Soil Science Society of America Journal 65:1307-1314 (2001)
© 2001 Soil Science Society of America
DIVISION S-8—NUTRIENT MANAGEMENT & SOIL & PLANT ANALYSIS
Cattle Slurry Affects Nitrous Oxide and Dinitrogen Emissions from Fertilizer Nitrate
R. James Stevens* and
Ronald J. Laughlin
Dep. of Agriculture and Rural Development, Agricultural and Environmental Science Division, Newforge Lane, Belfast BT9 5PX, UK
* Corresponding author (jim.stevens{at}dardni.gov.uk)
 |
ABSTRACT
|
|---|
Readily decomposable C in organic manures could enhance denitrification of NO3 existing in soil. The worst scenario occurs when farmers apply manures and NO3-containing fertilizers at the same time to meet the nutrient requirements of the next crop. If the denitrification produced N2O rather than N2, the emission factor of 1.25% of fertilizer N used to calculate national inventories for N2O would be an underestimate for this farming practice. We used the 15N gas–flux method to measure N2O and N2 fluxes from grassland when cattle slurry (CS) containing 60 kg NH4–N ha-1 and KNO3 (60 kg N ha-1) were applied at the same time. By labeling the KNO3 and the NH4 in CS, we quantified the processes producing N2O and checked for N2 production by microbial processes other than denitrification. On average over field experiments replicated in March, May, August, and September 1997, CS increased the flux of N2O by 0.63% of the applied NO3–N in the 104 h after application, but had no significant effect on the flux of N2. The maximum flux of N2O was always observed in the first measurement period (5–7 h) after CS application. All of the N2O was formed by reduction from NO3 apart from in August when 10% was formed by nitrification in the CS treatment. There was no evidence for production of N2 by other processes such as heterotrophic nitrifier denitrification or anaerobic NH4 oxidation.
Abbreviations: CS, cattle slurry • IPCC, Intergovernmental Panel on Climate Change • NAP, periplasmic nitrate reductase • NAR, membrane-bound nitrate reductase • VFA, volatile fatty acid
|
INTRODUCTION
|
|---|
METHODOLOGY FOR CALCULATING national inventories of N2O identifies three sources from agricultural systems (Mosier et al., 1998). These are: (i) direct emissions from agricultural soils, (ii) emissions from animal production, and (iii) emissions indirectly induced by agricultural activities. An emission factor for N2O of 1.25% of N input is applied to synthetic fertilizer and to animal excreta N (Mosier et al., 1998). The value of this emission factor is a large contributor to the uncertainty in the global estimate. Better data are needed for emissions due to animal excreta in a variety of agricultural systems to substantiate the choice of emission factors. In studies where CS was surface applied to grassland, denitrification losses ranged from 0.01 to 29.5% of NH4–N applied, while N2O emissions ranged from 0.1 to 4% of NH4–N applied (Stevens and Laughlin, 1997). Surface-spreading of CS on grassland can therefore result in N2O emissions well above the Intergovernmental Panel on Climate Change (IPCC) factor of 1.25% of N input.
To meet the nutrient demands of the next crop, farmers may apply organic manures together with inorganic fertilizers. Whenever fertilizer containing NO3 and CS are applied together or within a few days of each other, the potential exists for enhanced denitrification. Reviewers of studies on N2O emission have suggested that mineral N fertilizers plus organic manures may result in higher losses than with mineral N fertilizers alone (Bouwman, 1990; Granli and Bockman, 1994). Recent field studies support this suggestion. In wet soil conditions, cumulative N2O emissions were up to 4 times greater from NH4NO3 followed by CS than from NH4NO3 alone (McTaggart et al., 1997). When CS was supplemented with NH4NO3, the loss of N2O was 2.2% compared with 1.2% for NH4NO3 alone (Clayton et al., 1997). The relative contributions of the various microbial processes responsible for the production of N2O have not been quantified when CS and mineral N are applied together.
Nitrous oxide can be produced by either nitrification (Firestone and Davidson, 1989) or denitrification (Firestone et al., 1980). When CS is spread on the land, the NH4–N supplied increases the potential for nitrification. Provided NO3 is present, the addition of readily available C in the CS will also create conditions conducive to the production of N2O and N2 by denitrification. Nitrification and denitrification can occur simultaneously in aggregated soil because of the existence of microsites with differing aerobicity (Smith, 1980; Renault and Stengel, 1994). The relative importance of each of these processes needs to be known before mitigation strategies can be proposed. The 15N gas–flux method can measure N2O and N2 fluxes as well as quantifying the contributions of nitrification and denitrification to the N2O flux (Stevens et al., 1997).
All studies to date on measuring N2O and N2 fluxes from organic manures applied to grassland have used the acetylene block technique (Stevens and Laughlin, 1997; Ellis et al., 1998; Mogge et al., 1999). At the concentration of acetylene necessary to block N2O-reductase, nitrification is also blocked (Klemedtsson et al., 1988). Since nitrification may be producing N2O and supplying NO3 for denitrification, nitrification should be allowed to proceed when measuring N2O and N2 fluxes. We used the 15N gas–flux method in the field on a grassland soil to test if the concomitant application of CS and NO3-containing fertilizer resulted in enhanced fluxes of N2O and N2.
|
MATERIAL AND METHODS
|
|---|
Site
The 15N gas–flux method was used on a grassland soil at the Agricultural Research Institute of Northern Ireland, Hillsborough, County Down. The soil is an acid brown earth (fine loamy, acid, Typic Dystrochrept) with a pH of 6.0 and sand, silt, and clay contents of 480, 310, and 210 g kg-1 of mineral matter, respectively. It contained 120 g kg-1 oven-dry soil of organic matter in the 0- to 75-mm depth. The sward was dominated by perennial ryegrass (Lolium perenne L.) and had been under a three-cut silage regime receiving 300 kg N ha-1 yr-1 for the previous 5 yr. During 1997, we repeated an experiment to measure the fluxes of N2 and N2O on four occasions (Mar., May, Aug., and Sept.). A new area of grassland was used on each occasion. Soil and climatic conditions are given in Table 1.
View this table:
[in this window]
[in a new window]
|
Table 1. Soil and climatic conditions during the experimental period at the grassland site in Northern Ireland where the interaction between cattle slurry and fertilizer NO3 was studied on four occasions in 1997.
|
|
Treatments
The effect of CS on the flux of N2O and N2 from KNO3 applied at the same time was measured by labeling the NO3 component. By labeling the NH4–N pool of CS with 15N in paired treatments, we determined if nitrification of the NH4–N in the slurry was occurring and producing N2O. To check for N2 production by other microbial processes, such as anaerobic ammonium oxidation (Jetten et al., 1997) or heterotrophic nitrification (Kuen and Robertson, 1994; Richardson et al., 1998), we also labeled the NH4 and NO3 pools at the same time. Four treatments were therefore applied on each occasion: (i) unlabeled CS plus 15N-labeled KNO3 (14CS15NO3); (ii) 15N-labeled CS plus unlabeled KNO3 (15CS14NO3); (iii) 15N-labeled CS plus 15N-labeled KNO3 (15CS15NO3) and unlabeled NH4HCO3 plus 15N-labeled KNO3 (Control).
The treatments were applied in a randomized block design with five replicates. Sufficient CS (25 L) for the four experiments was collected in February 1997 from the storage tank underneath the slatted floor of a house containing beef cattle (Bos taurus) at the Agricultural Research Institute of Northern Ireland, Hillsborough, County Down. The CS (90 g kg-1 dry-matter) was passed through a 6-mm sieve and stored at 2°C. For each occasion, a portion of this CS was diluted with water until the dry-matter content was about 50 g kg-1 and then passed through a 1-mm sieve. Either unlabeled urea or urea enriched at 99 atom% 15N was added to aliquots of the CS to double its NH4–N concentration. The slurries were incubated for 3 d at 35°C to hydrolyze the urea to NH4HCO3. Some properties of these slurries are shown in Table 2. Organic C and total N were determined according to Ministry of Agriculture, Fisheries and Food (1981). Volatile fatty acids (VFAs) were determined by gas chromatography using a 10 m by 0.53 mm column of Carbowax 20M (Hewlett Packard HP-20M, Palo Alto, CA) at 90°C and flame ionization detection.
View this table:
[in this window]
[in a new window]
|
Table 2. Properties of the urea-amended cattle slurries used for studying their interaction with fertilizer NO3 on four occasions in 1997.
|
|
The rate of CS application was 22 m3 ha-1 (100 mL per enclosure) to supply 60 kg NH4–N ha-1 either at natural abundance in 15N or enriched at 52 atom% in 15N. Ammonium bicarbonate served as a control, supplying no degradable C but the same amount of water and NH4–N as CS. It was applied in an aqueous solution (100 mL per enclosure) to supply 60 kg N ha-1 at natural abundance. Potassium nitrate was applied in an aqueous solution (100 mL per enclosure) to supply 60 kg N ha-1 either at natural abundance in 15N or enriched at 52 atom% in 15N. The 15N-labeled KNO3 was purified of any 15NO2 according to Malone and Stevens (1998). The day prior to the application of treatments, the grass within each enclosure was clipped to a height of 20 mm above the soil surface and removed. The aliquots of fertilizer and CS solutions were applied uniformly over the soil surface within each enclosure using a 100-mL pipette. Potassium nitrate was added first, followed 2 min later by CS (or NH4HCO3).
Flux Measurement
Fluxes of N2, N2O, and CO2 were measured 6, 25, 32, 49, 56, 73, 80, 97, and 104 h after the treatments were applied for each occasion. Twenty enclosures (240-mm i.d.) consisting of a base and lid were used for every experiment. The base section was 120 mm in depth and was inserted 100 mm into the soil 4 wk prior to the start of each experiment. The lid was 30 mm in depth and was fitted with a gas sampling port. When the lid was in place, the headspace volume was 
3 L. The exact volume of each base section was determined at the end of each experiment by filling it with dry sand. At each sampling time the lid of the enclosure was fitted to the base section using a rubber band (40 mm wide) to form a gas-tight seal. After 2 h, samples of the headspace of each enclosure were taken using a gas-tight syringe fitted with a push-button value. A 12-mL sample was transferred to an evacuated (<100 Pa), septum-capped, 12-mL vial for the analysis of N2 and N2O. A 5-mL sample was transferred to a He-filled, 10-mL vial for the analysis of CO2. The isotopic composition of the N2, and the concentration and isotopic composition of the N2O were determined by continuous-flow isotope-ratio mass spectrometry (Stevens et al., 1993). A Europa Scientific 20-20 Stable Isotope Analyser with Trace Gas Preparation System (PDZ Europa, Crewe, England) and Gilson autosampler (Anachem, Luton, England) were used for all 15N analyses. The automation of valve switching and source setting facilate the analysis of N2 and N2O in the same sample. The concentration of CO2 was determined using a Varian 3800 Gas Chromatograph fitted with a thermal conductivity detector and autosampler (Varian, Walton-on Thames, England).
The flux of N2O was calculated from the change in N2O concentration with time. Cumulative fluxes were calculated by integration, assuming linear change in flux rates between observation times. The flux of N2 was calculated assuming that the labeled N2 evolved into the headspace was derived from the same single, uniformly-labeled NO3 pool as the N2O. The fraction of labeled N2 in the headspace (dN2) was calculated from the difference in 30R (30N2/28N2) between normal and enriched headspace (
30R) and the mole fraction of 15N in the NO3 pool (15XN) according to the equation of Mulvaney (1984).
 | (1) |
The isotopic composition of the N2O was used to apportion the N2O flux between nitrification and denitrification, and to calculate the enrichment of the denitrifying NO3 pool. When N2O is derived from nitrification of the NH4 pool at natural abundance and from denitrification of the uniformly-labeled NO3 pool, the distribution of 15N atoms within the N2O molecules in the mixture is nonrandom. The extent of the nonrandomness is reflected in the molecular ratios for N2O of 45R (45N2O/44N2O) and 46R (46N2O/44N2O). Using 45R and 46R, the enrichment of the denitrifying pool pool (aD) and the fraction of the N2O derived from this pool (dN2O) were calculated from the equations of Arah (1997). The value of 15XN was taken to be the same as that for aD.
Statistical Analysis
Analysis of variance was carried out using Genstat (1993) 5 to determine the significance of treatments on the fluxes of N2O, N2, and CO2, the enrichment of the N2O, dN2O, and aD.
|
RESULTS AND DISCUSSION
|
|---|
Effect of Cattle Slurry on the Fluxes of Nitrous Oxide and Dinitrogen
The flux of N2O was independent of the 15N-labeling in the CS treatment. Therefore the effects of the constituents of the CS, apart from NH4 and water, over all three treatments (14CS15NO3, 15CS14NO3, and 15CS15NO3) were averaged to compare with the control treatment (14NH4HCO3 15NO3). Cattle slurry increased the flux of N2O at each occasion of application, the effects being greatest immediately after application (Fig. 1). Effects persisted for up to 56 h in March and May, but <24 h in August and September. On average over the 104 h of observation, the cumulative flux of N2O with CS was higher by a factor of 4.9 in March, 3.4 in May, 1.9 in August, and 1.8 in September relative to the control (Table 3). The maximum flux was always measured in the first measurement period (5–7 h) after CS application. The impact of CS on N2O flux would have been missed entirely in August and September, if there had been no measurements until 24 h after application. High fluxes immediately after CS application have been recorded in other studies. Fluxes up to 1800 g N ha-1 d-1 (536 µmol N m-2 h-1) from CS supplemented with NH4NO3 were measured the day after application compared to a flux of 400 g N ha-1 d-1 (119 µmol N m-2 h-1) for NH4NO3 alone (Clayton et al., 1997). In wet soil, N2O emissions increased to >1 kg N ha-1 d-1 (298 µmol N m-2 h-1) immediately following the application of NH4NO3 and slurry, but decreased rapidly after 2 to 3 d. (McTaggart et al., 1997).
View larger version (14K):
[in this window]
[in a new window]
|
Fig. 1. The mean effect of cattle slurry (CS) (average of 14CS15NO3, 15CS15NO3, and 15CS14NO3 treatments) on the flux of N2O when applied at the same time as KNO3 to grassland on four occasions in 1997. (LSD values are for comparing any two means at P < 0.05).
|
|
View this table:
[in this window]
[in a new window]
|
Table 3. Cumulative fluxes of N2O, N2, and N2O plus N2 evolved in the 104 h after the application of cattle slurry and fertilizer NO3 to grassland on four occasions during 1997.
|
|
The flux of N2 can only be measured when the NO3 pool is labeled. In this study the measurement of 30R in N2 and fluxes of N2 were not significantly different between the 14CS15NO3 and 15CS15NO3 treatments (Table 4). Hence, the effects of the constituents of CS, apart from NH4 and water, over these two treatments were averaged to compare with the control treatment (14NH4HCO3 15NO3). On all four occasions, CS had no significant effect (P > 0.05) on the flux of N2 at any individual measurement time (Fig. 2). Cumulative fluxes, however, were significantly lower with CS on three of the four occasions (Table 3). On average over the 104 h of observation, the cumulative flux of N2 with CS was not significantly different from the control in Mar. but was 60% of the control in May, 71% in August, and 74% in September. The inhibition in N2 emission after CS application was balanced by increased N2O emission so that the total N-gas fluxes (N2O + N2) were the same as the controls in August and September (Table 3). In May, the increased N2O emission after CS application outweighed the inhibition of N2 flux so that the total N-gas flux was higher than the control. In March, the N2 flux after CS application was not significantly different from the control, but the increased N2O emission resulted in a significantly higher total N-gas flux.
View this table:
[in this window]
[in a new window]
|
Table 4. Effect of labeling the NH4 pool in cattle slurry on the average values for the enrichment and flux of N2 evolved from labeled NO3 on four occasions in 1997.
|
|
View larger version (14K):
[in this window]
[in a new window]
|
Fig. 2. The mean effect of cattle slurry (CS) (average of 14CS15NO3, and 15CS15NO3 treatments) on the flux of N2 when applied at the same time as KNO3 to grassland on four occasions in 1997. (LSD values are for comparing any two means at P < 0.05).
|
|
Sources of Nitrous Oxide and Dinitrogen
Using the procedure of Arah (1997), the flux of N2O was partitioned between nitrification and denitrification for one CS treatment (14CS15NO3) and the control treatment (14NH4HCO3 15NO3). Values for dN2O were not significantly different from one in March, May, and September 1997, indicating that all of the N2O was derived from the NO3 pool (Table 5). In August, 6% of the N2O was derived from the natural abundance pool for the control treatment, and 10% for the CS treatment. Nitrification is assumed to be the process responsible for producing N2O at natural abundance, with denitrification producing the N2O enriched in 15N. Denitrification was therefore the dominant process producing N2O at all times. Application of CS increased soil respiration (Fig. 3) and hence the chance of NO3 being used as the terminal-electron acceptor instead of O2. The VFAs contained in the slurry (Table 2) have been shown to be readily available C sources for heterotrophic denitrifiers (Paul and Beauchamp, 1989a).
View this table:
[in this window]
[in a new window]
|
Table 5. The fraction of the N2O flux (dN2O) derived from the labeled pool of NO3 in the 104 h after the application of cattle slurry and fertilizer NO3 to grassland on four occasions during 1997.
|
|
View larger version (17K):
[in this window]
[in a new window]
|
Fig. 3. The mean slurry-induced flux of CO2 (average of 14CS15NO3, 15CS15NO3, and 15CS14NO3 treatments corrected for flux from the control) over four applications of cattle slurry (CS) when applied at the same time as KNO3 to grassland in 1997.
|
|
Pool sizes were not measured, therefore definitive rates of mineralization, immobilization and nitrification could not be calculated. Assuming, however, that pool sizes changed little during the gas-flux measurement period, the occurrence of nitrification and mineralization can be inferred from the rate of dilution of the labeled NO3 pool. The enrichment of the labeled pool, aD, from which the N2O was derived by denitrification, was calculated for all treatments containing 15NO3 (Fig. 4). Nitrification appeared to occur in all treatments as indicated by the decreasing enrichment of the denitrifying pools. There was less pool dilution in the 14CS15NO3 treatments than in the control treatments, probably because CS delayed the onset of nitrification. Such a delay has been reported previously (Paul and Beauchamp, 1989b) and was thought to be due to the O2 stress created by the oxidation of readily available substrates such as VFAs. All CS treatments in our study contained VFAs (Table 2) and increased soil respiration after application (Fig. 3). Values for aD in the 15CS15NO3 treatment decreased with time but at a slower rate than in the 14CS15NO3 treatment for each application. Mineralization was therefore occurring as well as nitrification. All rates of change of enrichment were faster in August than at other times. Native soil NH4 concentrations were higher in August than at other times (Table 1), again indicating that N transformation rates were fastest at this time.
View larger version (17K):
[in this window]
[in a new window]
|
Fig. 4. The effect of labeling the NH4 pool in cattle slurry (CS) at 52 atom% 15N on the rate of dilution of the NO3 pool in soil, enriched by the application of KNO3 containing 52 atom% 15N at the same time to grassland on four occasions in 1997. (LSD values are for comparing any two means at P < 0.05).
|
|
Direct evidence that nitrification was occurring from the mineral NH4–N pool rather than the organic-N pool was provided by the data for enrichment of N2O from the 15CS14NO3 treatment (Fig. 5). The calculation of Arah (1997) was not applicable to the data from this treatment because the pool from which most of the N2O was derived was initially not labeled. The enrichment of the N2O always increased with time. Since denitrification was the dominant process producing N2O, nitrification must have oxidized 15N-labeled NH4 to 15N-labeled NO3, and hence, gradually enriched the NO3 pool from which denitrification was occurring. Although nitrification always occurred, it only contributed to N2O flux in August (Table 5). It was not possible to distinguish between autotrophic and heterotrophic nitrification as heterotrophic nitrifiers can oxidize either NH4–N or organic-N (Kuen and Robertson, 1994). The conditions conducive to producing N2O from nitrification are high temperature and 50 to 65% water-filled pore space (Linn and Doran, 1984). Conditions in August in our study (Table 1) were therefore most favourable to N2O formation during nitrification.
View larger version (15K):
[in this window]
[in a new window]
|
Fig. 5. The enrichment of N2O evolved when cattle slurry with its NH4 pool enriched at 52 atom% 15N and unlabeled KNO3 were applied at the same time to grassland on four occasions in 1997. (LSD values are for comparing means within application times at P < 0.05).
|
|
Processes Producing Nitrous Oxide and Dinitrogen
The production of N2 during heterotrophic nitrifier denitrification (Kuen and Robertson, 1994; Richardson et al., 1998) or by other microbial processes such as anaerobic ammonium oxidation (Jetten et al., 1997), was ascertained by comparing the flux from the 15CS15NO3 treatment with that from the 14CS15NO3 treatment. Since the NH4 and NO3 pools were enriched to the same extent in the 15CS15NO3 treatment, any N2 flux from either pool into the headspace will be regarded by the 15N gas–flux method as being derived from a single uniformly-labeled pool. Headspace analyses for 15N in N2 showed that there was no significant difference between the 15CS15NO3 treatment and the 14CS15NO3 treatment in any application (Table 4). There was therefore, no evidence for N2 formation directly from the 15NH4 pool by heterotrophic nitrifier denitrification or anaerobic ammonium oxidation. In heterotrophic nitrifier denitrification, nitrification products (NO2 and NO3) are reduced to N2O and N2 as soon as they are generated (Kuen and Robertson, 1994; Richardson et al., 1998). In anaerobic ammonium oxidation, NH3 and NO2 or NO3 combine directly into N2 (Jetten et al., 1997). Bacteria capable of this anaerobic oxidation of NH3 have only recently been identified in nature (Strous et al., 1999). In our study, all N2 was formed by reduction of the NO3 pool, presumably by respiratory denitrification in anaerobic microsites.
Nitrous oxide was also formed predominantly by denitrification. The application of CS increased the mole fraction of N2O (Table 3). The overall average for the mole fraction of N2O in the control treatment was 0.31, which was similar to the value of 0.25 reported for grassland in Southern England (Ryden, 1981). The denitrification process is diverse, being performed in aerobic and anaerobic conditions by bacteria, and in anaerobic conditions by fungi. In bacteria, the first step in denitrification is catalyzed by a membrane-bound NO3 reductase (NAR) and a periplasmic NO3 reductase (NAP) (Bell et al., 1990). Both are active in anaerobic conditions but NAP is the only enzyme active in aerobic conditions. This aerobic denitrifying ability is widespread among soil bacteria (Carter et al., 1995). The second step in denitrification is catalyzed by N2O-reductase. Both NAP and NAR could be expressed in conditions of O2 stress such as after CS application. As there is a time lag between the expression of NAP or NAR and N2O-reductase, the mole fraction of N2O will tend to increase when NO3 is available (Letey et al., 1980). Alternatively, in aerobic conditions if NAP was expressed because of the need to metabolize reduced C substrates such as VFAs (Sears et al., 1997), then N2O would be the only product of NO3 reduction. Many fungi have the ability to denitrify but most lack N2O-reductase (Shoun et al., 1992). Hence, if fungi dominated the microbial population, their metabolism would contribute to the production of N2O only. The relative importance of each of these processes cannot be ascertained in our study.
Relevance to Emission Factors
The annual IPCC emission factor for N2O in the absence of manure is 1.25% of the mineral N applied as fertilizer (Mosier et al., 1998). In this study the pulse of N2O derived from fertilizer NO3 in the 104 h after application was 0.29% without CS and 0.92% with CS on average overall applications (Table 2). A CS application could therefore increase the annual emission factor for fertilizer N by 0.63% giving a total annual emission factor of 1.88%. Such effects would be sufficient to warrant advisory recommendations to avoid the practice of applying NO3 fertilizer at the same time as organic manures. Further work on the interaction between organic manure and fertilizer is needed to devise mitigation strategies.
Received for publication February 21, 2000.
|
REFERENCES
|
|---|
- Arah, J.R.M. 1997. Apportioning nitrous oxide fluxes between nitrification and denitrification using gas-phase mass spectrometry. Soil Biol. Biochem. 29:1295–1299.
- Bell, L.C., D.J. Richardson, and S.J. Ferguson. 1990. Periplasmic and membrane-bound respiratory nitrate reductases in Thiosphaera pantotropha. FEBS Lett. 265:85–87.[ISI][Medline]
- Bouwman, A.F. 1990. Exchange of greenhouse gases between terrestrial ecosystems and the atmosphere. p. 61–127. In A.F. Bouwman, (ed.) Soils and the greenhouse effect. John Wiley & Sons, New York.
- Carter, J.P., Y.H. Hsiao, S. Spiro, and D.J. Richardson. 1995. Soil and sediment bacteria capable of aerobic nitrate respiration. Appl. Environ. Microbiol. 61:2852–2853.[Abstract]
- Clayton, H., I.P. McTaggart, J. Parker, L. Swan, and K.A. Smith. 1997. Nitrous oxide emissions from fertilized grassland: A two-year study of the effects of N fertilizer form and environmental conditions. Biol. Fert. Soil 25:252–260.
- Ellis, S., S. Yamulki, E. Dixon, R. Harrison, and S.C. Jarvis. 1998. Denitrification and N2O emissions from a UK pasture soil following the early spring application of cattle slurry and mineral fertilizer. Plant Soil 202:15–25.
- Firestone, M.K., and E.A. Davidson. 1989. Microbiological basis of NO and N2O production and consumption in soil. p. 7–21. In M.O. Andreae and D.S. Schimel (ed.) Exchange of trace gases between terrestrial ecosystems and the atmosphere. John Wiley & Sons, New York.
- Firestone, M.K., R.B. Firestone, and J.M. Tiedje. 1980. Nitrous oxide from soil denitrification: Factors controlling its biological production. Science (Washington DC) 208:749–751.[Abstract/Free Full Text]
- Granli, T., and O.C. B
ckman. 1994. Nitrous oxide from agriculture. Norwegian J. Agric. Sci. 12(suppl.):1–128. Norsk Hydro Research Centre, Porsgrunn.
- Jetten, M.S.M., S. Logemann, G. Muyzer, L.A. Robertson, S. de Vries, M.C.M. van Loosdrecht, and J.G. Kuenen. 1997. Novel principles in the microbial conversion of nitrogen compounds. Antonie van Leeuwenhoek 71:75–93.[ISI][Medline]
- Genstat. 1993. Reference manual 5 release 3.1. Statistics Dept., Rothamsted Exp. Stn., Hertfordshire, England (ed.). Oxford Univ. Press, Oxford, UK.
- Klemedtsson, L., B.H. Svensson, and T. Rosswall. 1988. A method of selective inhibition to distinguish between nitrification and denitrification as sources of nitrous oxide in soil. Biol. Fert. Soil 6:112–119.
- Kuenen, J.G., and L.A. Robertson. 1994. Combined nitrification-denitrification processes. FEMS Microbiol. Rev. 15:109–117.
- Letey, J., N. Valoras, A. Hadas, and D.D. Focht. 1980. Effect of air-filled porosity, nitrate concentration and time on the ratio of N2O/N2 evolution during denitrification. J. Environ. Qual. 9:227–231.[Abstract/Free Full Text]
- Linn, D.M., and J.W. Doran. 1984. Effect of water-filled pore on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci. Soc. Am. J. 48:1267–1272.[Abstract/Free Full Text]
- McTaggart, I.P., J.T. Douglas, H. Clayton, and K.A. Smith. 1997. Nitrous oxide emission from slurry and mineral nitrogen fertilizer applied to grassland. p. 201–209. In S.C. Jarvis and B.F. Pain (ed.) Gaseous nitrogen emissions from grassland. CAB International, Oxford, UK.
- Malone, J.P., and R.J. Stevens. 1998. Removal of nitrite impurity from nitrate labeled with nitrogen-15. Soil Sci. Soc. Am. J. 62:651–653.[Abstract/Free Full Text]
- Ministry of Agriculture, Fisheries and Food. 1981. The analysis of agricultural materials. Her Majesty's Stationary Office, London, England.
- Mogge, B., E.A. Kaiser, and J.C. Munch. 1999. Nitrous oxide emissions and denitrification N-losses from agricultural soils in the Bornhöved Lake region: Influence of organic fertilizers and land-use. Soil Biol. Biochem. 31:1245–1252.
- Mosier, A., C. Kroeze, C. Nevison, O. Oenema, S. Seitzinger, and O. van Cleemput. 1998. Closing the global N2O budget: Nitrous oxide emissions through the agricultural nitrogen cycle: OECD/IPCC/IEA phase II development of IPCC guidelines for national greenhouse gas inventory methodology. Nutr. Cycl. Agroecosyst. 52:225–248.
- Mulvaney, R.L. 1984. Determination of 15N-labeled dinitrogen and nitrous oxide with triple-collector mass spectrometers. Soil Sci. Soc. Am. J. 48:690–692.[Abstract/Free Full Text]
- Paul, J.W., and E.G. Beauchamp. 1989a. Effect of carbon constituents in manure on denitrification in soil. Can. J. Soil Sci. 69:49–61.
- Paul, J.W., and E.G. Beauchamp. 1989b. Biochemical changes in soil beneath a dairy cattle slurry layer: The effect of volatile fatty acid oxidation on denitrification and soil pH. p. 261–270. In J. Hansen and K. Henriksen (ed.) Nitrogen in organic wastes applied to soils. Academic Press, London.
- Renault, P., and P. Stengel. 1994. Modeling oxygen diffusion in aggregated soils: 1. Anaerobiosis inside the aggregates. Soil Sci. Soc. Am. J. 58:1017–1023.[Abstract/Free Full Text]
- Richardson, D.J., J.M. Wehrfritz, A. Keech, L.C. Crossman, M.D. Roldan, H.J. Sears, C.S. Butler, A. Reilly, J.W.B. Moir, B.C. Berks, S.J. Ferguson, A.J. Thomson, and S. Spiro. 1998. The diversity of redox proteins involved in bacterial heterotrophic nitrification and aerobic denitrification. Biochem. Soc. Trans. 26:401–408.[ISI][Medline]
- Ryden, J.C. 1981. N2O exchange between a grassland soil and the atmosphere. Nature 292:235–237.
- Sears, H.J., S. Spiro, and D.J. Richardson. 1997. Effect of carbon substrate and aeration on nitrate reduction and expression of the periplasmic and membrane-bound nitrate reductases in carbon-limited continuous cultures of Paracoccus denitrificans Pd1222. Microbiol. 143:3767–3774.
- Shoun, H., D.H. Kim, H. Uchiyama, and J. Sugiyama. 1992. Denitrification by fungi. FEMS Microbiol. Lett. 94:277–282.
- Smith, K.A. 1980. A model of the extent of anaerobic zones in aggregated soils, and its potential application to estimates of denitrification. J. Soil Sci. 31:263–277.
- Stevens, R.J., and R.J. Laughlin. 1997. The impact of cattle slurries and their management on ammonia and nitrous oxide emissisions from grassland. p. 233–256. In S.C. Jarvis and B.F. Pain (ed.) Gaseous nitrogen emissions from grassland. CAB International, Oxford, UK.
- Stevens, R.J., R.J. Laughlin, G.J. Atkins, and S. Prosser. 1993. Automated determination of nitrogen-15-labeled dinitrogen and nitrous oxide by mass spectrometry. Soil Sci. Soc. Am. J. 57:981–988.[Abstract/Free Full Text]
- Stevens, R.J., R.J. Laughlin, L.C. Burns, J.R.M. Arah, and R.C. Hood. 1997. Measuring the contributions of nitrification and denitrification to the flux of nitrous oxide from soil. Soil Biol. Biochem. 29:139–151.
- Strous, M., J.A. Fuerst, E.H.M. Kramer, S. Logemann, G. Muyzer, K.T. van de Pas-Schoonen, R. Webb, J.G. Kuenen, and M.S.M. Jetten. 1999. Missing lithotroph identified as new planctomycete. Nature 400:446–449.[Medline]
This article has been cited by other articles:
|
|
|
|
 
Y. Master, R. J. Laughlin, U. Shavit, R. J. Stevens, and A. Shaviv
Gaseous Nitrogen Emissions and Mineral Nitrogen Transformations as Affected by Reclaimed Effluent Application
J. Environ. Qual.,
July 1, 2003;
32(4):
1204 - 1211.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Laughlin and R. J. Stevens
Evidence for Fungal Dominance of Denitrification and Codenitrification in a Grassland Soil
Soil Sci. Soc. Am. J.,
September 1, 2002;
66(5):
1540 - 1548.
[Abstract]
[Full Text]
[PDF]
|
|
|
|
|
|
|
R. J. Stevens and R. J. Laughlin
Cattle Slurry Applied Before Fertilizer Nitrate Lowers Nitrous Oxide and Dinitrogen Emissions
Soil Sci. Soc. Am. J.,
March 1, 2002;
66(2):
647 - 652.
[Abstract]
[Full Text]
[PDF]
|
|
|
TOP
ABSTRACT
INTRODUCTION
