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DIVISION S-3-SOIL BIOLOGY & BIOCHEMISTRY

Effects of Freeze–Thaw and Soil Structure on Nitrous Oxide Produced in a Clay Soil

Soils and Crops Research and Development Centre, Agriculture and Agri-Food Canada, 2560 Hochelaga Blvd., Sainte-Foy, QC, Canada G1V 2J3

vanbochovee{at}em.agr.ca

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Freezing and thawing have been shown to cause significant soil physical and biological changes. The increase in denitrification following thawing may be attributed to the diffusion of organic substrates newly available to denitrifiers from disrupted soil aggregates. The objective of this study was to evaluate the effect of freezing and thawing on N₂O production in a clay soil under contrasting crop rotations and tillage practices. Laboratory experiments were conducted in soil slurries to favor substrate diffusion, in macroaggregate fractions separated by wet sieving to characterize the biologically active soil organic matter (SOM) pool, and in undisturbed soil cores to simulate field conditions. In slurries, a freezing and thawing cycle increased denitrification rates by 32%. Soil slurries from no-tillage under rotation (NT–R) exhibited denitrification rates 92% higher than those from conventional till under continuous cereal (CT–C). Macroaggregates fractions (0.25–2 and 2–5 mm) from both management systems increased their rates of C mineralization and denitrification activity by 95% following freezing, but the increases tended to be greater (57%) in small than in large macroaggregates. Higher rates of denitrification (55%) found in both aggregate fractions of NT–R system were attributed to the higher mineralizable organic C content. Undisturbed soil cores sampled in November showed increased N₂O production by 220% after thawing. This thawing effect was also significantly higher in cores from NT–R than in those from CT–C.

Abbreviations: CT–C, conventional till under continuous cereal • DEA, denitrification enzyme activity • DR, denitrifying rate • GC, gas chromatography • NT–R, no-tillage under rotation • OM, organic matter • SOM, soil organic matter • WSA, water-stable aggregate distribution

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
NITROUS OXIDE is a radiactively active atmospheric trace gas with a long lifetime (150 yr) and is currently accounting for 2 to 4% of total greenhouse warming potential (Watson et al., 1992). Cultivated soils are thought to be a major source of anthropogenic N₂O (Duxbury et al., 1993). Although the critical environmental factors responsible for N₂O emissions are well understood, sources and sinks of N₂O in agricultural soils are not yet fully quantified. One reason for this incomplete information is the lack of measurements in various agricultural systems (Mosier et al., 1996), especially during winter (Röver et al., 1998). Bremner et al. (1980) estimated that 6 to 21% of the annual N₂O flux from agricultural land occurred during thawing of topsoil in spring. In cold temperate climates (e.g., Canada and northern Europe), some studies reported significant N₂O losses from cultivated soils following freeze–thaw cycles in spring (Nyborg et al., 1997; Wagner-Riddle and Thurtell, 1998; Röver et al., 1998) or even during winter and snowmelt from unfrozen soils (van Bochove et al., 1996, 2000). The processes involved in N₂O emissions during freeze and thaw are unclear, although several factors have been investigated (Röver et al., 1998). In Québec, Canada, seasonal variations in denitrification enzyme activities (DEA) were observed and significant DEA were measured in the coldest months of the year (Pelletier et al., 1999).

Thawing causes the disruption of soil structure, mostly of macroaggregates, and enhances microbial activity due to the release of organic C from plant and microbial detritus (Christensen and Christensen, 1991). The relationships between disruption of soil macroaggregates and availability of readily mineralizable substrates for denitrification may play an important role in the potential of a soil to produce N₂O during a freeze–thaw event. Consequently, management-induced changes in aggregation may modify the denitrification potential of a soil. In fact, different long-term soil cropping and tillage practices have significant effects on the water-stable aggregate distribution (WSA) of macroaggregates (Tisdall and Oades, 1980; Elliott, 1986; Angers et al., 1993b). Among these practices, no-till increases aggregate stability and C and N content (Cambardella and Elliott, 1993; Angers and Carter, 1996). Stable macroaggregates are relatively enriched in labile C of recent origin (Elliott, 1986; Puget et al., 1995).

However, reduced tillage also reduces total soil porosity (Pagliai and De Nobili, 1993) and increases soil moisture content (Rice and Smith, 1982), a factor known to restrict O₂ diffusion through soil. The presence of an anaerobic microsite at the center of soil aggregates is critical for the occurrence of denitrification (Sexstone et al., 1985).

Under circumstances of specific soil management practices, freeze–thaw cycles may cause physical disruption of soil structure, diffusion of soluble C, and changes in soil porosity that may promote denitrification and episodic N₂O emissions. Under the Québec climate, in fall, agricultural soils undergo overnight freeze and thaw cycles. We performed various incubations in the laboratory to investigate the effect of freeze–thaw cycles on N₂O production in soils under contrasting agricultural practices. Three types of incubations were carried out as follows: (i) soil slurries to determine denitrification activities in conditions that remove substrate diffusion constraints, (ii) fractions of macroaggregates to characterize the biologically active pool of SOM that may be associated with N₂O production, (iii) soil cores to evaluate N₂O production in conditions where diffusion is a function of the undisturbed soil structure.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Field Site and Soil Sampling
Cultivated plots were located at the Agriculture and Agri-Food Canada Experimental Farm at La Pocatière, Québec, on a Kamouraska clay (Orthic Humic Gleysol). The long-term experimental plots were arranged in a split-plot design with four replicates. Crop sequence treatment was the main plot treatment and tillage practice was the subplot treatment (Angers et al., 1993a). Two treatments with contrasted cropping–tillage combination treatments were selected: (i) no-tillage with a 2-yr barley (Hordeum vulgare L.)–red clover (Trifolium pratense L.) rotation (NT–R) in the second year of rotation and (ii) conventional till moldboard plowing with continuous barley (CT–C).

For incubation in slurries and on macroaggregates, three replicate soil samples (0–5 cm depth) were cored randomly from each plot on 5 Oct. 1995.

For incubation of the undisturbed soil structure, soil cores were collected in three replicates from each plot at the 0- to 5-cm depth on two sampling dates, 5 Oct. and 27 Nov. 1995. Stainless steel corers (i.d., 11 cm; height, 10 cm) were sharpened at one end and soil cores were collected with a driver system that allows a precise core of 5-cm depth.

Incubation Experiments
Denitrification Rate in Slurries
Sieved soil samples (6 mm) were frozen at -12°C for 20 to 24 h and then thawed for 25 min. Unfrozen controls were kept at 4°C before incubations started. After freezing–thawing simulation, denitrifying rate (DR) was determined on four subsamples of each soil sample. The DR incubations were conducted at 25°C under anaerobic conditions in the presence of 10% acetylene (C₂H₂). Assay solution contained 10 mM NO^-₃ to provide nonlimiting electron acceptor. Glucose and chloramphenicol were not added to the solution (modified from Martin et al., 1988). The C₂H₂ was purified by bubbling successively through solutions of H₂SO₄ (2 M) and deionized water (Nanopure series 851 system, Barnstead/Thermolyne, Dubuque, IA) to remove traces of acetone. Gas samples were collected in vacutainers (Vacutainer Brand, Becton Dickinson and Co., Rutherford, NJ) at 0.5, 2, and 4 h after the incubation vessels were sealed. Incubation vessels were not shaken during incubation to minimize aggregates breaking.

Incubations of Macroaggregate Fractions
Prior to macroaggregate fractionation by wet sieving, soil samples were gently passed through a 6-mm sieve and kept at 4°C in crush-resistant air-tight containers. Field-moist soil samples were wetted under vacuum and constant head at 5 cm H₂O during 30 min to minimize slaking of aggregates during wet sieving following the method of Le Bissonnais (1989). The separation into two macroaggregate size fractions (0.25–2 and 2–5 mm) was performed using an apparatus similar to that described by Bourget and Kemp (1957); operating conditions were 3.7-cm stroke at 29 cycles s^-1 during 10 min. After wet sieving, macroaggregate fractions were equilibrated under constant head at 10 cm H₂O. Soil water content was determined gravimetrically on each fraction, small macroaggregates (0.42 kg kg^-1) were wetter than the large ones (0.30 kg kg^-1). Aggregate fractions were divided into subsamples to measure (i) N₂O and CO₂ production during anaerobic incubation for denitrification following a freeze–thaw simulation and (ii) mineralization rate of organic C during aerobic incubation.

Anaerobic Incubations for Denitrification
Macroaggregates were confined in polyvinyl chloride cores (i.d., 5 cm; height, 3 cm) that were placed in 125-mL air-tight jars before freezing treatment at -12°C for 18 to 24 h. Unfrozen soil controls were kept at 4°C. After 20 min for thawing, the headspace of frozen and unfrozen jars was flushed with N₂, and C₂H₂ (10%, v/v) was injected in jars to measure denitrification. Anaerobic N₂O and CO₂ accumulations were monitored during 3 h at 25°C using gas chromatography (GC) as described below.

Aerobic Incubations for Carbon Mineralization
Aerobic CO₂ production was estimated during 27 d of incubation at 25°C. To characterize the biologically active SOM (Zibilske, 1994), the CO₂ evolved was trapped in NaOH and the excess NaOH was titrated with standardized HCl after addition of BaCl₂ and phenolphtalein. The pool of mineralizable C (C₀, mg CO₂–C kg^-1) and the corresponding mineralization coefficient (k, d^-1) were estimated by fitting the data for the cumulative mineralized C_T (mg CO₂–C kg^-1) with a first-order kinetic model using nonlinear regression

Incubations of Undisturbed Soil Cores
Undisturbed soil core incubations were performed in stainless steel pipes (i.d. 11 cm, height 10 cm) closed at each end with a neoprene sealed cover and equipped with independent recirculation gas systems. Unfrozen control cores were kept at 4°C. Frozen cores were put at -20°C for 18 h and then thawed at 25°C during 1 h before incubations started. The core headspace volume was estimated using pure Kr (Germon, 1980). The core and headspace atmosphere was recirculated during incubation by using sealed aquarium pumps (Elite 799, Mansfield, MA) operating at 10.35 x 10³ Pa and air output of 1200 cm³ min^-1. Soil cores were successively incubated during 3.5 h under aerobic (ambient air) and anaerobic (90% N₂ + 10% C₂H₂, v/v) conditions, with the gas recirculation system. Gas samples were collected periodically (30 min) through rubber septa inserted in the cover and analyzed for N₂O and CO₂ by GC.

Gas Analysis
At sampling time, the air from incubation flasks or cores was sampled with syringes and drawn directly from the syringes into evacuated vials (7.5 mL) with Vacutainer septa (10-mL Vacutainers). The N₂O and CO₂ concentrations were analyzed by gas chromatography (Hewlett Packard 5890 series II, Wilmington, DE) equipped with an automatic sample injector system (CTC Analytics, Zwingen, Swirzerland). The operating setup and conditions for CO₂ were: a Porapak Q column (Chromatographic Specialties, Brockville, ON) (50°C) used with N₂ as a carrier gas (40 mL min^-1), CO₂ was reduced to CH₄ in a Ni catalyst tube coupled to the flame ionization detector (250°C). The operating setup and conditions for N₂O were: a Porapak Q precolumn (0.91 m by 0.32 cm diam.) coupled to an analytical column (1.83 m by 0.32 cm diam.) used with Ar/CH₄ as carrier gas (0.95:0.05 m³ m^-3, 45 mL min^-1), and an electron capture detector (250°C). The detection limit and precision were, respectively, 77 x 10^-6 mol mol^-1 and 16 x 10^-6 mol mol^-1 for CO₂ analysis, and 70 x 10^-9 mol mol^-1 and 14 x 10^-9 mol mol^-1 N₂O analysis.

The Kr concentrations were analyzed by gas chromatography (Hewlett Packard 5890). The operating conditions for Kr were: thermal conductivity detector (110°C), Porapak Q column (i.d. 0.32 cm; length 6 m), and carrier gas He (25 mL min^-1).

Statistical Analyses
All statistical analyses were performed using SAS (SAS Institute, 1988). The data from DR assays were analyzed statistically using the ANOVA procedure. The data from incubation on macroaggregate fractions were first checked for homogeneity using Bartlett's test and then logarithmically transformed before ANOVA analysis. The C₀ and k values calculated for the replicates of each aggregate size fraction and each treatment were analyzed using ANOVA. The data from the dynamic soil cores incubations were first checked for homogeneity using the Bartlett test and then analyzed using a nonparametric multiple comparison test, PROC RANK (Montgomery, 1984; Conover, 1980).

	Results and discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Effects of Freeze–Thaw and Agriculture Practice on Denitrifying Rate in Slurries
Both freeze–thaw and agricultural practices had a significant effect on DR (Fig. 1) . Denitrification rates were higher in frozen–thawed than in unfrozen treatments. In general, it is assumed that N is not limiting during anaerobic slurry incubation of agricultural soils (Myrold and Tiedje, 1985). Moreover, the addition of NO₃ to the slurries of the present study assures that C substrate and/or denitrifying enzymes were the only limiting factors for denitrification. We also assume that breaking of aggregates was minimized under experimental conditions for DR. Therefore, the burst of denitrification after thawing probably resulted from the release of organic C substrates previously sequestered in aggregates that are disrupted by freezing or from microbial biomass and microfauna that are killed by the freezing process (Soulides and Allison, 1961; Bullock et al., 1988). The increases of 32% in denitrification following thawing were similar for both agricultural practices. Denitrification rates were 92% higher under NT–R than under CT–C. Because N was not limiting in slurry incubations, the higher denitrification rates in soils from NT–R may be due to greater concentrations of mineralizable organic C in soils from this conservation practice than in CT–C. Both no-till and red clover are agricultural practices known to increase the concentrations of mineralizable C and mineralizable N in soil (Odell et al., 1984; Sheaffer and Barnes, 1987). Although not significant, data collected from our experimental plots in September 1995 showed higher levels of organic C and total N in NT–R than in CT–C (Nicole Bissonnette, 2000, personal communication). Furthermore, on the same plots, Angers et al. (1993a) observed significant increases in microbial biomass C and hot water–extractable and acid-hydrolyzable carbohydrates due to the soil management and to a lesser extent to the rotation after 4 yr of no-till. The differences in concentrations of organic mater (OM) labile forms were also greater for the NT than for the CT in 1995. This is in agreement with other studies showing that soil conservation management systems (e.g., reduced tillage, rotation) result in higher aggregate stability and organic matter content than conventional systems (Angers et al., 1993b; Beare et al., 1994). Higher rates of denitrification in soils from NT–R may also be attributed to differences in enzymes present in samples at the beginning of incubation, as the DR assay (adapted from Martin et al., 1988) was initially designed to show.

View larger version (26K): [in this window] [in a new window]   Fig. 1 Effect of thawing and agriculture practices on denitrifying rate (DR) in soil slurries of conventional till continuous barley (CT–C) and no-tillage–barley–red clover rotation (NT–R) treatments. Agricultural practices and freeze treatments indicate significant differences (P < 0.0005 and 0.05); interaction between treatments was not significant. Vertical bars represent standard error of four replicates

View larger version (28K): [in this window] [in a new window]   Fig. 2 Effect of freezing on denitrification rates in 0.25- to 2- and 2- to 5-mm macroaggregate fractions from continuous barley under conventional till (CT–C) and a barley–red clover rotation under no-till (NT–R) management systems

Effects of Freezing–Thawing on Nitrous Oxide and Carbon Dioxide Emissions in Soil Cores
Under aerobic conditions, agricultural practices and freezing–thawing cycle showed a significant effect on N₂O emission from soil sampled in November but not from that sampled in October (Table 2 , Fig. 3a) . In undisturbed soils obtained in November, as observed in slurries, the NT–R treatment exhibited N₂O production significantly higher (500%) than those from CT–C, indicating that environmental factors conducive to denitrification were more likely present in the late autumn (November). Among the critical environmental factors, volumetric soil water content, which regulates O₂ availability to denitrifiers, averaged 39% in soil cores sampled in November and 28% in those sampled in October. In November, N₂O emission also increased (220%) similarly in both agricultural practices after a freezing–thawing cycle. This is in agreement with other studies showing that the thawing of a soil can cause temporal increase in N₂O production by denitrification (Christensen and Tiedje, 1990). Measurements of N₂O made under aerobic (ambient air) conditions represented the net emission of N₂O evolved from soils, whereas measurements in anaerobic conditions and in the presence of acetylene represented the potential of N₂O plus N₂ production by denitrification.

View larger version (45K): [in this window] [in a new window]   Fig. 3 Effect of freezing–thawing cycle and agricultural practices on N2O and CO2 emissions in undisturbed soil cores under aerobic (ambient air) and anaerobic (N2 + 10% C2H2, v/v) incubations

Production of CO₂ from soil cores was significantly affected by agricultural practices and by freezing–thawing cycle, except for the aerobic incubation in October (Table 2, Fig. 3b). Despite the lack of effects of agricultural practices on N₂O and CO₂ emissions in October, the pattern of Fig. 3b suggests that differences in available C occurred in October. In general, CO₂ production, which is due to microbial respiration, followed the same trend as N₂O production (Fig. 3a). Both gases were higher in NT–R than in CT–C soils, probably reflecting the higher mineralizable C (not shown) that can support denitrification. There was also a burst of CO₂ production following thawing, which supports the increase in microbial activity, such as denitrification.

	Conclusions

TOP ABSTRACT INTRODUCTION Materials and methods Results and discussion Conclusions REFERENCES

 
Soils under no-tillage–barley–clover rotation practice (NT–R) showed higher capacities to denitrify than those from conventional till–continuous culture (CT–C). These soil properties (e.g., available C and sufficiently depleted O₂) were reflected in the levels of N₂O produced from undisturbed soils when conditions for denitrification were not limiting. This study also showed that a freezing–thawing cycle increases denitrification activity, which may result in higher net N₂O emissions from soils.

Our results showed that a single short freezing and thawing cycle caused a burst of denitrification in macroaggregates. This burst was sustained by C mineralization from organic matter released by disruptive forces induced by freezing, and it was higher in small than in large macroaggregates. The greater effect of freezing on small aggregates was probably due to their higher water content. The no-tillage and rotation system (NT–R) resulted in a greater pool of mineralizable C in macroaggregates, and stimulated denitrification rates in the topsoil compared with a conventional tillage with continuous barley system (CT–C).

The effects of freezing and thawing cycles should be included in simulation models of N₂O emissions for climatic zones where freezing of the topsoil is a frequent event. Understanding of exact mechanisms and quantification of the fundamental relationships between microstructure with denitrification activity and organic matter availability will improve the accuracy of model outputs.SAS Institute 1988

	ACKNOWLEDGMENTS

 
This study was supported by the GHG Initiative of Agriculture and Agri-Food Canada. We wish to thank Dr. D.A. Angers and Dr. C. Chenu for their valuable comments at the beginning of this study, as well as G. Lévesque and Dr. H. Benmoussa for their work in the laboratory. The technical assistance of Brigitte Patry is also gratefully acknowledged. We thank Dr. D.A. Angers and Dr. B.H. Ellert for valuable comments on earlier version of this manuscript.

Received for publication October 26, 1999.

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