agriculture, ecosystems and environmentsoilandwater.bee.cornell.edu/publications/olga_nitrous...

Agriculture, Ecosystems and Environment xxx (2009) xxx–xxx

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AGEE-3390; No of Pages 8

Nitrous oxide emission at low temperatures from manure-amendedsoils under corn (Zea mays L.)

Olga Singurindy 1, Marina Molodovskaya, Brian K. Richards *, Tammo S. Steenhuis

Department of Biological and Environmental Engineering, Riley-Robb Hall, Cornell University, Ithaca, NY 14853-5701, USA

A R T I C L E I N F O

Article history:

Received 21 October 2008

Received in revised form 10 March 2009

Accepted 10 March 2009

Available online xxx

Keywords:

Nitrous oxide emission

Denitrification

Tillage effects

Soil freeze–thaw

Soil moisture content

A B S T R A C T

Manure fertilization of soil significantly impacts the level of nitrous oxide (N2O) emission. Despite their

short duration, periods of significant N2O emissions during soil thaws in winter and spring are an

important portion of the total annual emissions from agricultural lands. The goal of this study was to

understand the effects of tillage, moisture content and manure application on N2O emissions from

agricultural soils at low temperatures. We summarize here both field and laboratory experiments. The

field chamber study was focused on quantification of N2O flux from a field (Hudson clay loam: fine, illitic,

mesic Glossaquic Hapludalf) growing corn (Zea mays L.) located in upstate New York. The field was

moldboard plowed in the fall and then fertilized with liquid dairy manure. Intact soil cores were

collected from the site both before and after field treatments for subsequent laboratory incubation that

included freeze–thaw cycles. The results demonstrated that tillage reduced N2O emissions in non-

manured soils by 20–30% in the 35–50 days following the tillage event, attributed to improved aeration

resulting from reduced bulk densities and pore space saturation. The maximal emission of

200 mg N m�2 h�1 was found at soil temperatures greater than 5 8C and at WFPS between 40 and

70%. Subsequent application of liquid manure caused an increase in the total intensity of N2O emission.

The emission of N2O from manure-amended soils was not limited to thawing events: emissions began at

soil temperatures below 0 8C and continued even after complete soil freezing. The tillage history prior to

manure application was found to have a significant influence on N2O emission during freezing/thawing

cycles following manure application. The subsequent total winter N2O emissions were greater from the

field areas that were tilled earlier in the fall, particularly in the first few freeze–thaw cycles, during which

the maximum N2O fluxes occurred.Increasing soil saturation in a wet area formed during a spring thaw

caused increasing N2O emissions up to a maximum of 200 mg N m�2 h�1 at �60–70% saturation.

However, emissions dropped dramatically with further increases in soil moisture, decreasing to

50 mg N m�2 h�1 in the most saturated areas (90% saturated). Overall, maximal emissions were found at

temperatures greater than 5 8C and at water filled porosities between 40 and 70%.

� 2009 Elsevier B.V. All rights reserved.

Contents lists available at ScienceDirect

Agriculture, Ecosystems and Environment

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1. Introduction

A primary source of gaseous N losses to the atmosphere comesfrom the spreading of animal waste on agricultural fields,amounting to 35% of the global annual emission (Kroeze et al.,1999). Key agricultural management practices regulating N2Oformation and release from agricultural fields include use ofmanure as a fertilizer, crop cultivation and land treatments. For agiven amount of N applied to soils, manure application typically

* Corresponding author. Tel.: +1 607 255 2463.

E-mail address: [email protected] (B.K. Richards).1 Present address: Department of Earth and Ocean Sciences, University of British

Columbia, BC, Canada.

Please cite this article in press as: Singurindy, O., et al., Nitrous oxidecorn (Zea mays L.). Agric. Ecosyst. Environ. (2009), doi:10.1016/j.age

0167-8809/$ – see front matter � 2009 Elsevier B.V. All rights reserved.

doi:10.1016/j.agee.2009.03.001

results in greater N2O emissions than does synthetic N fertilization(Clayton et al., 1997).

Nitrous oxide is produced in soil by microbial nitrification anddenitrification processes. The most important factors controllingthese processes are soil mineral N (NH4

+ and NO3�) concentra-

tions, oxygen partial pressure and, in the case of denitrification,available carbon to fuel the heterotrophic processes (e.g. Cloughet al., 2003). Soil water content influences diffusion conditions inthe soil and thus impacts the supply of oxygen (Robertson andTiedje, 1987) which in turn controls the amount of N2O emitted.When the water filled pore space (WFPS) exceeds 60%, deni-trification becomes the dominant process producing N2O (e.g.Lemke et al., 1999), however production of N2O declines when theWFPS exceeds 80% because N2O is reduced to N2 (Veldkamp et al.,1998). In contrast, any N2O production at WFPS below 60% is

emission at low temperatures from manure-amended soils undere.2009.03.001

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http://dx.doi.org/10.1016/j.agee.2009.03.001

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O. Singurindy et al. / Agriculture, Ecosystems and Environment xxx (2009) xxx–xxx2

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typically attributed to nitrification, because increased diffusion ofO2 limits denitrification (Robertson and Tiedje, 1987).

Significant N2O emissions occur during winter and spring soilthaw events, characterized by N2O peaks which usually last forseveral days (Christensen and Tiedje, 1990). Despite its limitedduration, the phenomenon represents a significant fraction of thetotal annual emissions from agricultural lands (e.g. Wagner-Riddleand Thurtell, 1998) and may exceed 50% of the annual emissions(Flessa et al., 1995). There are two possible explanations for N2Oemission during freezing–thawing cycles: (1) gradual accumula-tion of N2O produced in the unfrozen subsoil that is unable todiffuse through the frozen soil surface until a thaw takes place (e.g.Goodroad and Keeney, 1984) and (2) favorable denitrificationconditions at the time of soil thawing result in a surge of N2Oproduction due to greater carbon and nitrogen availability formicrobial activity and high degree of soil saturation (Edwards et al.,1986; Nyborg et al., 1997).

A number of studies have measured N2O emissions from soilsexposed to repeated freeze–thaw cycles. The results are interestingbut also indicate large variability (and hence uncertainty) arisingfrom soil heterogeneity and the complex interactions betweenchemical, physical and biological factors. Nitrous oxide emissionshave been reported to decrease with repeated freeze–thaw cycles(Schimel and Clein, 1996; Prieme and Christensen, 2001). Thedecrease in gas production suggests either depletion in microbialnutrient availability or damage to soil microbes. Some studiesreported significant N2O losses from cultivated soils followingfreeze–thaw cycles in spring (Nyborg et al., 1997; Wagner-Riddleand Thurtell, 1998).

Thawing causes the disruption of soil structure (primarilymacroaggregates) and enhances microbial activity due to release oforganic C from plant and microbial detritus. The combination ofthese two factors can change the denitrification potential of soiland therefore influence N2O production during a freeze–thawevent (van Bochove et al., 2000). Consequently, tillage practiceshave significant effects on the water-stable aggregate distribution.Reduced tillage also reduces total soil porosity and increases soilwater content, a factor known to restrict oxygen diffusion throughsoil (Rice and Smith, 1982).

More research is needed to obtain a quantitative understandingof how farm management practices can affect and ideally reduceN2O emissions. Of special interest is understanding some of theapparent complexities involving the interactions between tillagepractices and soil conditions and how these affect N2O emissionssoon after manure application when potential losses are thegreatest. A good example of the complexities involved in designingmanure management strategies is the practice of manure injectioninto soil (for liquid slurries) or rapid plow down of surface spreadmanures to reduce odor emissions (Webb et al., 2004). Althoughthis is known to reduce ammonia emissions, there are concernsthat these direct applications into soil may significantly increaseN2O emissions by increasing the pool of mineral N in soil(Bouwman, 1996).

We focused our study on understanding the interactionsbetween tillage effects, moisture content, manure applicationand N2O emissions from corn field soils at low temperatures.

2. Materials and methods

Field monitoring using chambers was carried out in order toexamine the evolution of nitrous oxide flux as affected by mildwinter temperature fluctuations (freeze–thaw cycles), soiltillage, and winter liquid manure application. To furtherinvestigate these phenomena under more controlled conditions,soil columns were extracted from the field and monitored duringa series of laboratory experiments.


2.1. Field monitoring experiments

The experimental site was planted with corn on a clay loam soil(Hudson series—fine, illitic, mesic Glossaquic Hapludalf) located ona large dairy farm in central New York (Fig. 1). The mean annualprecipitation is 850 mm and the mean annual temperature is 10 8C.The site was historically fertilized with dairy manure once a year,either spring or fall. On October 10th, 2004, polyvinylchloridechambers (each covering a rectangular area of 0.89 m2) wereinstalled in the field after corn harvesting and about 6 months afterthe last fertilization. On November 4, 2004 one-half of the field(designated here as area #1) was moldboard plowed. Theremaining half (designated as area #2) was plowed on December16, 2004. On December 17, 2004 liquid dairy manure (5.4% drymatter, total C 4.6–11.3% and total N contents ranging between 0.3and 0.5%, wet weight basis) was injected into the field with atractor and a draghose at a liquid loading rate of 75,000 L ha�1. Theexperiment ended on 15 April 2005.

The number of chambers installed in the field varied, with 31chambers permanently installed and 18 additional chambersinstalled for specific campaigns. The distance between chamberswas 25 m, with a total grid area of 30625 m2 (3.06 ha). Theadditional chambers were installed in the field during fivedistinct 3-day campaigns, four during winter thawing eventsand the fifth when spring thawing started at the end of theexperiment. Each chamber consisted of a frame permanentlylocated in the ground which could be sealed for 1–3 h withremovable plastic lid and additional plastic seal to prevent airexfiltration from the chambers. Each chamber lid was equippedwith rubber septa to allow gas sampling with a syringe.Triplicate gas samples were collected in evacuated crimp-sealedminivials at the start and termination of each testing interval.Twenty vertical metal tubes were installed at a depth of �5 cmat 10 locations in the field in order to collect gas samplesduring winter when the soil surface was frozen. During theexperiment, gas samples were collected at intervals rangingfrom 1 to 4 days.

Soil temperature measurements were made using digitalthermometers. Soil samples were collected at 10 cm depth neareach chamber whenever air samples were taken, and weretransported to the laboratory for NO3

�, NH4+, pH, and gravimetric

moisture content analysis.

2.2. Laboratory experiments

For laboratory experiments, 16 intact soil cores (10 cm dia.,20 cm deep) were collected from field areas #1 and #2 inDecember 2004. Ten additional cores (5 each from manured andnon-manured areas) were collected on December 22, 2004, whichwas 5 days after manure application. Cores were obtained byhammering aluminum tubes (10 cm dia., 40 cm long) into the soiland then carefully excavating them. No compression of the soil wasobserved. The cores were transported to the laboratory and storedoutdoors (temperatures thus close to field conditions) for 3 daysprior to experimentation.

Each soil column microcosm system was built from thealuminum column in which the soil core was extracted, whichhad a head space of�20 cm. The top of each column was sealed anda rubber septum was installed for sampling. Air samples (6 mL)were taken with syringes every 6 h. After each sampling, thecolumns were briefly opened to atmosphere and then resealed. Soilcolumn temperatures were monitored by two sensors installed inthe middle of six of the columns.

During the experiment, the soil cores were subjected to fourfreeze/thaw cycles by shifting them between a freezer (set at�5.5 8C) and an incubator (25 8C) equipped with a circulation



Fig. 1. The topographic map of the field site area (428350N, 768310W) where field monitoring experiments were carried out and gas/soil samples were collected. Field areas #1

and #2 correspond to areas that were tilled on November 4th and December 16th, respectively.

O. Singurindy et al. / Agriculture, Ecosystems and Environment xxx (2009) xxx–xxx 3

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fan. The duration of the experiment was 55 days. Theexperiment was started at 22 8C. The columns were then placedin the freezer. Soil temperatures were monitored every 2 h; circa15 h were required for the columns to freeze and equilibrate. Atthe end of the experiment soil samples were extracted from thecolumns, sectioned at 5 cm depth intervals, and analyzed forgravimetric moisture content, NO3

�, NH4+, and total carbon

content.

2.3. Soil and gas analysis

Air sample N2O concentrations were measured with a Varian3700 gas chromatograph (GC) with a Ni63 electron capturedetector operated at 350 8C and with Ar:CH4 (95:5) carrier gas(30 mL min�1). Solution analysis for NO3

� and NH4+ were carried

out according to APHA (1985). Soil pH, gravimetric moisturecontent, and soil organic matter content were determined usingstandard methods described in ASA (1965). Total carbon contentwas determined via persulfate oxidation with an OIAnalyticalModel 1010 total organic carbon analyzer (O-I-Analytical). Soilbulk density was determined using undisturbed soil cores (Birke-land, 1984). The water filled pore space, defined as the fraction oftotal pore space filled with water (expressed as percent) wascalculated as

WFPS ¼ ½bulk density� gravimetric water content=water density�porosity

(1)

porosity ¼ 1� bulk density

particle density

� �(2)

The standard particle density used (2.65 g cm�3) was modified by areduction of 0.02 g cm�3 per percent of soil organic matter.


2.4. Statistical analysis

The error in measured concentration values within eachexperiment was in all cases less than �0.5%. All concentrationmeasurements in both laboratory and field experiments wererepeated in triplicate therefore all reported measurementsrepresent averages of three samples each. Standard error bars(Fig. 2) were included on the graphs to show the variation of thedata. A probability level of 5% (P = 0.05) was used to test thestatistical significance of all treatments.

3. Results

Field data collected before tillage and manure applicationindicate that initial soil properties were similar in the areas withsubsequently differing tillage treatments with respect to soiltexture, pH, bulk density, soil C, and total N. There were nosignificant differences found in average N2O flux or soil moisturecontent at the beginning of experiment (Table 1).

3.1. Field measurements

Fig. 2 presents the N2O emission and gravimetric soil moisturecontent measured from areas #1 and #2 in the 35 days prior tomanure application. Before tillage, the average N2O flux from thefield was 147 mg N m�2 h�1 (Table 1), and tillage resulted in animmediate �40% reduction in area #1 (Fig. 2b). N2O emissionremained significantly greater in area #2 (Table 2) for the periodfrom 4 November to 2 December 2004, but during the final 2 days areduction to 77.5 mg N m�2 h�1 was observed. The opposite wasobserved in area #1 soil, where the flux gradually increased andreached a maximum of 166 mg N m�2 h�1 on 4 December. N2Oemission in both areas #1 and #2 generally increased with



Fig. 2. Field monitoring results from field areas #1 (tilled) and #2 (not yet tilled)

before manure application: (a) N2O emissions and (b) soil moisture content. The

black arrows indicate the first date and amount (total of 5 days) of precipitation that

caused increased in N2O emissions.

Fig. 3. Field monitoring results from field areas #1 and #2 following manure

application: (a) Soil temperature—numbers above the temperature peaks represent

the thaw cycle number; (b) N2O emission—numbers above N2O peaks represent the

cumulative N2O emission (mg N m�2 period�1) during each thawing event, the top

number corresponding to area #1, the bottom to area #2.


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increasing soil moisture content (Fig. 2b) following three indicatedprecipitation events. In area #2, the maximal emission of �186mg N m�2 h�1 was observed on November 9th, 19th, and December2nd (Fig. 2a). For area #1, the first two peaks (149 and 133 mgN m�2 h�1) were concurrent with those in area #2, whereas the thirdpeak was delayed by several days relative to area #2.

Fig. 3 shows the course of the soil temperatures and N2Oemissions following tillage of area 2 and manure application ofthe whole field on December 17. Soil temperature fluctuationsindicate nine cycles of freezing and thawing (Fig. 3a), with sevencycles (lasting from 4 to 12 days) during which N2O emissionsoccurred. Low levels of emission were found during the thawcycles between days 41 and 46. The thaw cycle starting at day 51was apparently too brief to allow emission to occur. The numbersabove each peak in Fig. 3b represent the cumulative N2Oemissions (mg N m�2 period�1) during that thawing event (thetop number corresponds to area #1, the bottom to area #2).Despite the fact that both field areas had been tilled by the timeof manure application, the results shown in Fig. 3b and Table 2demonstrate continuing differences in N2O emissions betweentwo areas tilled at different times. The differences were greatestduring the first three thaw cycles (Table 2), where emissionsfrom earlier-tilled area #1 were much greater than from area #2:

Table 1Soil characteristics from two parts of the field (#1 and #2) at the beginning of the fiel

Area Sand (%) Silt (%) Clay (%) pH (in water) Total C (%)

#1 15 53 32 7.2 1.8

#2 16 54 30 7.1 1.7


e.g. 700 mg N m�2 vs. 257 mg N m�2 during the first cycle. Thegreatest emission rate of 289 mg N m�2 h�1 was observed fromarea #1 soil during the first thaw-related peak. However, thisdifference in tillage history effects was no longer observed afterthe long freezing period (with two short thaws) precedingthawing cycle 4: subsequent N2O peaks were more consistentand were both greater and longer. In some cases a low level ofN2O emission continued for a time after complete soil freezing,continuing between first and second thawing cycles andpersisting for 3–4 days after the second and third cycles(Fig. 3a). Emission of N2O also occurred just prior to the onsetof thawing cycle 6. The cumulative emissions of N2O for allfreeze/thaw cycles were 2860 and 2120 mg N m�2 for areas #1and #2 soils, respectively. The pH values were 7.3–7.7 and total Nvaried from 0.5 to 0.7%. Total mineral nitrogen (NO3 + NH4) wasbetween 19 and 28 mg N kg�1 of dry soil.

The results of a 3-day campaign during spring thawing areshown in terms of soil saturation and N2O emission (Fig. 4). Theresults show that the sample grid contained a large wet area wherethe pore space reached a maximum saturation of 90%, compared to30–50% saturation in the rest of the field (Fig. 4a). Corresponding tothis is the pattern of N2O emissions (Fig. 4b), which increased withincreasing soil saturation up to about 60–70% to a maximum of200 mg N m�2 h�1. However, at greater 70–90% saturation in themiddle of the wet area, N2O emissions dropped dramatically to50 mg N m�2 h�1.

3.2. Laboratory experiments

The freeze/thaw cycles resulting from the freezer/incubatorcycling are evident in the soil core temperatures in Fig. 5a. The

d monitoring experiments, before tillage and manure application.

Total N (%) Bulk density

(g cm�3)

Soil moisture (%) Nitrous oxide flux

(mg N m�2 h�1)

0.2 1.25 21 148

0.2 1. 22 146



Table 2Summary of cumulative N2O emissions (mean � standard deviation) from field chamber and soil column experiments. Statistical comparisons made between areas 1 and 2: values

followed by asterisks are statistically different (P = 0.05).

Experiment and time frame Period

(days)

Area #1 (tilled November 4)

(mg N m�2)

Area #2 (tilled

December 17) (mg N m�2)

Field chambers

After tilling, before manure application 35 2425 � 120* 3302 � 159*

After tilling and manure application (first three freeze–thaw cycles) 41 1043 � 34* 588 � 19*

After tilling and manure application (entire period) 121 2860 � 115* 2120 � 88*

Soil columns

Collected after tilling, before manure application (four freeze–thaw cycles) 50 1631 � 24* 1992 � 37*

Collected after tilling, after manure application (first freeze–thaw cycle) 10 1425 � 27* 1189 � 23*

Collected after tilling, after manure application (four freeze–thaw cycles) 50 6128 � 96 6332 � 89


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laboratory cores extracted from field areas #1 and #2 had differingbulk densities and therefore differing initial WFPS levels of 35%(area #1) and 70% (area #2).

During these four freeze/thaw cycles, the N2O emissions fromthe soil cores collected before manure application were greater forarea #2 in terms of peak rates (Fig. 5b) as well as cumulativeemissions (1631 mg N m�2 vs. 1992 mg N m�2 for areas #1 and #2,respectively; Table 2). The greater N2O emission corresponded tothe higher soil water content. In area #2 soils the emission peakedimmediately after thawing (approximately 300 mg N m�2 h�1

maximum during the first cycle) and declined markedly thereafter(Fig. 5b). The general trend in emissions over time was similar forboth treatments, with the greatest emissions occurring in cycle 1,cycles 2 and 3 having similar emissions, and lower emissionsduring the last thawing cycle.

Fig. 4. Field monitoring results from 3-day chamber array campaign during spring thaw e

each grid point (25 m grid spacing), with a total grid area of 30,625 m2 (3.06 ha).


Unsurprisingly, the soil cores collected after manure applica-tion had greater N2O emission rates (Fig. 5c) than those collectedbefore application, with a maximal emission rate of approximately396 mg N m�2 h�1 observed from area #1 soil cores during the firstthaw-related peak. The area #1 cores had a significantly greatercumulative emission during the first thaw cycle (Table 2).However, the cumulative emissions of N2O from the four freeze/thaw cycles did not differ significantly during the four cycles 6128and 6332 mg N m�2 for areas #1 and #2 soils, respectively. Inaccordance with the field measurements, the most intensiverelease of N2O was found immediately after thawing started (withtemperatures climbing over 0 8C at the point of measurement) inall four freeze/thaw cycles. However, emissions were not limited tothe thaw periods: low levels of emission were recorded 2 daysbefore first and third thaws, continued between the first and

vent. (a) Degree of soil saturation and (b) emission of N2O. Chambers were located at



Fig. 5. Result of laboratory experiment with undisturbed soil cores collected from field areas #1 and #2: (a) soil temperature, (b) N2O emission from columns collected before

manure application, and (c) N2O emission from columns collected after manure application.


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second thaw events, and also continued 2 days after soil freezing inthe second cycle. Finally, unlike the non-manured soil cores, therewas no reduction of N2O emission during the fourth thaw,presumably due to the high availability of C (and mineral N) in themanured soils.

4. Discussion

The soil water filled pore space strongly affected N2Oproduction, likely via effects on oxygen availability. Fig. 6integrates the combined effects of WFPS and soil temperature onmeasured N2O flux. Generally, the optimal conditions for N2Oproduction were at temperatures greater than 5 8C and at soilWFPS levels between 40 and 70%. Temperatures lower than 5 8Creduced soil microbial activity and consequently reducedemissions. The maximal flux of N2O was found at moisturelevels of approximately �55% WFPS, which corresponds wellto the results obtained by Davidson et al. (2000) for differentsoil types. Oxygen deficiency and an associated increase inN2O production could even occur at lower saturation levelsin soils with high microbial activity. With good soil aeration(WFPS of 40–60%), both organic and clay soils had increasedN2O production at a lower temperature than did silt or loam


soils, which could be associated with greater organic matterdegradation rates in the organic and clay soils (Koponen et al.,2004). High water content favors denitrification associated withthe limitation of oxygen diffusion. We could not perform anisotopic analysis needed to show the possible changes of N2O/N2

ratio in our specific experimental conditions. Maag and Vinther(1996) demonstrated that N2O/N2 ratio in denitrificationincreases with a decrease of temperature, and thus enhanceN2O production.

Though the gravimetric water contents were sometimes similar(especially after intense precipitation; Fig. 2b) in the tilled andnon-tilled parts of the field, the WFPS was different because of thediffering bulk densities (1.06 g cm�3 tilled vs. 1.25 g cm�3 non-tilled). Subsequent tillage of area #2 followed by manureapplication homogenized the two areas of the field with respectto soil bulk density and WFPS. Nevertheless, significant differencesin N2O emissions between areas #1 and #2 were still identifiedduring the first three freezing–thawing cycles (Fig. 3b), the totalN2O emission being greater in the better pre-aerated soils of area#1. A possible explanation for the high peaks of N2O duringthawing was that greater microbial activity resulted in greatermineralization/nitrification rates as well as greater oxygenconsumption.



Fig. 6. Generalized relationship of N2O emission with temperature and WFPS: field

data before manure application.


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Emission of N2O was always observed during thawing in bothlaboratory and field experiments. Surprisingly little spatialvariability was observed in the field measurements except duringthe intensive spring thawing such as the 3-day campaign in theearly spring, when more ice and snow started to melt at the soilsurface. The sample grid encompassed a wet area that wassubstantially wetter than the rest of the field (Fig. 4a). Correspond-ing to this is the pattern of N2O emissions, which increased withincreasing soil saturation up to about 60–70% WFPS. However, athigher WFPS levels (with the wet spot nearing saturation), N2Oemissions dropped dramatically: under saturation, anaerobicconditions would dominate and, consistent with expected trends,favor N2 production during extended denitrifying conditions. Asimilar phenomenon was observed by Nyborg et al. (1997). Inaddition, drainage problems are well-known in this specific soiltype, especially in spring.

Our field measurements demonstrate that N2O emissioncontinued even after complete soil freezing (Fig. 3). Teepe et al.(2001) observed constant N2O emission for several days in freezingperiods as evidence of microbial activity in the frozen soil.Goodroad and Keeney (1984) reported that N2O emission was dueto the temperature fluctuations that cause microbial activity at thesoil surface. Kaiser et al. (1998) suggested that N2O emissionsduring the time of deepest soil freezing occurred as a result of N2Oproduction in deeper soil horizons, with the gas escaping throughfrost-induced cracks. In our study, during the period from 41 to 65days after manure application, considerable snow precipitationcaused the formation of the deep snow and ice layer that preventedthe escape of nitrous oxide. During the subsequent thaw, thetrapped N2O was released within few days, resulting in a highemission peak. The fact that these peaks were wide may be due tothe melting snow causing elevated soil moisture conditions thatfavored denitrifier activity.

Edwards and Cresser (1992) showed that 8–20% of the soilwater remained unfrozen for several days although the soiltemperature was�5 8C. There are significant amounts of unfrozensoil water down to�20 8C (Rivkina et al., 2000), mostly because of


salting-out effects. The unfrozen water covers the soil matrix withthe thin water film which in turn is covered with ice, creatingconditions are favorable for denitrification, because microorgan-isms are isolated from oxygen by the ice barrier (Teepe et al.,2000).

In addition, field and laboratory data demonstrated that, insome cases, thawing begins at the temperatures below 0 8Cfollowed by production of N2O. As a result a small peak of N2Oemission was observed before thawing cycle number 6 (Fig. 3b).This phenomenon occurred as a result of the presence of ions inthe soil solution. Gas samples taken at �5 cm depth in the fieldand from soil cores during freezing (soil temperatures �5 8C)demonstrated accumulation of N2O. A portion of the large fluxof N2O that was released just after thawing (temperaturesclose to 0 8C) might have originated from the liberation of N2Ostored in the frozen soils, an effect much more pronounced withthe manure-applied soils. These results are in agreement withthe laboratory observations of Koponen et al. (2004) whosuggested that there was N2O production in soils at least downto �6 8C.

In the laboratory experiments with cores collected beforemanure application (Fig. 5b), the maximum thaw-related N2Oemission occurred during the first thaw cycle. The first cycle peakwas also higher in field #1 soil (Fig. 3b). Koponen and Martikainen(2004) found a similar difference for N2O emission between thetwo cycles. Schimel and Clein (1996) reported a similar phenom-enon for CO2 emissions from tundra and taiga soils. Theyconcluded that freeze–thaw cycles caused a flush of microbial Cand N during the first cycle, but after repeated cycles the ability ofmicrobial communities to decompose soil organic matter falls. Anadditional explanation given by Koponen and Martikainen (2004)is that amount of organic and inorganic substances declines fromcycle to cycle, leading to lower thaw-related N2O emissions insubsequent cycles. Moreover, it can be due to the high availabilityof C as a result of film microorganisms killed during freeze/thawcycles (Christensen and Tiedje, 1990) coupled with high concen-trations of both inorganic and organic solutes (Edwards andCresser, 1992) may cause favorable conditions for N2O formation inwater films.

In our previous study (Singurindy et al., 2006) we observed thatthis specific soil has a high capacity for NH4

+ fixation by clayminerals. Moreover, nitrate and ammonium immobilization by soilmicrobial biomass shortly after field N application (Muller et al.,2002) would increase the potential for N2O emission duringfreezing–thawing periods. Manured soils (high content of activebiomass and organic material) and clay dominated aggregatestherefore have an elevated potential for N2O emission duringfreeze/thaw events. This conclusion is in line with observationsthat the greatest thaw-related emissions were measured fromorganic soils and soils with a high content of clay-associatedaggregates (Christensen and Tiedje, 1990; van Bochove et al., 2000;Singurindy et al., 2008).

5. Conclusions

In this study, we have characterized the N2O emission effects oflate fall tillage and liquid dairy manure application to soil. Tillagereduced N2O emission in non-manured soils for the 35–50 days ofour observation periods. The differences in the emissions wereattributed to the reductions in bulk density and water filled porespace (and thus improved aeration) in the tilled area.

Application of liquid manure to the soil increased the totalintensity of nitrous oxide emission, and the majority of winteremissions occurred during periodic soil thaw events. In both fieldand laboratory studies, the timing of tillage prior to manureapplication was found to have a significant influence on N2O




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emissions, which were greatest from the earlier-tilled field areaduring the initial freezing/thawing cycles following manureapplication. In addition, in the field study, the cumulative winteremissions following manure application were greater from theearlier-tilled area. The emission of nitrous oxide from manure-amended soils started at temperatures below 0 8C and continuedafter complete soil freezing.

A large wet area formed during a substantial spring thaw had amaximum pore space saturation of 90%, compared to 30–50%saturation in the rest of the field. Corresponding N2O emissionsincreased with soil moisture to a maximum of 200 mg N m�2 h�1 at�60–70% saturation. However, emissions dropped dramaticallywith further increases in soil moisture, decreasing to50 mg N m�2 h�1 in the most saturated areas. Overall, maximalemissions were found at temperatures greater than 5 8C and atwater filled porosities between 40 and 70%.

Acknowledgments

This research was supported by USDA-NRI project no. 123527and Vaadia-BARD Postdoctoral Award No. F1-357-04 from BARD,The United States - Israel Binational Agricultural Research andDevelopment Fund. We thank Hardie Dairy Farms for theircooperation and technical assistance.

References

APHA, 1985. Standard Methods for the Examination of Water and Wastewater, 16thed. Port City Press, Baltimore, MD.

ASA, 1965. Methods of Soil Analysis: Part 2. Chemical and Microbiological Proper-ties. American Society of Agronomy, Madison, WI.

Birkeland, P.W., 1984. Soils and Geomorphology. Oxford University Press, NewYork.

Bouwman, A.F., 1996. Direct emissions of nitrous oxide from agricultural soils. Nutr.Cycl. Agroecosyst. 46, 53–70.

Davidson, E.A., Keller, M., Erickson, H.E., Verchot, L.V., Veldkamp, E., 2000. Testing aconceptual model of soil emissions of nitrous and nitric oxides. BioScience 50(8), 667–680.

Flessa, H., Dorsch, P., Beese, F., 1995. Seasonal variation of N2O and CH2 fluxes indifferently managed arable soils in southern Germany. J. Geophys. Res. -Atmos.100, 23115–23124.

Goodroad, L.L., Keeney, D.R., 1984. Nitrous oxide emissions from soils duringthawing. Can. J. Soil Sci. 64, 187–194.

Clayton, H., McTaggart, I.P., Parker, J., Swan, L., Smith, K.A., 1997. Nitrous oxideemissions fro fertilized grassland: a two-year study of the effects of N fertilizerfrom the environmental conditions. Biol. Fertil. Soils 25, 252–260.

Clough, T.J., Sherlock, R.R., Kelliher, F.M., 2003. Can liming mitigate N2O fluxes froma urine-amended soil? Aust. J. Soil Res. 41, 439–457.

Christensen, S., Tiedje, J.M., 1990. Brief and vigorous N2O production by soil atspring thaw. J. Soil Sci. 41, 1–4.

Edwards, A.C., Cresser, M.S., 1992. Freezing and its effect on chemical and biologicalproperties of soil. Adv. Soil Sci. 18, 59–79.


Edwards, A.C., Creasey, J., Cresser, M.S., 1986. Soil freezing effects on upland. WaterRes. 20 (7), 831–834.

Kaiser, E.A., Kohres, K., Kucke, M., Schnug, E., Heinemeyer, O., Munch, 1998. Nitrousoxide release from arable soil: importance of N fertilization, crop and temporalvariation. Soil Biol. Biochem. 30, 1553–1563.

Koponen, H.T., Martikainen, P.J., 2004. Soil water content and freezing temperatureaffect freeze–thaw related N2O production in organic soil. Nutr. Cycl. Agroe-cosyst. 69, 213–219.

Koponen, T.H., Flojt, L., Martikainen, P.J., 2004. Nitrous oxide emissions fromagricultural soils at low temperature: a laboratory microcosm study. Soil Biol.Biochem. 36, 757–766.

Kroeze, C., Mosier, A., Bouwman, L., 1999. Closing the global N2O budget: a retro-spective analysis. Global Biogeochem. Cycles 13, 1–8.

Lemke, R.L., Izaurralde, R.C., Nyborg, M., Solberg, E.D., 1999. Tillage and N sourceinfluence soil-emitted nitrous oxide in the Alberta Parkland region. Can. J. SoilSci. 79, 15–24.

Maag, M., Vinther, F.P., 1996. Nitrous oxide emissions by nitrification and deni-trification in different soil types and at different soil moisture contents andtemperatures. Appl. Soil Ecol. 4, 5–14.

Muller, C., Martin, M., Stivens, R.J., Laughlin, R.J., Kammann, C., Ottow, J.C.G., Jager,H.-J., 2002. Processes leading to N2O emissions in grassland soil during freezingand thawing. Soil Biol. Biochem. 34, 1325–1331.

Nyborg, M., Laidlaw, J.W., Solberg, E.D., Malhi, S.S., 1997. Denitrificationand nitrousoxide emissions from black chernozemic soil during spring thaw in Alberta.Can. J. Soil Sci. 77, 153–160.

Prieme, A., Christensen, S., 2001. Natural perturbations, drying–wetting and freez-ing–thawing cycles, and the emissions of nitrous oxide, carbon dioxide andmethane from farmed organic soils. Soil Biol. Biochem. 33, 2083–2091.

Rice, C.W., Smith, M.S., 1982. Denitrification in non-till and plowed soils. Soil Sci.Soc. Am. J. 46, 1168–1173.

Rivkina, E.M., Friedmann, E.I., McKay, C.P., Gilichinsky, D.A., 2000. Metabolic activitypermafrost bacteria below the freezing point. Appl. Environ. Microbiol. 66,3230–3233.

Robertson, G.P., Tiedje, J.M., 1987. Nitrous oxide sources in aerobic soils: nitrifica-tion, denitrification and other biological processes. Soil Biol. Biochem. 19,187–193.

Schimel, J.P., Clein, J.S., 1996. Microbial response to freeze–thaw cycles in tundraand taiga cycles soils. Soil Biol. Biochem. 28, 1061–1066.

Singurindy, O., Molodovskaya, M., Richards, B.K., Steenhous, T.S., 2006. Nitrousoxide and ammonia emissions from urine applied to soils: texture effect.Vadose Zone J. 5 (4), 1236–1245.

Singurindy, O., Molodovskaya, M., Richards, B.K., Steenhous, T.S., 2008. Gaseousnitrogen emission from soil aggregates as affected by clay mineralogy andrepeated urine applications. Water Air Soil Pollut. 10.1007/s11270-008-9746-4.

Teepe, R., Brumme, R., Breese, F., 2000. Nitrous oxide emissions from frozen soilsunder agricultural, fallow and forest land. Soil Biol. Biochem. 32, 1807–1810.

Teepe, R., Brumme, R., Breese, F., 2001. Nitrous oxide emissions from soil duringfreezing and thawing periods. Soil Biol. Biochem. 33, 1269–1275.

van Bochove, E., Prevost, D., Pelletier, F., 2000. Effects of freeze–thaw and soilstructure on nitrous oxide produced in a clay soil. Soil Sci. Soc. Am. J. 64,1638–1643.

Veldkamp, E., Keller, M., NuNez., 1998. Effects of pasture management on N2O andNO emissions from soils in the humid tropics of Costa Rica. Global Biogeochem.Cycl. 12, 71–79.

Webb, J., Chadwick, D., Ellis, S., 2004. Emission of ammonia and nitrous oxidefollowing incorporation into the soil of farmyard manures stored at differentdensities. Nutr. Cycl. Agroecosyst. 70, 67–76.

Wagner-Riddle, C., Thurtell, G.W., 1998. Nitrous oxide emissions from agriculturalfields during winter and spring thaw as affected by management practices.Nutr. Cycl. Agroecosyst. 52, 151–163.



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