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Article

Natural Nitrogen Isotope Ratios as a Potential Indicator of N2O Production Pathways in a Floodplain Fen

by
Mohit Masta
1,
Holar Sepp
2,
Jaan Pärn
1,
Kalle Kirsimäe
2 and
Ülo Mander
2,*
1
Department of Geography, Institute of Ecology and Earth Sciences, University of Tartu, Vanemuise 46, 51003 Tartu, Estonia
2
Department of Geology, University of Tartu, Institute of Ecology and Earth Sciences, Ravila 14a, 50411 Tartu, Estonia
*
Author to whom correspondence should be addressed.
Water 2020, 12(2), 409; https://doi.org/10.3390/w12020409
Submission received: 30 December 2019 / Revised: 23 January 2020 / Accepted: 31 January 2020 / Published: 4 February 2020
(This article belongs to the Special Issue Wetlands in Action: Sustainable Water Management and Resource Recovery)
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Abstract

:
Nitrous oxide (N2O), a major greenhouse gas and ozone depleter, is emitted from drained organic soils typically developed in floodplains. We investigated the effect of the water table depth and soil oxygen (O2) content on N2O fluxes and their nitrogen isotope composition in a drained floodplain fen in Estonia. Measurements were done at natural water table depth, and we created a temporary anoxic environment by experimental flooding. From the suboxic peat (0.5–6 mg O2/L) N2O emissions peaked at 6 mg O2/L and afterwards decreased with decreasing O2. From the anoxic and oxic peat (0 and >6 mg O2/L, respectively) N2O emissions were low. Under anoxic conditions the δ15N/δ14N ratio of the top 10 cm peat layer was low, gradually decreasing to 30 cm. In the suboxic peat, δ15N/δ14N ratios increased with depth. In samples of peat fluctuating between suboxic and anoxic, the elevated 15N/14N ratios (δ15N = 7–9‰ ambient N2) indicated intensive microbial processing of nitrogen. Low values of site preference (SP; difference between the central and peripheral 15N atoms) and δ18O-N2O in the captured gas samples indicate nitrifier denitrification in the floodplain fen.

1. Introduction

Floodplains and other riparian ecosystems are important buffers controlling water quality and providing several other ecosystem services [1]. However, beside their water purification and habitat provision roles, riparian zones can be significant sources of greenhouse gas (GHG) emission [2]. Periodically flooded floodplains are a significant source of nitrous oxide (N2O), a powerful GHG and a major ozone-depleting gas [3,4,5]. N2O is produced in soil via nitrification under aerobic conditions, where ammonia is oxidized, and by denitrification, which occurs under anaerobic conditions, where nitrate is sequentially reduced to nitrite, NO, N2O, and pure molecular nitrogen (N2) [6]. The gaseous nitrogen losses directly depend on soil moisture, which affects oxygen availability in the soil. Hence, understanding the relationship between soil moisture, oxygen content, and N2O emissions is highly important to understand N2O production and consumption mechanisms in floodplains.
The effect of draining or flooding on nitrous oxide emissions has been studied in several studies. N2O emissions follow a bell-shaped distribution with the peak at intermediate soil moisture [7]. Experiments show that variation in soil oxygen content induces high N2O emissions [8]. Lower soil nitrate levels have been observed during the flooding periods, whereas a peak in N2O emissions followed by a sudden drop has been observed as an after-effect of flooding [9]. These short-lived peaks, which were recorded when the water table was below soil surface, are also found to be a major source of global N2O emissions. When the soil was continuously and completely submerged, N2O emissions dropped significantly [6,7,10,11].
For understanding the N2O production, analysis of isotopic signatures has been developed in the past decades [12]. The N2O molecule has an asymmetric structure (N-N-O) and the two N atoms are distinct referred to as beta (β) and alpha (α)-NβNαO [12]. It has also been shown that there is a preference for enrichment of 15N at the central (α) position of the N2O molecule in atmosphere [13]. The ground state zero-point vibrational energy of 14N15N16O is less than 15N14N16O, which is why formation of the former is favoured over the latter under equilibrium conditions [14]. Also, the 14N-16O is reduced more easily as compared to 15N-16O, due to its low bond strength [15]. The enrichment of 15N at the central (α position) of the N2O molecule has been observed during nitrification and denitrification [16,17]. Moreover, studies conducted with pure cultures of microbes producing N2O have observed high site preferences (expressed as SP = δ15Nα – δ15Nβ) for nitrification and low site preferences of ~0‰ for bacterial denitrification respectively [18,19,20,21,22]. High site preference has also been observed in fertilized arable soils indicating autotrophic nitrification [23]. Contrary to these results, there have also have been studies that have shown non-uniform site preference during denitrification conditions, which creates a dilemma on answering the question of whether site preference can be used as a tool to differentiate between nitrification and denitrification [24,25,26,27,28].
The majority of 15N analyses related to N2O fluxes have been made in mineral soils, and only a limited number of studies consider peat soils. For instance, Rückauf et al. (2004) [29] performed 15N tracer experiments in drained and reflooded microcosms filled with fen peat and found that denitrification was the main N transformation process, whereas N2O emission from reflooded (anoxic) conditions was significantly lower than that from drained microcosms. Similar results were gained in field studies by Tauchnitz et al. (2015) [30] with 15N tracer studies on nitrogen gases released from a transition bog and found high N2O and low N2 from drained conditions and the reversed situation in rewetted cases. Likewise, Yang et al. (2011) [31] found significantly higher emission from drained soils with oxic conditions, using field-based 15N-N2O pool dilution technique to measure gross N2O production in soil. However, the natural isotope composition of N2O to differentiate between nitrification and denitrification source processes has not been studied before in floodplain peats.
The objective of this study is to analyze the impact of water table depth and oxygen content on N2O production pathways in a drained nitrogen-rich floodplain fen using experimental flooding and the natural isotope composition of N2O.

2. Materials and Methods

2.1. Site Description

We collected gas samples from three positions in a drained fen in the floodplain of the Emajõgi River, Estonia (58°25′41.0′′ N 26°30′30.3′′ E; 58°25′38.2′′ N 26°30′45.6′′ E and 58°25′35.5′′ N 26°31′02.8′′ E) between 5 October and 12 November 2018. The positions differed in distance from the river, soil moisture, and oxygen concentration (Figure 1). We collected the gas samples from chambers to glass vials of 50 ml for gas analysis and 100ml for gas-isotope analysis. The chambers were organized in equilateral triangles. The side of the equilateral triangle was 1.6 meters. White 65-litre chambers were used on top of the collars to trap the gas emitted from the soil. Observation wells were placed to read the water table. The three positions were labelled as A, B, and C depending on their distance from the river. Position C was closest to the river and A was farthest away with B at the centre. During one-hour sessions, samples were collected after every 20 min and ten such sessions were conducted for this study. Position C was flooded with ditch water for 2 h before collecting samples using a garden pump to achieve anoxic conditions. Oxygen sensors (Fibox 4 by PreSens, Regensburg, Germany) were placed at depths of 5 cm, 25 cm, and 50 cm for a vertical oxygen profile at all three sampling positions. Soil temperature was monitored at all positions in each session at depths of 10 cm, 20 cm, 30 cm, and 40 cm. Soil samples were collected from at different depths.

2.2. Soil and Gas Isotope Analysis

Soil samples were collected at various depths. For bulk nitrogen isotope analysis, samples were dried to remove moisture and 1 milligram of each was packed into a tin capsule. Soil samples were then analyzed using a Delta V Plus mass spectrometer coupled with a Flash HT element analyser (Thermo Scientific, Bremen, Germany) in the Isotope Ratio Mass Spectrometer laboratory at University of Tartu. Nitrogen isotopes were calibrated against IAEA-N1 and IAEA-N2 international standards. Analytical precision was better than ±0.2‰. Soil chemical analysis was done at the Estonian University of Life Sciences. 100 mL of NH4+—acetate solution was paired with titanium-yellow reagent. A flow injection analyser was used to determine plant-available magnesium (Mg2+). To analyse available calcium (Ca2+), the flame photometrical method was used with the same solution. Soil pH was calculated on a 1N KCl solution and flow-injection analysis was used on a 2M KCl extract of soil to determine soil NH4-N and NO3-N. Oven-dried samples were used to determine total nitrogen via dry combustion method on a varioMAX CNS elemental analyzer (manufacturer: elementar, Langenselbold, Germany). Organic matter of oven-dry soil was calculated by loss on ignition at 360 °C. Soil bulk density was calculated considering that peat consists of organic matter, mineral matter, and water. Individual bulk densities of 0.23, 2.65, and 1 g/cm3 for mineral matter, organic matter, and water, respectively, were used to calculate the bulk density of each peat sample [32,33].
Gas-phase N2O concentrations were measured using a gas chromatograph equipped with an electron detector (GC-2014, Shimadzu, Kyoto, Japan). Soil gas N2O isotopomer ratios (bulk nitrogen δ15Ngas), and 15N site preference (SP) were concentrated and purified on a modified PreCon [34] and GasBench II and analyzed on a Delta V mass spectrometer (Thermo Scientific: Waltham, MA, USA) (Figure 2). We replaced the viton seals with rubber rings in PreCon and also bypassed the oven. We removed the sample loop in the GasBench II and used the same ports to connect PreCon, and used 100 ml sample bottles. For mass 31 measurements we used higher amplification (3.00 × 1011) according to Potter et al. [35]. The isotope and site preference values were calculated according to Toyoda and Yoshida [12] and calibrated against standard reference gas.
Isotopomer ratios were noted as δ values defined as:
δ15Ni = R15samplei/R15standard−1 (i = α, β, or bulk)
The 15Rα and 15Rβ are the 15N/14N ratios at central (α) and terminal (β) nitrogen position in the linear N2O molecule, respectively. 15Rbulk denotes the average value of 15N/14N ratios. Standard is an international standard of atmospheric N2 for N. The 15N site preference was calculated from isotopomer ratios as SP = δ15Nα − δ15Nβ. The δ values and SP value are expressed in per mil (‰). The standard deviations of the measurements were 0.3‰ for δ15Nbulk and 0.9‰ for δ15Nα.
Conversion of measured ratios into isotopomers ratios was done using the following equations [12]
45R = 15Rα + 15Rβ + 17R
46R = 18R + (15Rα + 15Rβ) 17R +15Rα 15Rβ
31R = 15Rα + 17R
32R = 18R +15Rα 17R
Here 45R and 46R represent the isotopomers of N2O that contribute to mass 45 and 46, 17R represents the heavy oxygen and 31R and 32R correspond to isotopomers of NO.

3. Results and Discussion

3.1. N2O Emissions Varying with Soil Chemistry

Soil properties of all the three positions at different depths are reported in Table 1. Our results for the C/N ratio show similarly low values among the three positions, ranging from 9% to 11%. Hence at our experimental site the variability of N2O emissions must depend significantly on other factors such as water table depth and oxygen concentration, and not only on C/N ratio. Klemedtsson et al. (2005) [36] have shown that at C/N ratios > 20, N2O emissions are low irrespective of other physical factors such as pH, water table, and soil oxygen content but when C/N ratios are low they affect N2O emissions. Our results showed a negative trend N2O emissions and bulk density. Leifeld (2018) [37] found similar results. Liu et al. (2019) [38] found a positive correlation between bulk density and N2O emissions, which is in contradiction with our results. The concentrations of ammonium and nitrate increased from position A to C, without a trend with N2O emissions. This indicated that inorganic nitrogen was not a driving factor responsible for the N2O emissions. Organic matter content increased from position A to B and then decreased from position B to C, but due to similar C/N ratios, we expect it would not affect the N2O emissions. No strong trends were observed between site preference and soil chemistry factors such as bulk density and C/N ratio. Also, according to the World Reference Base for Soil Resources (2007), soils containing 12% or more carbon are classified as peat. In our experimental site, all three positions had more than 12% of carbon and hence could be classified as peat [39].

3.2. N2O Emissions Varying with Water Table

In response to changing water table depth, the N2O emissions showed two maxima at water levels between −40 and −50 cm, and when the soil was submerged (Figure 3). Dobbie et al. (2001 and 2003) [9,40] have also observed similar trends in their experiment where they have shown an increase in N2O emissions with increasing water-filled pore space (WFPS) [9,40,41]. Furthermore, Goldberg et al. (2009) [42] have observed that N2O in fen peat is mostly produced at depths between 0.3 and 0.5 m. Also, it has been shown that the emissions peak at one optimum point and are at the lowest in dry or saturated soil [43,44]. This is similar to the soil-moisture optimum observed worldwide [7]. We also observed temporal variation of emissions from each position. High spatial and temporal variability of fluxes seems to be typical for N2O and has been observed in both mineral and organic soils [7,8,9,27,30,37,38,40]. Characteristically large temporal variations of N2O emissions have also reported in a review paper by Henault et al. (2012) [45].

3.3. N2O Emissions Varying with Flooding Time.

The N2O emissions were observed to increase after the flooding over 80 minutes, after which a sudden drop was observed in N2O emissions and emissions remained low at longer flooding times (Figure 4A). This also explains the high N2O emissions observed during the positive water table as when the flooding process would begin, it would take some time to achieve anoxic conditions and during this time some N2O bursts or peaks were observed. Hansen et al. (2014) [46] have observed a similar trend in agricultural soils where emissions increased after flooding until a maximum at a certain flooding time and after that decreased with a steep fall [46]. Similar trends have also been observed in rice paddies in Indonesia and China [47,48].

3.4. N2O Emissions Varying with Oxygen Content

Under anoxic conditions (0 mg O2/L), most of the N2O emissions were low (Figure 4B). This could indicate reduction of N2O to N2 due to a lack of oxygen. From the suboxic peat (0.5–6 mg O2/L) emissions were high and showed a peak at oxygen content of 6 mg/L. From the oxic peat (6–12 mg O2/L), N2O emissions were lower than from the suboxic peat but higher than from the anoxic peat. Vor et al. (2003) [40] and Rubol et al. (2012) [8] show similar trends in N2O emissions where suboxic or intermediate oxygen content results in the highest N2O emissions from the soil [10,49,50]. Furthermore, Zhua et al. (2013) [51] have also shown that as conditions approach an anoxic nature, heterotrophic denitrification is the major active process [51]. This coheres with our results and hypothesis and is further confirmed by the isotope results below.

3.5. Variation of Soil δ15Nbulk soil

The δ15N values of total soil nitrogen showed low δ15N (‰ air N2) values with little variation with depth at position B, possibly due to its suboxic nature (Figure 5). However, in flooded position C there is a decreasing δ15Nbulksoil trend with peat depth in the upper part of the section, which starts to increase again from the soil depth of 40 cm. This might be due to the flooding effect. In contrast, at position A, the δ15Nsoil values increased with soil depth to 30 cm, after which the δ15Nsoil decreased. The increasing trend of δ15Nsoil has also been observed by Brenner et al. (2001) [52] during their study in grasslands in California. They indicated soil inputs such as soil roots, as the cause for this trend [52]. However, as the flooding process was conducted for a time span of over a month, during which ten sessions were conducted in our experiment, the microbial activity due to fluctuating water table depth and oxygen content could have been responsible for the enrichment of heavy nitrogen isotope during this time. Increased δ15N values have also been observed in forest soil by Snider et al. (2009) [53].

3.6. δ15Ngas and Site Preference in N2O

Both total N2O emissions and δ15N values of the gas samples were highest at the water table depth of −40 to −50 cm (Figure 3). Schmidt et al. [16] have explained a decrease in heavy isotope at the central position of the N2O molecule with increase of water table depth. The 15Nα enrichment trend in our data was similar to the total N2O emissions showing an optimum around the −40 cm water table (Figure 3). The increasing enrichment (Figure 3) is in coherence with the results found by Sutka et al. [21] who observed an increase of δ15Nα produced by denitrifying bacteria with depletion of soil oxygen. SP values were negative (Figure 6A). This, with negligible N2O emission (Figure 4B) and high soil 15N abundance (Figure 5) indicated denitrification. In the suboxic peat the negative SP, high N2O emissions and low soil 15N abundance indicated incomplete denitrification.
Most of the earlier studies on N2O site preference observed an increasing trend for site preference vs. N2O oxygen isotopic composition [54,55,56,57] though no clear trend was observed between the oxygen isotope composition of N2O and site preference under heterotrophic denitrification in pure bacterial cultures [21]. Interestingly in our suboxic peat (Pos B) site preference increased with δ18O (Figure 6B). The positive relationship between site preference and δ18O has been observed by a few studies focused on denitrification in soils [53,58]. Under the varying soil oxygen status, heavy oxygen enrichment was higher than heavy nitrogen enrichment, showing significant correlation (Figure 6C). This can be considered as one of the indicators of denitrification as the dominant producer of N2O in the floodplain fen. Similar trends have been observed by Menyailo et al. (2006) [59] in their study of Siberian soils under denitrifying conditions. In our study, low values of site preference (SP; difference between the central and peripheral 15N atoms) and δ18O-N2O in the captured gas samples indicate nitrifier denitrification in the floodplain fen (Figure 6B,C). This is also supported by the findings in relevant publications on N2O production pathways [60,61,62].
Fluctuating water table in riparian zones [56] and floodplain fens [63] is a natural phenomenon that is increasing N2O emissions. Agricultural use and climate change in floodplain fens will intensify N2O losses and therefore, mitigation measures are necessary. Poyda et al. (2016) [64] propose to avoid arable use of floodplain fens. A productive three-cut system grassland would yield the lowest emission rate from high groundwater (long-term mean < 20 cm below the surface) [64]. For northern Europe, climate change models forecast increasing precipitation sum and more frequent climate events (floods and droughts; IPCC, 2014) [4], wherefore the range of water-table fluctuation will be most likely increasing in floodplains. Therefore, adaptation strategies and mitigation measures are becoming increasingly important. Using nuclear techniques will be helpful to understand processes and identify N2O sources. That is necessary for the further development of mitigation measures [65].

4. Conclusions

In the anoxic floodplain fen peat, N2O emission was low. Accumulation of the heavy nitrogen isotope in the soil, low values of site preference, and δ18O-N2O in the captured gas samples indicate nitrifier denitrification in the anoxic floodplain peat. In the suboxic peat the isotopic signals were similar but N2O emissions were high, indicating that the denitrification was incomplete. Further investigation should focus on distinguishing N2O production pathways using microbial analysis (metagenomic and qPCR approaches) and labelled 15N techniques. This is important for better regulation of land use in floodplains to mitigate N2O emissions.

Author Contributions

Conceptualisation: Ü.M., K.K. and J.P.; M.M., J.P. and Ü.M. conceived and designed the experiments; M.M. and J.P. performed the experiments; H.S. and M.M. performed the gas, water and soil analyses and analysed the data; M.M. and Ü.M. made visualisations; K.K. contributed materials and analysis tools; M.M. wrote the draft; K.K., J.P., Ü.M. and M.M. corrected and edited the paper. All authors have read and agreed to the published version of the manuscript.

Funding

The research was supported by the Ministry of Education and Research of Estonia (IUT2-16 and PRG-352 grants), the EU through European Regional Development Fund (ENVIRON and EcolChange Centres of Excellence, and the MOBTP101 returning researcher grant by Mobilitas+), and the Estonian Centre of Analytical Chemistry (AKKI). The methodological groundwork for the study was laid by IAEA’s Coordinated Research Project (CRP) on “Strategic placement and area-wide evaluation of water conservation zones in agricultural catchments for biomass production, water quality and food security”.

Conflicts of Interest

The authors declare no conflict of interest.

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Water 12 00409 g001 550
Figure 1. Study site view showing varying ground water level and peat depth at Kärevere in Tartu, Estonia.
Figure 1. Study site view showing varying ground water level and peat depth at Kärevere in Tartu, Estonia.
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Figure 2. Schematic for the instrumentation of continuous flow measurements for nitrogen isotopes in gas.
Figure 2. Schematic for the instrumentation of continuous flow measurements for nitrogen isotopes in gas.
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Figure 3. Total N2O emissions and δ15Nα enrichment in N2O versus water table. In flooded conditions, fluxes depend on O2 concentration changing with flooding time. The parabolic trendline of N2O emissions is shown (R2 = 0.08; p < 0.05).
Figure 3. Total N2O emissions and δ15Nα enrichment in N2O versus water table. In flooded conditions, fluxes depend on O2 concentration changing with flooding time. The parabolic trendline of N2O emissions is shown (R2 = 0.08; p < 0.05).
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Figure 4. (A) N2O emissions varying with flooding time from three chambers per session at Position C (see Figure 1). (B) Variation of N2O emissions with varying oxygen content showing anoxic, suboxic, and oxic zones.
Figure 4. (A) N2O emissions varying with flooding time from three chambers per session at Position C (see Figure 1). (B) Variation of N2O emissions with varying oxygen content showing anoxic, suboxic, and oxic zones.
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Figure 5. δ15N ‰ values of the bulk soil varying with position and soil depth. Position (Pos) B has the lowest N2O-N emission values (see Figure 4B).
Figure 5. δ15N ‰ values of the bulk soil varying with position and soil depth. Position (Pos) B has the lowest N2O-N emission values (see Figure 4B).
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Figure 6. (A) Variation of site preference in gas samples in relationship with soil oxygen concentration. Position (Pos) A has anoxic conditions, Positions B and C are suboxic and oxic, respectively. (B) N2O SP (site preference) vs. δ18O relationship for all measurements. (C) N2O isotopic signatures showing variation of δ18O vs. δ15N.
Figure 6. (A) Variation of site preference in gas samples in relationship with soil oxygen concentration. Position (Pos) A has anoxic conditions, Positions B and C are suboxic and oxic, respectively. (B) N2O SP (site preference) vs. δ18O relationship for all measurements. (C) N2O isotopic signatures showing variation of δ18O vs. δ15N.
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Table
Table 1. Soil properties at Kärevere field site. DM—dry matter.
Table 1. Soil properties at Kärevere field site. DM—dry matter.
Position and DepthBulk Density g/cm3DM %pHKClOrganic Matter %Total Carbon %N %NH4-N mg/kgNO3-N mg/kgC/N Ratio
A 0–10 cm1.549.05.522.712.71.33.25.710.1
A 10–20 cm1.859.15.915.88.80.91.916.09.9
A 20–30 cm1.861.96.112.67.00.72.114.410.0
A 30–40 cm2.071.76.47.74.30.41.211.410.7
B 0–10 cm1.135.45.751.028.52.65.114.110.9
B 10–20 cm1.135.36.151.929.02.85.515.010.5
B 20–30 cm1.130.46.054.530.42.86.528.810.7
B 30–40 cm1.130.26.255.831.22.910.135.110.6
B 40–50 cm1.128.66.547.626.62.43.628.210.9
C 0–10 cm1.444.15.230.116.81.55.520.611.0
C 10–20 cm1.652.85.120.911.71.22.929.19.5
C 20–30 cm1.859.85.012.36.90.72.611.69.5
C 30–40 cm1.442.54.929.216.31.56.045.010.7
C 40–50 cm1.751.45.115.48.60.82.819.511.0

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MDPI and ACS Style

Masta, M.; Sepp, H.; Pärn, J.; Kirsimäe, K.; Mander, Ü. Natural Nitrogen Isotope Ratios as a Potential Indicator of N2O Production Pathways in a Floodplain Fen. Water 2020, 12, 409. https://doi.org/10.3390/w12020409

AMA Style

Masta M, Sepp H, Pärn J, Kirsimäe K, Mander Ü. Natural Nitrogen Isotope Ratios as a Potential Indicator of N2O Production Pathways in a Floodplain Fen. Water. 2020; 12(2):409. https://doi.org/10.3390/w12020409

Chicago/Turabian Style

Masta, Mohit, Holar Sepp, Jaan Pärn, Kalle Kirsimäe, and Ülo Mander. 2020. "Natural Nitrogen Isotope Ratios as a Potential Indicator of N2O Production Pathways in a Floodplain Fen" Water 12, no. 2: 409. https://doi.org/10.3390/w12020409

APA Style

Masta, M., Sepp, H., Pärn, J., Kirsimäe, K., & Mander, Ü. (2020). Natural Nitrogen Isotope Ratios as a Potential Indicator of N2O Production Pathways in a Floodplain Fen. Water, 12(2), 409. https://doi.org/10.3390/w12020409

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