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Published online 27 October 2006
Published in Soil Sci Soc Am J 70:2106-2113 (2006)
DOI: 10.2136/sssaj2006.0085
© 2006 Soil Science Society of America
677 S. Segoe Rd., Madison, WI 53711 USA
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Soil & Water Management & Conservation

New Method to Simulate Soil Freezing and Thawing Cycles for Studying Nitrous Oxide Flux

Q. C. Hua, E. van Bochoveb, Jon Warlanda, Bev Kaya and C. Wagner-Riddlea,*

a Dep. of Land Resource Science, Univ. of Guelph, Ontario, Canada N1G 2W1
b Soils and Crops Research and Development Center, Agriculture and Agri-Food Canada

* Corresponding author (cwagnerr{at}uoguelph.ca)


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Field experiments are essential for elucidating the processes involved in N2O production during soil freezing/thawing (FT) cycles, but laboratory simulations can provide the advantage of controlled conditions. Past studies have used disturbed or undisturbed soil cores placed in a controlled temperature environment, so that FT occurred from the external surface to the inside of the core (omni-directional method, OD). A new method of soil FT for simulating field conditions more closely in the laboratory was developed and its effect on N2O fluxes evaluated. Three methods were examined: OD, uni-directional (UD) with the soil column surrounded by filled-in soil, and a variant of UD with water accessible to the base of the core (UDW). The rate of soil cooling with time was significantly faster and similar at all depths (–0.29°C h–1) for OD, than for UD or UDW methods (–0.16°C h–1 at 1 cm, –0.10°C h–1 at 20 cm). This differential cooling resulted in a significant change in soil temperature with depth for UD and UDW methods 0.125°C cm–1 during freezing and –0.35°C cm–1 during thawing, but of only 0.04 and –0.02°C cm–1 for the OD method. Comparison with field temperature data indicated that the UD and UDW method more closely resembled the gradual top-to-bottom freezing of soil layers that occurs in field conditions (changes of –0.20°C h–1 at 1 cm; –0.05°C h–1 at 20 cm). Gravimetric water content in the frozen layer 0 to 20 mm in the UDW (60.6 g kg–1) was significantly higher than in UD (44.4 g kg–1) and OD (37.6 g kg–1) soil columns. Fluxes of N2O during thawing were significantly affected by the incubation method used, probably due to the intensity and duration of freezing, and the water content prevalent under each method with OD (13 ng N2O-N m–2 s–1) > UDW (4.8 ng N2O-N m–2 s–1) > UD (2.1 ng N2O-N m–2 s–1). We conclude that the UD (and UDW) method allows for manipulation of FT in soil columns gradually layer-by-layer providing the conditions needed to link the site of N2O production in the soil profile with surface N2O fluxes in laboratory studies.

Abbreviations: FT, freezing and thawing • OD, Omni-directional freezing and thawing • UD, Uni-directional freezing and thawing with the soil column surrounded by filled-in soil • UDW: uni-directional freezing and thawing with filled-in soil and water accessible to the base of the core


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
BOTH N2O AND CO2 are greenhouse gases that are emitted by terrestrial ecosystems (Duxbury et al., 1993), and contribute to the enhanced atmospheric greenhouse effect (IPCC, 2001). Increased gas fluxes from thawing frozen soil were first observed in the 1960s (Soulides and Allison, 1961; McGarity, 1962; Mack, 1963). In recent years, research has focused on the importance of N2O and CO2 fluxes during soil thawing for annual emissions (Skogland et al., 1988; Christensen and Tiedje, 1990; Wagner-Riddle and Thurtell, 1998; Müller et al., 2002). Skogland et al. (1988) showed that CO2 fluxes increased nearly threefold after soil thawing when compared with that before freezing. The N2O emissions from agricultural soils during spring thaw have been shown to account for up to 70% of total annual emissions (Wagner-Riddle et al., 1997; Röver et al., 1998). However, the soil processes that lead to high N2O and CO2 fluxes at thawing are still not well understood.

Laboratory methods used to simulate the effect of FT on gas production have included the FT of small columns containing either disturbed, sieved, or undisturbed soil cores. In what we term the ‘omni-directional’ (OD) procedure, columns were placed in a controlled temperature environment with FT temperature applied in sequence to the external surface of the cores (Soulides and Allison, 1961; McGarity, 1962; Mack, 1963; Skogland et al., 1988; Wang and Bettany, 1993; Koponen et al., 2004; Teepe et al., 2004). Teepe et al. (2001) and Wagner et al. (2003) froze soil columns from one end of the column by using a cooling coil, but the frozen soil was thawed completely from all directions. In these laboratory studies, typical soil water and temperature profiles as encountered in field conditions under FT cycles have not been realistically simulated. In field conditions, soil freezing and then thawing, occur mainly and gradually from the soil surface to deeper layers according to the surface energy budget and heat transfer through the soil profile. Thawing also occurs upward from the bottom of the frozen layer induced by ground heat (Ferguson et al., 1964). As soil water freezes, water redistribution occurs via water migration from unfrozen soil by liquid flow (Ferguson et al., 1964; Konrad and Morgenstern, 1980) and to a lesser extent by vapor diffusion (Yershov, 1998). The existence of a water table in field conditions influences both the water content and the water potential in the unfrozen soil above it.

The objectives of this study were: (i) to develop a microcosm system to simulate the gradual soil FT from the top to the bottom of soil columns including a simulated water table, (ii) to compare the effect of different laboratory freezing methods on soil temperature, water content profiles, and N2O fluxes during FT cycles.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Soil
Undisturbed soil columns (length 25 cm) were collected by gently tapping a hammer on a steel ring over PVC tubing in April 2003 using PVC tubing (10 cm ID, length 26.5 cm) from plots that have been under no-tillage in a corn-soybean-winter wheat rotation at the Elora Research Station, Ontario, Canada, since 2000. The previous crop was winter wheat that had received 60 kg N ha–1 during the growing season of 2002. Wheat residue present on the soil surface was left on the surface of collected soil columns. These were sealed in plastic bags and stored at 4°C until the microcosm system was set up. The soil at the experimental site is a Conestogo silt loam (Gray Brown Luvisol). The soil consists of 29% sand, 52% silt, and 19% clay. Total organic C and NO3––N contents in the 0- to 15-cm soil layer at the time of soil column collection were 31 g kg–1 and 15 mg kg–1, respectively.

Microcosm System
The microcosm system was made from three small styrofoam household coolers without lids (33 cm [H] x 40 cm [L] x 29 cm [W]), in which PVC columns containing soil were placed. The coolers were put in a walk-in freezer with a temperature control range from –10 to 25°C. Each cooler was used to incubate four undisturbed soil columns. A plastic board (4 mm thick) was placed in the cooler at 2 cm from the bottom, to support the soil columns and to allow for the simulation of a water table (Fig. 1 ). If water was present at the bottom of the cooler, it was transported to the soil columns via cotton wicks fitted through holes that were drilled through the board.


Figure 1
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  		Fig. 1. Schematic diagram of the microcosm system containing four soil columns used for freezing-thawing cycle simulation. 1. Cooler; 2. PVC column; 3. Undisturbed soil; 4. Filled soil; 5. Cotton wick; 6. Water; 7. Tubing for adding water; 8. TDR probe; 9. Thermocouple; 10. Plastic board; 11. Pad supporting plastic board. Note: The filled soil was not present in the omni-directional method; water was only present in the UDW method; and only two soil columns are seen but two other columns were present behind the columns shown.

 
The FT treatments studied were (1) OD, which consisted of placing soil columns vertically in the cooler without any material between the columns and without a water table; (2) UD, in which the space between the vertically placed columns was filled with soil but without a water table; (3) uni-directional FT with soil between the columns and water (2 L) present in the bottom of the cooler (UDW) (Fig. 1). The soil used to fill the spaces between soil columns was collected at the same site where soil columns were obtained, and had a gravimetric water content and bulk density similar to the soil in columns, 30 g kg–1 and 1.35 g cm–3, respectively. The OD method reproduced the approach that has been used in previous laboratory studies of N2O fluxes as affected by FT cycles. The UD and UDW were a variation of the same method (with and without a water table present), where the soils packed around the columns had the intention of making FT occur within the column in a one-dimensional manner, to mimic field conditions more closely than the OD method. The water present in the bottom of the cooler in UDW method provided a source for water to migrate to the frozen layer in liquid and/or vapor form.

Two FT cycles were simulated. The freezer available for this study required manual setting of desired temperatures. In the first FT cycle, the temperature in the freezer was set to –4°C for 27 h, and then to –10°C for 18 h. Thereafter, the temperature in the freezer was adjusted to 10°C for 32 h. In the second FT cycle, the freezer temperature was adjusted to –10°C for 7 h, and then 20°C for 3 h followed by 15°C for 10 h. These FT cycles were chosen somewhat arbitrarily to compare the temperature variation inside the soil columns in each method. The ‘cooling’ and ‘warming’ phase of the first FT cycle mimic changes in hourly air temperature that may occur over the course of <24-h field conditions (i.e., from +5 to –10°C, from –10 to +10°C), but due to the manual nature of the temperature setting, the laboratory changes were step-changes and hence, more abrupt than expected under field conditions.

Thermocouples and TDR probes (7.5 cm length) were inserted through holes in the PVC column at 1-, 5-, 9-, and 20-cm depths in one soil column for each freezing treatment. Silicone was used to seal the holes. Thermocouples were connected to a multiplexer and datalogger placed outside the freezer, which recorded the hourly average temperature. The TDR probes were connected to a TDR instrument (Topp and Davis, 1985) and volumetric water content was measured at the time of gas sampling during the thawing cycles as these probes only measure liquid water content and not frozen water content.

Soil and Gas Analysis
During the first freezing cycle, approximately 20 g of frozen soil from the 0-to 20-mm layer of each soil column was sampled at 35 h from the start of the first FT cycle (46 h after the start of the experiment), and separated into 0- to 5-, 5- to 10-, 10- to 15-, 15- to 20-mm layers using a knife. Approximately 20 g of unfrozen soil with similar water content as at the start of the incubation was used to refill the sampling location. We only sampled the 0- to 20-mm layer to not disturb the soil columns during the N2O flux measurement period. It was assumed that replacement of the small amount of soil (20 g) did not affect N2O fluxes. Water contents for each sampled soil layer were determined using the gravimetric method.

Nitrous oxide fluxes from the soil columns were determined using the closed chamber method. The chamber consisted of a 5-cm height PVC cap with a 3.3-cm height PVC section with the same diameter as the PVC column (10 cm ID) glued into its interior. An O-ring (10 cm in diameter, 0.2 cm thick) was placed at the edge of the 3.3 cm height PVC section. The chamber was placed on the 1.5 cm height PVC wall protruding from the soil column. Consequently, the height of the chamber was 5 cm and the total headspace volume of the chamber was 3.925 x 10–4 m3. A rubber septum located at the top of the chamber allowed for gas sampling. Petroleum jelly and a rubber bungee cord were used to ensure a good seal between chamber and soil column.

Gas samples were taken during the periods of soil FT cycles. Each time, after a chamber was placed over the soil column, the headspace air was sampled after 1 h. In a field experiment using chambers at the same site where soil cores were collected, N2O concentrations in the headspace were found to increase linearly over 1.5 h during the winter period. Gas samples of 7.5 mL were obtained from the headspace using a syringe and injected into 6-mL glass vials to be analyzed for N2O by gas chromatography with an automatic sample injector system in the laboratory of Soils and Crops Research Center, Agriculture and Agri-Food Canada as described in van Bochove et al. (2000). The N2O concentration in ambient air (Ca) of the freezer was subtracted from the N2O concentration in the air trapped in chamber (Ct) to give net N2O flux over 1 h ({Delta}t) from soil column surface (s):

Formula 1[1]
where v denotes volume of chamber.

Statistics
The water content and N2O flux data were first tested for normal and random distribution using the Shapiro-Wilk and Restricted Maximum Likelihood test. The significance of treatment was conducted using the ANOVA method (SAS Institute, 1999). The multiple comparisons for the data were tested with the Least Significant Difference (LSD) (P ≤ 0.05).


   RESULTS AND DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS
 REFERENCES
 
Temperature and Soil Water Content
The soil temperature patterns with depth during FT cycles were significantly affected by the methods studied (OD, UD, and UDW) (Fig. 2 ). At 5-cm depth, the temperature fell below 0°C after 4, 16, and 22 h for OD, UD, and UDW, respectively, after setting the freezer to –4°C. The lowest temperature at 5-cm depth during the first FT cycle was significantly lower for OD, when compared with UD or UDW (–8.1 vs. –2.0°C). During the thaw sequence, the temperature exceeded 0°C at 5-cm depth after 4, 8, and 10 h of setting air temperature to 10°C for the OD, UD, and UDW treatments, respectively. During the first FT cycle UD and UDW methods showed a distinct change in soil temperature with depth with differences between surface and 20 cm of 0.125°C cm–1 at 50 h (cooling phase) and –0.35°C cm–1 at 79 h (warming phase). In contrast, the OD method had a smaller change in soil temperature with depth with 0.04°C cm–1 at 50 h and –0.02°C cm–1 at 79 h. With soil columns placed in an empty cooler (OD method), temperatures at all depths changed quickly and were similar at the end of each FT period. The rapid change of soil temperature across the layers has been observed in most laboratory studies on soil FT using a similar OD method (Koponen et al., 2004; Teepe et al., 2004). In this method, the atmospheric temperature influenced the soil temperature directly at all depths in the soil column, causing the column to cool or warm in all directions nearly simultaneously. In contrast, methods UD and UDW showed a gradual decrease or increase of soil temperature, with cooling or warming occurring from top to bottom of the soil profile.


Figure 2
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  		Fig. 2. Soil temperature at different depths in soil columns incubated according to methods: (a) omni-directional, (b) uni-directional with filled-in soil, and (c) uni-directional with filled-in soil and water present in the bottom of cooler over two soil freezing-thawing cycles, as indicated with air temperature.

 
It is difficult to compare directly laboratory soil temperature obtained from imposed air temperature changes with field results, as solar radiation, and snow cover play an important role in the magnitude of soil temperature response. We selected two periods from field experiments at the same site where soil columns were collected, to illustrate that soil temperature changes over time and with depth obtained with UD (and UDW, data not shown) method simulated field conditions at our site more closely than the OD method (Fig. 3 ). In response to a 15°C drop in air temperature (DOY 3 to 5), field soil temperature at 1 and 20 cm changed –0.20 and –0.05°C h–1, respectively, and resulted in a temperature difference of 0.12°C cm–1 between 20 and 1 cm (Fig. 3a). A similar decrease in air temperature in the laboratory (–14°C over 45 h), resulted in a soil temperature change at 1 cm of –0.29°C h–1 for OD and –0.16°C h–1 for UD, while at 20 cm the change was also –0.29°C h–1 for OD, but at a lower rate for UD (–0.10°C h–1). The temperature difference between 20- and 1 cm-depth was 0°C cm–1 for OD, but closer to field conditions for UD at 0.13°C cm–1. During thawing (DOY 84 to 86) the increase in soil temperature, particularly at 20 cm, was delayed for UD when compared with OD, but still was faster than in field conditions (Fig. 3).


Figure 3
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  		Fig. 3. Air and soil temperature at two depths in the profile at the Elora Research Station, Ontario, Canada, over two calendar days early in January 2004 (DOY 3 to 5), and in March 2004 (DOY 84 to 86). For comparison purposes air and soil temperature measured in the laboratory experiment using (a) the omni-directional method, and (b) uni-directional with filled-in soil method over a cooling (left graphs) and warming cycle (right graphs) are superimposed on the field data, which for clarity is repeated in the top and bottom graphs. The field site is the same where soil columns for the laboratory experiment were collected in April 2003.

 
The subzero temperature in the soil columns resulted in redistribution of soil water during soil freezing. Total gravimetric water content in the 0- to 20-mm soil layer increased significantly after 46 h from the start of the experiment compared with the initial moisture content of 30 g kg–1, with UDW (60.6 g kg–1) > UD (44.4 g kg–1) > OD (37.6 g kg–1) (Fig. 4 ). Migration of water from unfrozen soil to frozen soil occurs when soil undergoes freezing (Ferguson et al., 1964). Omni-directional freezing in the OD soil columns (Wagner et al., 2003) meant that water migrated radially rather than vertically, as the columns froze from the outside to the middle. This limited water migration to the top layer of the soil columns, resulting in the lowest water content in the 0- to 20-mm layer in OD columns (Fig. 4).


Figure 4
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  		Fig. 4. Mean gravimetric water contents in the 0- to 20-mm frozen soil layer of omni-directional (OD), uni-directional (UD), and uni-directional with filled-in soil and water accessible to the base of the core (UDW) soil columns after freezing but before thawing at 46 h after the start of the experiment. Bars indicate standard error of mean. Bars with the same letter indicate means across soil depths are not significantly different at P ≤ 0.05.

 
Continuous water supply in the UDW soil column resulted in the highest water content observed (Fig. 4). In addition, the gradual freezing of soil layers from ‘top to bottom’ in the profile of UD and UDW methods resulted in water movement to the surface layers, as can be seen by comparing water content of 10- to 20-mm layer and 0- to 10-mm layer in UD method (Fig. 4). Measurement of water content using TDR during the first soil thawing period (57 to 81 h) gave a mean volumetric water content in the 0- to 20-cm soil column of 0.33, 0.35, and 0.39 m m–3 for OD, UD, and UDW, respectively. Water contents were quite constant (< ±0.05 m m–3) throughout the soil column over the thawing period as melting water was redistributed. However, OD and UD soil columns showed a decrease in water content as the soil profile warmed (from initial volumetric water content of 0.40 m m–3), while the water at the bottom of the UDW columns ensured a steady supply to the soil matrix.

Nitrous Oxide Flux
Different values of N2O fluxes among OD, UD, and UDW were found in this simulation (Fig. 5 ). Although mean N2O fluxes during freezing (3–50 h) were small (<0.6 ng N2O-N m–2 s–1), and not significantly affected by the incubation method, fluxes increased during thawing and were significantly higher for OD (13 ng N2O-N m–2 s–1) than that from both UD and UDW. Mean flux of N2O from UDW column also was significantly higher than that from UD column during this period (4.8 ng N2O-N m–2 s–1 vs. 2.1 ng N2O-N m–2 s–1). Fluxes increased significantly after the first thaw was started (51 h), and temperature at 1 cm increased above 0°C. For the OD method, fluxes stayed above 10 ng N2O-N m–2s–1 for the remainder of the experiment, decreasing for a brief period during the second freezing cycle. In contrast, soil columns incubated under the UD and UDW methods had shorter thaw emission episodes, lasting only 14 h for UD (until 70 h, Fig. 5), and until 93 h for UDW.


Figure 5
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  		Fig. 5. Mean N2O fluxes (bars show standard error of mean) for soil columns incubated according to method: (a) omni-directional, (b) uni-directional with filled-in soil, and (c) uni-directional with filled-in soil and water present in the bottom of cooler over two soil freezing-thawing cycles, as indicated with soil temperature at 1 cm (solid line) and 20 cm (dashed line).

 
From the soil temperature and water content profiles it is clear that the FT cycles resulted in very different conditions in the soil columns depending on the incubation method used. These conditions led to contrasting N2O emissions from the soil columns. The method resulting in most freezing in the soil column (OD) had the highest fluxes during thawing. Previous studies have shown that duration and intensity of freezing affect N2O fluxes in the subsequent thaw period. Wagner-Riddle and Thurtell (1998) observed that field N2O fluxes were higher following longer freezing periods. In a laboratory study, Teepe et al. (2001) measured larger N2O emissions during a second FT cycle due to its higher intensity of freezing and duration, although part of these emissions occurred during soil freezing, which was not observed in our study. In another study, freezing of soil columns for 2.4 vs. 11.5 d increased the N2O emissions by two- to five-times depending on water filled pore space (WFPS) as affected by soil texture (Teepe et al., 2004). Interestingly, the maximum N2O flux following the 2.4 d-freezing period using an OD method was ~30 ng N2O-N m–2 s–1 (Teepe et al., 2004), which is in the range of maximum flux observed in this study (Fig. 5).

The lower N2O fluxes during thawing for UD and UDW methods can be attributed to the lower intensity and duration of freezing, although water content seems to have played a role as well. Öquist et al. (2004) observed a significant increase in potential N2O production when incubating soil samples with water content > 60% of the soil's holding capacity at temperatures below zero. A readily available supply of water in the UDW method allowed for higher moisture content of the frozen soil layers (Fig. 4) when compared with UD method, and likely resulted in the higher fluxes observed (Fig. 5). It is interesting to note that the freezing intensity and duration effect on fluxes during thawing from OD soil columns appeared to ‘over-ride’ the effect of lower water content of these columns. Another potential explanation for the higher N2O fluxes during thawing of OD, compared with UD and UDW soil columns, is the rapid increase in soil temperature throughout the profile once the first thawing phase was started. Mean soil temperature in the OD column reached 10°C at 80 h (Fig. 2), which was significantly higher than 6°C in UD and 4.6°C in UDW columns. This higher temperature combined with a larger overall volume of thawed soil water (due to the larger volume of frozen soil) could have caused the higher N2O emissions in OD columns.

Several processes for explaining the burst in N2O fluxes due to winter freezing and spring thawing have been proposed: (1) microbial activity enhanced by available C from freezing lysis (McGarity, 1962; Christensen and Tiedje, 1990) and disintegrating aggregates (Edwards and Killham, 1986; van Bochove et al., 2000); (2) the release of N2O trapped in unfrozen water film by ice (Teepe et al., 2001; Koponen et al., 2004); (3) the physical release of N2O produced during winter and trapped at depth in unfrozen soil as the ice barrier melts (Bremner et al., 1980; Burton and Beauchamp, 1994); and (4) N2O production triggered by water from melted snow, accumulated in the top layer due to the presence of a frozen layer (Nyborg et al., 1997; Lemke et al., 1998). That is, increased fluxes triggered by thawing are believed to be either due to stored N2O that is released during melting, and/or due to ‘new’ N2O produced as the soil layers thaw. Knowledge of the relative importance of these two mechanisms is important for greenhouse gas mitigation and modeling efforts. Linking the site(s) of N2O production in the soil profile to the temporal dynamics of surface N2O fluxes is needed to elucidate the processes at work. The UD method (and its variant UDW) provides a laboratory incubation approach by which FT in soil columns could be manipulated to occur gradually layer-by-layer, as opposed to the ‘bulk’ approach of the OD method. Instrumentation of the soil columns with soil gas probes and an open-chamber approach, combined with tunable diode laser spectroscopy for continuous measurements of N2O concentrations (Brown et al., 2000) could provide the data needed for this analysis.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
REFERENCES
 
A new microcosm system was designed to simulate the field conditions during soil FT, to study soil process and gas emission under laboratory conditions. The method proposed (UD) is simple and based on undisturbed soil columns, which are placed in a larger volume of similar thermal characteristics (cooler with filled-in soil), and may have access to water at depth (UDW). This method was effective in producing gradual FT cycles in soil columns, from top to bottom or vice-versa, closer to field conditions than the OD method. Fluxes of N2O were significantly affected by the incubation method used probably due to the intensity and duration of freezing, and the water content prevalent under each method. We suggest that the UD (and UDW) method provides the conditions needed to link the site of N2O production in the soil profile with surface N2O fluxes in laboratory studies.


   ACKNOWLEDGMENTS
 
This project was funded by the BGSS program managed by CARC and Agriculture and Agri-Food Canada under the Canadian Climate Change Action Fund initiative. We acknowledge G. Thériault and N. Goussard from AAFC for analysis using gas chromatography.

Received for publication February 22, 2006.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS
 REFERENCES
 





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