oswald et al., 2013; Mamtimin et al., 2016; Wu
et al., 2014; Weber et al., 2015). Mamtimin et al. (2016) observed NO-N
fluxes of 57.5,
18.9 and 4.1 ng m-2 s-1 at 25 ∘C for soil of grape and cotton fields
and desert soil from an oasis in China, respectively. Oswald et al. (2013)
found HONO-N and NO-N emissions between 2 and 280 ng m-2 s-1
(each) from different soil from all over the world covering a wide range of
pH levels, nutrient content and organic matter. Biogenic NO emissions of 44 soil
samples from arid and semiarid regions were reviewed by Meixner and Yang (2006)
with N fluxes ranging from 0 to 142 ng m-2 s-1.
Correlation between maximum flux of HONO and NO and nutrient content
of all Cyprus soil and biocrust samples with Pearson correlation factors (of
log-transformed data; **: p < 0.001; *: p < 0.05).
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In contrast to the results of the present study, in which bare soil showed
the
highest emissions, Weber et al. (2015) found the lowest emissions from bare soil
in samples from South Africa. In that study, dark cyanobacteria-dominated
biocrusts revealed the highest emission rates (HONO-N and NO-N each up to 200 ng m-2 s-1),
followed by light cyanobacteria-dominated biocrusts (up
to 120 ng m-2 s-1), whereas in the present study, emissions of
dark cyanobacteria-dominated biocrusts tended to be lower. No significant
difference in HONO-N and NO-N emissions from light BSC between both sample
origins were found. HONO-N and NO-N emissions of moss- and
chlorolichen-dominated biocrusts were low in both studies (each < 60 ng m-2 s-1)
but still significantly higher for samples from South
Africa than from Cyprus. In the present study HONO maximum emissions were
higher than for NO (integrated emissions were comparable) while in the
study of Weber et al. (2015) HONO maximum fluxes were somewhat lower than
those of NO. The present results of nitrogen emissions correlated well with
the nutrient contents (especially NO2- and NO3-, Fig. 6).
Bare soil, in which the highest NO3- and NO2- levels were found,
also showed the highest HONO and NO emissions. A good linear correlation was
found between NO2- contents and emissions of both nitrogen gas-phase
species for all samples (R2=0.84 for HONO and 0.85 for NO;
p < 0.001). The level of correlation between NO3- and HONO and
NO was lower, but still significant (R2 = 0.68 and 0.67,
respectively; p < 0.001). Low correlations were found between HONO or
NO emissions and NH4+ contents (R2 = 0.165 and
0.232; p = 0.05). Thus, in the present study it seems that reactive nitrogen
emissions predominantly depend on NO2- and NO3- contents and
not on surface cover types, although biocrusts (especially with cyanobacteria
and cyanolichens) are able to fix atmospheric nitrogen (Belnap, 2002; Elbert
et al., 2012; Barger et al., 2013; Patova et al., 2016). The results of a
two-factorial ANOVA showed that HONO or NO emissions were not significantly
related to soil cover type but rather to nitrite content, i.e., its direct
aqueous precursor. For nitrate, the two-factorial ANOVA indicated
dependencies of both cover type and nutrient content. Long-range transport
and instantaneous atmospheric deposition
of NOx NO3-, NO2- and NH4+
can be excluded to be a dominant source of HONO and NO precursors in local
soil, as the observed concentrations in Cyprus ambient air were very low
(Meusel et al., 2016; Kleanthous et al., 2014). A dominant contribution from
microbial activity to the nutrient content is anticipated, although long-term
atmospheric accumulation of nutrients in the soil prior to the field campaign
cannot be excluded. While biocrusts increase nutrient availability via N
fixation, it is their possible associations with ammonia-oxidizing microbes
(bacterial and archaea) that finally convert the fixed nitrogen to nitrite
and nitrate. Determination of the microbial community below the biocrust or
in bare soil was not carried out as it was outside the scope of this study.
Nitrification and other nitrogen cycling processes are not restricted to
biocrusts and can also occur in non-crusted soils. The relevance of these
processes is expected to depend on substrate richness (i.e., amount of
ammonium available for nitrifiers). Our results differ from those obtained by
Weber et al. (2015) on South African samples, as their HONO and NO emissions
were not correlated with bulk concentrations of ammonium, nitrite and
nitrate. In their study nitrite content was lowest for bare soil compared to
other biocrust types. Ammonium and nitrite levels were also lower than in the
present study. Therefore, Weber et al. (2015) indicated that biocrusts can
enhance the N cycle and emission of reactive nitrogen.
Since most of the samples were slightly alkaline and only moss samples were
slightly acidic, no effect of pH could be observed. However, in general it is
expected that with higher nutrient and lower pH values HONO emission is
increased by simple partitioning processes (Su et al., 2011). The simulated
equilibrium concentration at soil surface [HONO]* (Eqs. S1 and S4 in Su et al.,
2011) is much lower than the measured one (see Fig. S3). This deviation is probably based
on the nonideal behavior of the soil samples (adsorption, Kelvin and solute
interaction effects on gas–liquid partitioning). However, this method does not
allow argumentation on physical or biological processes.
Comparison of soil emissions and observed missing source
To quantify the flux rate of HONO emissions from soil to the local
atmosphere and to compare it to the unaccounted-for source found in Cyprus in
2014 (Meusel et al., 2016), we applied a standard formalism describing the
atmosphere–soil exchange of trace gases as a function of the difference
between the atmospheric concentration and the equilibrium concentration at
the soil solution surface [HONO]* (Su et al., 2011):
F∗=vt([HONO]∗-[HONO]),
where [HONO] is the ambient HONO concentration measured on Cyprus (mean
daytime average 60 ppt) and [HONO]* is the equilibrium concentration at soil
surface. [HONO]* can be determined from measurements in a static chamber. In
a dynamic chamber system, there is a concentration gradient of HONO between
the headspace (where HONO was measured) and the soil surface. Here we used
the measurements of water vapor to correct for the soil surface
concentration and equilibrium concentration of HONO by assuming a similar
gradient for the two species. A correction coefficient of 3.8 was
determined, which is the ratio of the equilibrium relative humidity of 100 % over wet
soil surface to the initial headspace relative humidity of 25–30 % after inserting the
wet sample into the chamber. The transfer velocity, vt, depends
primarily on meteorological and soil conditions and is typically on the
order of ∼ 1 cm s-1. The flux rate of NO was calculated
accordingly with mean daytime NO concentrations of 38 ppt. The calculated
flux F*
was about (67 ± 3) % of the flux measured in the chamber.
The distribution of nine different surface cover types was mapped (Fig. 2),
including stones, vascular vegetation and litter not being attributed to
emit significant amounts of HONO and NO to the atmosphere. The residual HONO-emitting surface covers comprised 45.6 % of total surface in the
investigated area. Combining the information on soil–biocrust population and
the calculated flux F*, a site-specific community emission Fcomm of
HONO and NO can be estimated via following equation (Eq. 6).
Fcomm,max=∑itypeFmax,i∗⋅pi/100orFcomm,int=∑itypeFint,i∗⋅pi/100,
where Fcomm denotes the estimated community flux, Fmax,iorint,i∗
the maximum or integrated emission rates of each individual
surface cover type i (ng N m-2 s-1 or µg N m-2) and
pi the fraction of population type i (%).
Under optimum soil water conditions (20–30 % WHC) and constant temperatures
of about 25 ∘C, between 2.2 and 18.8 ng m-2 s-1 of total
HONO-N and between 1.6 and 16.2 ng m-2 s-1 of total NO-N are emitted from the
different crust–soil population combinations derived from the vegetation
cover assessment. In the lower range of total emissions the contribution from
bare soil dominates with up to 69 % (HONO) and 55 % (NO),
followed by moss BSC (HONO: 23 %; NO: 32 %). At high levels of total
emissions, the contribution from light BSC dominates (HONO: 43 %; NO:
49 %), decreasing the contribution of bare soil down to about 25 % (HONO)
and 13 % (NO). Emissions from dark BSC contribute about 20 or 24 % to
the total HONO or NO flux while the contribution from moss BSC decreases to
10 or 12 %. Emissions from chlorolichen BSC
do not play a significant role (< 2.4 %) in general
(see Fig. 7).
Contributions of different ground surfaces to the total F*.
![]()
After heavy rainfalls moistening the soil to full WHC,
11–113 µg m-2 of HONO-N and 10–131 µg m-2 of NO-N
can be calculated for one complete wetting–drying period. Assuming 30
rain events per year (based on the statistic of 4 years of precipitation data),
a wetting–drying cycle time of 7 days, and constant emissions in between
them (at 10 % WHC), up to 160 mg m-2 yr-1 of nitrogen can be
emitted directly by the sum of HONO-N and NO-N from Cyprus natural ground
surfaces, i.e., excluding heterogeneous conversion of NO2 on ground
surface.
The release of HONO from the ground surface to the atmosphere can be related
to the atmospheric HONO production rate via Eq. (7) (adapted from Su et al.,
2011) and then compared to the missing source.
Sground=Fcomm,max(T,swc)BLH⋅a,
with Sground as the HONO or NO emitted from ground surface; BLH the boundary
layer height (mixed layer height) and a the factor to convert nanograms of
nitrogen
into the number of
molecules (10-9 ⋅ 6.022 × 1023/14).
Diel pattern for HONO and NO emissions in comparison with the
observed HONO concentrations and missing source during the CYPHEX 2014
campaign. Panels (a, d) show observed concentration of HONO and NO in
black; missing source shown in pink. Panels (b, e) show mean surface temperature
and mean surface humidity measured in April 2016 in Cyprus and estimated
soil water content in red, green and blue, respectively. Panels (c, f)
show the calculated mean F* (mean temperature) with the shaded area indicating the lower and
upper limits.
![]()
During the CYPHEX campaign in summer 2014 a mean boundary layer height of 300 m a.g.l. was observed by means of a ceilometer. Due to missing
precipitation during CYPHEX, but high relative humidity prevailing (CYPHEX
2014: 75–100 %), a mean SWC
of 10 % WHC (at 25 ∘C) can be estimated (Likos, 2008; Leelamanie, 2010), reducing the HONO source
strength to 35 % of the emission maximum at optimum SWC. Integrating the
lowermost versus the uppermost observed HONO emissions per soil–crust type,
the emissions at 25 ∘C and a SWC of 10 % WHC would span a wide
range between 1.1 × 105 and 9.6 × 105 molecules cm-3 s-1,
covering 9 to 73 % of the missing mean source of 1.3 × 106 molecules cm-3 s-1
observed in the field (Meusel et al., 2016). However,
temperatures in the field have strong diel cycles, and a temperature increase
from 25 to 50 ∘C has been shown to lead to 6–10 times
higher emissions at constant SWC (Oswald et al., 2013; Mamtimin et al., 2016).
On Cyprus the observed soil surface temperatures changed from 10 ∘C
at
night up to 45 ∘C during the daytime (Fig. 8, red line, or
Fig. S2). In the natural habitat the micrometeorological parameters change in
concert, i.e., with increasing temperature the SWC decreases, influencing the
flux-enhancing effect of temperature. Based on the assumption of a linear
change of SWC with temperature, a diel course of the SWC between 6 and 14 %
of WHC is simulated (Fig. 8, blue line), lowering the emission flux
(22–49 % of optimum). Applying the described SWC dependence and the
temperature dependence on flux rates as reported by Oswald et al. (2013),
high daytime temperatures increase the simulated diel course of HONO-N flux
up to a daytime maximum of 7.4 ng m-2 s-1 (Fig. 8, lower panel), but
with a notable dip at high noon due to the opposing effect of decreasing SWC
at higher temperatures. The NO-N emissions show a similar pattern, with a
slightly lower flux range (up to 6.4 ng m-2 s-1). Converted into
production rates (Eq. 7), the ground-based soil and biocrust emissions at
noon would be up to 1.1 × 106 molecules cm-3 s-1 HONO-N and
0.9 × 106 molecules cm-3 s-1 NO-N covering up to 85 and
8.5 % of the missing HONO and NO source found during CYPHEX 2014 (Meusel et
al., 2016). Note that during CYPHEX there were two periods with lower relative humidity, in
which even a NO sink was detected. In some mornings of the campaign dew
formation was expected, causing an increase in soil humidity. Combined with
rising temperatures after sunrise, these optimized meteorological conditions
may have led to enhanced soil emissions and would confer a reasonable
explanation for the strong HONO morning peaks observed during the campaign.
Field observations (VandenBoer et al., 2013; Zhang et al., 2009; Tsai et al.
2017) as well as model results (Wong et al., 2013) showed that HONO
concentrations typically decrease exponentially from the surface upwards.
Equation (7) does not include a chemistry–transport model nor accounts for the
existence of a vertical profile of concentrations, which may bias the
calculation on HONO source strength. However, the method for predicting the ground
source using homogeneous mixed air columns is consistent with other recent
studies (Stemmler et al., 2006; Tsai et al., 2017). Tsai et al. (2017)
clearly showed the presence of an important ground source of daytime HONO at
a rural basin in Utah during winter (no snow, low temperatures). They
inferred that ground surface fluxes may account for 63 ± 32 % of the
unidentified HONO daytime source throughout the day. HONO-N fluxes of up to
7.4 ng m-2 s-1 (Fig. 8c) determined in this study are
comparable to HONO-N fluxes found in other regions, e.g., 2.7 ng m-2 s-1
reported for the northern Michigan forest canopy (Zhang et al.,
2009; Zhou et al., 2011), the average daytime HONO-N flux
of 7.0 ng m-2 s-1 measured over an agricultural field in Bakersfield (Ren et al.,
2011) and the average HONO-N flux of about 11.6 ng m-2 s-1
measured by Tsai et al. (2017). In contrast to the present study, the latter
concluded that, under the prevailing high NOx conditions, the respective HONO
formation was related to solar radiation and NO2 mixing ratios, such as
photo-enhanced conversion of NO2 or nitrate photolysis on the ground.
This can be ruled out in this study, as pure air (no NO2) was used to
purge the chambers and no light was applied. While in Cyprus the observed
soil emissions can explain high amounts of atmospheric HONO, other studies
excluded soil emission as a dominant source (Oswald et al., 2015; Laufs et
al., 2017). Oswald et al. (2015) studied soil samples from a boreal forest in
Finland and observed HONO emissions below the detection limit. However, those
samples had very low nutrient contents and were highly acidic (pH ≈ 3), for which microbial activity is supposed to be low (Fierer and Jackson,
2006; Persson and Wirén, 1995; Ste-Marie and Pare, 1999; Šimek and Cooper,
2002). Similarly, Laufs et al. (2017) did not find correlations
between HONO fluxes and temperature or humidity measured in the field and
concluded that HONO sources other than biological soil emissions must have dominated. In contrast to the SWC in Cyprus, the water
contents at the field site studied by Laufs et al. (2016) were higher than
the optimum SWC presented by Oswald et al. (2013).