Cold season soil NO fluxes from a temperate forest: drivers and contribution to annual budgets

Nitric oxide (NO) is a main precursor of tropospheric ozone (O₃) (Ludwig et al 2001), which is an important short-lived greenhouse gas (GHG) and a key compound affecting the oxidizing capacity of the troposphere (Delon et al 2008, Steinkamp et al 2009). Sources of tropospheric NO are not only energy generation processes, but also soils. NO emissions from soils have been reported for agriculturally managed and natural ecosystems. Emissions are a result of microbial and physicochemical soil N cycling processes (Schindlbacher et al 2004, Medinets et al 2015). Despite that NO fluxes from soils are generally low (<2–10 kg NO-N ha⁻¹ yr⁻¹), the large areal extent of agricultural land and forests results in a significant contribution of soils to regional and global budgets (Butterbach-Bahl et al 2009, FAO 2015). Therefore, for further improving estimates, an accurate assessment of the magnitude and drivers of soil NO fluxes is required.

In recent years understanding of the diverse abiotic and biotic NO sources and sinks in soil has increased considerably (Medinets et al 2015, Heil et al 2016), and resulted in improvements of process descriptions in biogeochemical models (Butterbach-Bahl et al 2009, Pilegaard 2013). However, the uncertainty of annual soil NO budgets from temperate ecosystems is still considerable as NO fluxes from soil during the non-vegetation period are rarely quantified (Yao et al 2010, Kim et al 2012, Medinets et al 2016).

During the cold season, low soil temperatures decrease the activity of soil microorganisms and accordingly the process rates of microbial N transformations. Therefore, cold season soil NO fluxes were often considered as negligible (Yao et al 2010, Kim et al 2012, Medinets et al 2016). It, however, has been shown that cold season soil carbon dioxide (CO₂) fluxes contribute significantly to the annual soil C budget (e.g., Chen et al 2013, Schindlbacher et al 2014) and that nitrous oxide (N₂O) fluxes from soil can even peak during the cold season (e.g., De Bruijn et al 2009, Filippa et al 2009, Goldberg et al 2010, Yanai et al 2011). Therefore, microbial breakdown of organic matter and associated N cycling during the cold season could result in significant fluxes of NO. If cold period emissions are not accounted for, annual NO fluxes from ecosystems which experience seasonal climate may be underestimated.

There is evidence of significant NO emission during freeze/thaw periods in temperate cropland and grassland soil (Yao et al 2010, Laville et al 2011). Cold season NO emission pulses were observed from arable soil in Southern Ukraine (Medinets et al 2016) and from snow-covered soils in temperate and polar regions (e.g. Peterson and Honrath 2001, Davis et al 2004, Helmig et al 2009). While most of these studies are covering one or two seasons (Helmig et al 2009, Kim et al 2012, Medinets et al 2016), longer time series are required for a better quantification of the cold season soil NO contribution to annual budgets and for a determination of emission drivers and controls.

Here we use the unique soil NO flux measurements of the Höglwald Forest research site covering 16 years for characterizing cold season NO fluxes. Postulating that the dynamics of soil NO fluxes at the Höglwald Forest are representative of forest soil NO fluxes in the temperate zone, we hypothesize that (i) forest soils in temperate continental climate zones have significant NO fluxes during the cold season, (ii) soil NO emissions increase with soil temperatures and peaks occur during freeze-thaw periods, (iii) that NO emissions are more closely correlated with soil N₂O than soil CO₂ emissions.

2.1. Study site

2.2. Flux measurements

2.3. Soil and meteorological measurements

2.4. Definition of the cold season and freeze/thaw period

2.5. Seasonal and annual NO budgets

2.6. Statistical analysis

3.1. Meteorology during the cold season

3.2. Cold season NO, N₂O and CO₂ fluxes

3.3. Contribution of cold season NO fluxes to annual soil NO budgets

In seven out of 15 years the number of missing data was <20%, which was considered to be sufficient to accurately assess the contribution of the cold period to annual soil NO emission budgets (figure 1). The average cumulative cold period NO flux was 1.8 ± 0.7 kg NO-N ha⁻¹. For these years the total annual cumulative soil NO flux (warm and cold period fluxes) ranged between 7.3–10.2 kg NO-N ha⁻¹ with an average of 8.5 ± 1.0 kg NO-N ha⁻¹. The mean contribution of cold periods to the annual NO budget was 22.3 ± 10.2% with a minimum of 12.8% in 2005/06 and a maximum of 41.3% in 1994/95 (figure 1).

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Significant positive relationships between mean NO flux and mean cold season air temperature (r² = 0.69, p < 0.05; figure 2(b)) as well as less significant between individual year cold season NO flux and duration of the cold season (r² = 0.43, p < 0.1; figure 2(a)) could be demonstrated. While a negative dependence of time normalized (monthly) quantity of frost events (r² = 0.56, p < 0.05; figure 2(c)) on cold season NO flux was observed, a show significant relationship of cold season NO flux with snow cover was not existing.

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3.4. Relationship between soil NO flux and environmental drivers

Hourly variations in soil NO fluxes for the entire cold season dataset significantly (p < 0.001) positively correlated with air (r² = 0.17), organic layer (r² = 0.18; figure 3(a)) and mineral soil temperatures (r² = 0.12). Similar relationships were found for the entire cold season data set, if fluxes observed during freeze-thaw events were excluded. There were no correlations between soil NO fluxes and soil moisture content (SMC) at both organic and mineral soil layers for the whole cold season observation period. However during periods of freeze-thaw events positive relationships were observed (organic layer SMC: r² = 0.08, p < 0.05 and mineral layer SMC: r² = 0.27, p < 0.0001).

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3.5. Relationships between soil NO fluxes and soil fluxes of N₂O and CO₂

Fluxes of NO and CO₂ had similar positive response to soil temperature increase (figure 3(a)) resulting at cross-correlation between those fluxes (r² = 0.10, p < 0.0001; figure 4(a)). NO and N₂O fluxes were not correlated (figure 4(a)) across the entire cold season, though during freeze-thaw events (figure 4(b)) NO flux correlated with N₂O flux (r² = 0.28, p < 0.0001) and was weakly related to CO₂ fluxes (r² = 0.10, p < 0.0001) too.

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Cold season NO flux contributed on average 22% (1.8 kg NO-N ha⁻¹) to the total annual NO budget at our observation site the Höglwald Forest. Postulating that the forest is representative for the dynamic of soil NO fluxes of temperate forests this confirms our hypotheses (i) that temperate forest soils can emit significant amounts of NO during the cold season. The contribution of cold season NO flux to the annual budgets varied considerably between years (13%–41%) and was positively correlated to the duration of the cold seasons and the mean cold season air temperatures. This suggests that, cold season NO emissions were higher in years with longer lasting cold periods during spring and/or autumn (periods, which fell below the <3 °C threshold in our study) and that such periods should not be ignored when measuring soil NO fluxes. The lowest contribution of cold season NO emissions (13%–17%) occurred in those seasons where mean air temperature was below zero (range: −1.8 to −1.0 °C) and frost periods were well above 71 days (table 2, figure 1). This suggests that soil NO emissions during short and cold winters were comparatively low. Nevertheless, even during these years, cold season emissions still contributed more than 10% to the annual budget and therefore should not be treated as negligible.

At the Höglwald Forest cold season NO emissions were mostly larger than the N₂O fluxes in this period. Soil NO emissions showed a positive relationship to soil temperature (confirming hypotheses (ii)), an observation which is in line with previous studies (e.g., Ludwig et al 2001, Butterbach-Bahl et al 2004, Laville et al 2011, Medinets et al 2016). However none of these studies had specifically focused on the cold periods. Contrary N₂O fluxes did not correlate significantly with soil temperature, but responded very distinctively to freeze thaw cycles (figure 3(b)). The very large freeze thaw emission peaks as for N₂O (e.g., Luo et al 2012) were not observed for NO (rejecting hypotheses (iii)). But, freeze-thaw cycles, did raise NO emissions slightly above background (figure 4(b)).

Thawing frozen soil increases the soil moisture content and thereby rehydrates microbial and plant cells, mobilizes and releases soil nutrients and stimulates the metabolic activity of dormant microbial communities (Kemmitt et al 2008, De Bruijn et al 2009, Kim et al 2012). All of these activities can lead to soil NO and N₂O emission pulses (Yao et al 2010, Laville et al 2011, Yanai et al 2011, Kim et al 2012). During freeze-thaw in our study, N₂O fluxes significantly exceeded NO fluxes. Due to the relatively minor contribution of freeze-thaw events to the overall cold season period and the comparatively small freeze-thaw impact on NO emissions, freeze-thaw did not significantly affect the magnitude of the overall cold season NO emission. This is further confirmed by the inverse relationship of the number of frost events with cold season NO fluxes (figure 2(c)). This suggests, that the quantity and duration of the frozen period, which is an important aspect for N₂O pulse emissions (Papen and Butterbach-Bahl 1999, De Bruijn et al 2009, Wu et al 2010, Yanai et al 2011) had an opposite impact on NO flux by lowering its release in absolute values compared to the rest of the cold season. As freeze-thaw seems quantitatively less important regarding NO emissions, but also with regard to soil CO₂ emissions (Luo et al 2012), cold season NO emissions correlated with cold season soil CO₂ flux (figure 4(a)), which showed the typical dependency on wintertime soil temperature (Schindlbacher et al 2014).

In spite of snow cover not being identified as a driver for cold season NO fluxes, snow cover may reduce NO release to the atmosphere. Snow melting causes topsoil over-saturation by water (Wolf et al 2012), which restricts gas diffusion and thereby also suppresses immediate NO release (Kiese and Butterbach-Bahl 2002, Mu et al 2012, Wu et al 2014). Furthermore, following snow melt soils often do not reach WFPS optimum conditions for NO release (Wu et al 2014). Whilst, abiotic transformations of NO occurring in snowpack and between snow and air which are possible and still not completely understood. E.g., Medinets et al (2016) observed weak net uptake of NO during snow cover periods at an agricultural site in the Ukraine. However, contradicting results have been published with regard to NO fluxes from snow covered soils as i) according to Henry's constant for NO (Sander 2015), it does not interact with snow (Bartels-Rausch et al 2013) and soil originated NO can be emitted via snowpack to the atmosphere (e.g., Helmig et al 2009), ii) snow is considered as a source of NO (France et al 2012) which can be produced via photolysis of ${{{\rm{NO}}}_{2}}^{-},$ NO₂ and ${{{\rm{NO}}}_{3}}^{-}$ as a by-product together with NO₂ (Seok et al 2015 and references therein). With our chamber design, we measured trace gas fluxes from/ to the snow surface and it therefore was not possible to distinguish if the NO was produced in the soil or in the snow layer. However, since NO efflux was similar during snow free periods and periods with snow cover (at similar soil temperatures), we attribute the NO production primarily to soil processes. With this regard, it also should be noted that our chamber system operated only until snow depth of max. 15 cm. We therefore, occasionally, had to remove snow to keep this 15 cm threshold. As the mean snow depth at our site was (ca. 4.6 cm) and snow depth exceeded the threshold of 15 cm depth for only 1.6 days per year on average, we do not expect the snow removal having any significant effect on annual NO budgets. It is further noteworthy, that other reported NO fluxes from snow covered soil and from the snowpack itself are low 0.25–0.40 μg NO-N m⁻² h⁻¹ (Helmig et al 2009; high elevation alpine forest) and 0.21–0.35 μg NO-N m⁻² h⁻¹ (France et al 2012; onshore and offshore coastal Alaskan snowpacks), when compared to the mean cold season flux from snow covered soil (31.2 ± 9.9 μg NO-N m⁻² h⁻¹) at our temperate forest site, which in turn was 1.7 time lower than the average cold season flux (53.0 ± 15.7 μg NO-N m⁻² h⁻¹). Overall, our results indicate that snow cover itself plays a less dominant role in regulating cold season soil NO emissions at the temperate forest studied. As snow cover is mostly shallow, frost can penetrate the topsoil even during periods of snow-cover. This may be one reason for the poor relationship between snow cover and NO emissions. However, a further decrease of snow cover depth and snow cover duration, ahead with concurrent climate warming (Kreyling and Henry 2011, Klein et al 2016), is thus unlikely to lead to colder soils in a warmer world (Groffman et al 2001) but to result in warmer soils and higher soil NO emissions.

We conclude that cold season soil NO emissions can contribute significantly to the annual NO emissions of a temperate forest soil. Therefore, cold season emissions should not be neglected in annual emission budgets of these ecosystems. Compared to N₂O, NO showed little response to freeze-thaw and NO emissions were not distinctively affected by snow cover. Since cold season NO fluxes showed a strong positive relationship to air and soil temperature, these environmental drivers should receive priority, when modeling NO fluxes during winter.

We gratefully acknowledge funding of 2 projects 'Wintertime Emission of Nitric Oxide from Soil' (WTENOS) and 'Relationships between soil N₂O and NO Emission under Freeze-Thawing Events' (REFTE) from the Transnational Access to Research Infrastructures activity in EC 7th Framework Programme 'The Experimentation in Ecosystem Research' (ExpeER, Grant Agreement No. 262060) project, and support from the 'Effects of Climate Change on Air Pollution Impacts and Response Strategies for European Ecosystems' (ÉCLAIRE) project funded under the EC 7th Framework Programme (Grant Agreement No. 282910).