Published in J. Environ. Qual. 33:1647-1652 (2004).
© ASA, CSSA, SSSA
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TECHNICAL REPORTS
Ecological Risk Assessment
Quantification of the Effect of Fumigation on Short- and Long-Term Nitrogen Mineralization and Nitrification in Different Soils
Stefaan De Nevea,*,
Gabor Csitárib,
Joost Salomeza and
Georges Hofmana
a University of Gent, Department of Soil Management and Soil Care, Division of Soil Fertility and Soil Data Processing, Coupure Links 653, 9000 Gent, Belgium
b Present address: University of Veszprem, Georgikon Faculty of Agronomy, Department of Chemistry and Microbiology, Deák F. u. 16, 8360 Keszthely, Hungary
* Corresponding author (Stefaan.DeNeve{at}UGent.be).
Received for publication July 3, 2003.
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ABSTRACT
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The effect of soil fumigation on N mineralization and nitrification needs to be better quantified to optimize N fertilizer advice and predict NO–3 concentrations in crops and NO–3 leaching risks. Seven soils representing a range in soil texture and organic matter contents were fumigated with Cyanamid DD 95 (a mixture of 1,3-dichloropropane and 1,3-dichloropropene). After removal of the fumigant, the fumigated soils and unfumigated controls were incubated for 20 wk and N mineralization and nitrification were monitored by destructive sampling. The average short-term N mineralization rates (ks) were significantly larger in the fumigated than in the unfumigated soils (P = 0.025), but the differences in ks between fumigated and unfumigated soils could not be related to soil properties. The average long-term N mineralization rates (kl) were slightly larger in the fumigated soils but the difference with the unfumigated soils was not significant. Again, the differences in kl values could not be related to soil properties. Nitrification was inhibited completely for at least 3 wk in all soils, and an effect on nitrification could be observed up to 17 wk in one soil. An S-shaped function was fitted to the nitrification data corrected for N mineralization, and both the rate constant (
) and the time at which maximum nitrification was reached (tmax) were strongly correlated to soil pH. However, since no correlations were found between the effect of fumigation on N mineralization and soil properties, taking into account the effects of fumigation in fertilizer advice and in the prediction of NO–3 leaching risks will need further research.
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INTRODUCTION
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IN CROPPING SYSTEMS where crops are grown in monoculture or in short rotations with little diversification, the pressure from soil-borne pests and diseases is often very high. This is the case, for example, in intensive vegetable rotations, especially in protected cultivation. Farmers often resort to soil fumigation to suppress soil-borne pests and diseases without having to diversify the rotation. Fumigants are chemical compounds that act in the gaseous state to destroy pests such as insects, nematodes, arachnids, fungi, and weeds.
Fumigants drastically alter soil biology. After fumigation, respiration is often initially less than in an unfumigated control. However, after some time, the respiration rate of the fumigated soil becomes greater than that of the control. Thus, after that short period, fumigated soil consumes more O2 and evolves more CO2 than the untreated soil. Moreover, fumigants usually cause an immediate increase in the extractable NH+4 content of the soil. In addition to the NH+4 released from the biomass killed by fumigation, the microflora that recolonizes the soil continues to release NH+4 (Jenkinson and Powlson, 1976; Rovira, 1976; Shen et al., 1984). Nitrifying organisms are particularly vulnerable to fumigation, so that NH+4 often remains in an unoxidized form for long periods in fumigated soils. Fumigants also modify the activities of various soil enzymes (Tu, 1994). These changes may be of great importance in crop production.
An extensive amount of literature exists on the fact that the microbial community following the fumigation event may differ greatly from the original community in its ability to decompose organic matter and to perform N transformations, both in the short and long term (e.g., Bloem et al., 1994; Malkomes, 1995; Stevenson et al., 2000; Zelles et al., 1997). However, there has been very little research to quantify these effects. The effects of soil fumigation on N mineralization in the short and long term are important with respect to N fertilizer application rates in the period following the fumigation. A quantification of the short- and long-term effects on N mineralization can be used to adjust N fertilizer advice systems. The effect of fumigation on nitrification is also important from a plant nutrition point of view. Crops grown in soils where the mineral N is to a large extent in the form of NH+4 may have strongly reduced NO–3 concentrations as compared with soils where mineral N is almost completely present as NO–3 (Richardson and Hardgrave, 1992; Steingröver et al., 1993), which is an important quality aspect, for example, for leafy vegetables. The lower NO–3 concentrations are due to the limiting effect of NH+4 on NO–3 uptake by plants, because NH+4 is quickly assimilated to amino acids in the roots (Breteler and Siegerist, 1984). In soils with a large fraction of NH+4, the total N content of, for example, lettuce (Lactuca sativa L.), was not inferior to lettuce grown in soils with a small fraction of NH+4, while the NO–3 concentration in the crop was much smaller. De Temmerman (1995) observed strongly reduced NO–3 concentrations in greenhouse lettuce following soil fumigation with Cyanamid DD 95 due to increased NH+4 concentrations in the soil. The effect of fumigation on nitrification is also important with respect to leaching risks of nitrogen. The larger the fraction of the mineral N that is in the NH+4 form, the smaller the risk for NO–3 leaching.
The aim of this study was to quantify the effect of soil fumigation on N mineralization, in the short and the long term, and on nitrification in different soils and to derive relationships between the effect of fumigation on these processes and soil properties.
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MATERIALS AND METHODS
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Soils
In total, seven soils were selected for this study, to represent a range in soil texture and organic matter content. Soil was sampled from the plow layer in all cases, as in practice the fumigant is injected at about 30 cm under the soil surface to fumigate the plow layer. The soils were sampled in a way to represent major soil types in Flanders (Belgium), namely following the northwest to southeast gradient from the sand region (Soils 1 and 2), over the sandy loam region (Soils 3 and 4) to the loam region (Soils 5, 6, and 7). Soil 1 was taken from a greenhouse, whereas all the other soils were sampled from open arable fields. Detailed soil analytical data are presented in Table 1.
Organic carbon contents were determined by wet oxidation using the method of Walkley and Black (Nelson and Sommers, 1986). Calcium carbonate contents were determined by addition of 0.5 M H2SO4 and back titration of the excess acid with NaOH. Particle size analyses were performed using the pipette method (Gee and Bauder, 1986). The pH was measured potentiometrically both in water and KCl. The pH (H2O) was measured in a 1:5 soil to H2O extract and the pH (KCl) in a 1:2.5 soil to KCl extract. Soil moisture contents at field capacity were measured on undisturbed soil cores using the sand box method at pF = 2 for the more sandy soils (Soils 1–4), whereas for Soils 5, 6, and 7, the pressure membrane method was used (pF = 2.54) (Klute, 1986).
Soil Fumigation Procedure
Soils 1, 2, and 3 had large initial NO–3 concentrations. Because these could interfere with the measurements of N mineralization and nitrification, these soils were leached with distilled water before the start of the experiment. At the start of the experiments, the soil moisture content was adjusted to 70% of field capacity for all soils. The soils were put in plastic tubes (0.19-m i.d. and 0.40-m length; two tubes per soil), which were filled to a height of 0.3 m and were preincubated in these tubes for 3 d. The amount of soil contained in each tube was sufficient for the subsequent incubation procedure. The fumigant used was Cyanamid DD 95 (former name SHELL DD), a mixture of 1,3-dichloropropane and 1,3-dichloropropene, which is mainly used in control of nematodes (Cheroux and Richard-Molard, 1984). This fumigant had been used before in a study on the influence of soil fumigation on NO–3 concentrations in greenhouse lettuce (De Temmerman, 1995). After preincubation, Cyanamid DD 95 was added to one of the two tubes for each soil in amounts corresponding to normal application rates (500 L ha–1). The second tube was not treated with Cyanamid DD 95 and was used as control. This resulted in a total of 14 treatments (one fumigated and one unfumigated treatment for each of the seven soils). All tubes were then sealed air tight and stored at a temperature of 23°C for 1 wk. After this incubation, the soil was removed from the tubes and was taken to a ventilation hood to remove the fumigant. Ten days were allowed for the removal of the Cyanamid DD 95 and during this period moisture content was adjusted every 2 d.
Incubation Procedure
A plant biotest with water cress (Nasturtium officinale R. Br.) was performed after 10 d in the fumigated treatments and proved the removal of the fumigant. The soil was then re-incubated as follows. Moist soil (equivalent to 250 g oven dry soil) was put into plastic tubes (0.046-m diameter and 0.18-m length). The soils were then compacted manually (De Neve and Hofman, 2000) to obtain a target bulk density, depending on the soil type (1.4 Mg m–3 for Soils 1–4, 1.35 Mg m–3 for Soils 5 and 6, and 1.25 Mg m–3 for Soil 7). Mineral N fertilizer was added to all tubes at a rate of 44.4 mg N kg–1 (in the form of dissolved NH4NO3), equivalent to between 167 and 186 kg N ha–1 (depending on the bulk density) when calculated for a 30-cm layer. After fertilizer addition, the tubes were sealed with gas-permeable Parafilm to prevent excessive water loss and incubated at 23°C for 20 wk. Weights of the tubes were recorded at the start of the incubation to allow adjustment of the soil water content if needed. Samples were taken at the end of Weeks 1, 2, 3, 4, 6, 8, 10, 12, 16, and 20. Sampling was done by removing intact tubes in triplicate. The soil was removed from the tubes and mixed thoroughly, and duplicate samples of soil (30 g) were shaken with 1 M KCl (1:2 extraction ratio) for 1 h on a rotational shaker. Then the soil slurries were filtered and NO–3–N and NH+4–N were measured colorimetrically using a continuous flow autoanalyzer (ChemLab System 4; ChemLab Instruments, Hornchurch, UK). Nitrate was reduced to NO–2 using NO–3 reductase from E. coli as catalyst (Beernaert et al., 1987), which after formation of a diazocompound was measured at 520 nm. Ammonium was reacted with sodiumsalicylate and sodiumdichloroisocyanurate to give a blue color that was measured at 650 nm. Water content of the soil in each tube was determined by oven-drying at 105°C until constant weight.
The statistical analyses were performed using SPSS for Windows (SPSS, 1999). All nonlinear curve fittings were performed using the Levenberg–Marquardt algorithm.
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RESULTS AND DISCUSSION
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Effects on Nitrogen Mineralization
Net N mineralization here is defined as the net increase of soil mineral N content 
over a given period. Net N mineralization rates were much higher in the fumigated soils than in the unfumigated soils during the first weeks of incubation, and after Week 4 the differences tended to become smaller (Fig. 1 and 2). Soil fumigation has been shown to increase short-term N mineralization rates, due to mineralization of microbial biomass killed during fumigation, which is the basis for the fumigation–incubation method for measuring soil microbial N (Jenkinson and Powlson, 1976). The same short-term effect was observed in this experiment (without addition of microbial inoculum), with higher initial amounts of NH+4–N at the start of the incubation in the fumigated soils and with a marked increase in net N mineralization during the first weeks of the incubation (except in Soil 5). The increase in mineral N concentrations in the fumigated soils as compared with the unfumigated soils was in the same range for all soils (between 5.6 and 10.0 mg N kg–1 soil), except for Soil 5 (increase of 23.9 mg N kg–1 soil) (Table 2). This indicates that microbial biomass was comparable in all soils except Soil 5, which seemed to have much higher microbial biomass.
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Table 2. Mineral N concentrations at the start of the incubation (Nmin,start), mineral N contents at the end of the incubation (Nmin,end), and short- (ks) and long-term (kl) N mineralization rates in the unfumigated (U) and fumigated (F) soils.
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We wanted to look at possible differences in N mineralization between fumigated and unfumigated soils in both the short and long term. Knowledge about this long-term effect is important, for example, with respect to optimizing N supply and N use efficiency for the crop grown following the fumigation. We therefore distinguished between two phases of N mineralization for the quantitative analysis, namely a short-term phase (from the start of the incubation until Week 4) and a long-term phase (from Week 5 until the end of the experiment).
We assumed zero-order kinetics for N mineralization in both treated and untreated soils and for both short- and long-term N mineralization:
 | [1] |
 | [2] |
where N(t) (mg N kg–1 soil) is the mineral N content as a function of time, k is the mineralization rate (mg N kg–1 soil d–1), N0 (mg N kg–1 soil) is a constant, and the subscripts s,u, s,f, l,u, and l,f stand for short- and long-term N mineralization in the unfumigated and fumigated treatments, respectively. Differences in the amounts of N mineralized between fumigated and unfumigated soils thus consisted of three terms: the difference in mineral N concentrations in the fumigated and unfumigated soils at the start of the incubation (i.e., 10 d after the removal of the fumigant), which is a result of the NH+4–N released as a direct result of the fumigation, and the differences in short- and long-term N mineralization rates (ks and kl).
The short-term N mineralization rates were larger in the fumigated than in the unfumigated soils, except for Soil 5 (Table 2). A paired samples t test showed that the average difference in ks value (0.201 mg N kg–1 soil d–1) was significant at P = 0.025. The short-term N mineralization in the unfumigated soils ks,u was positively correlated (P = 0.01) with the soil organic matter content and negatively with the percentage of clay (P = 0.09). In the fumigated soils there was a positive correlation between ks,f and the percentage of sand (P = 0.09) and a negative correlation with the percentage of silt (P = 0.09). There were large variations in the value of ks,f – ks,u between soils, but these differences were not correlated to soil properties. The long-term N mineralization rates kl were on average slightly larger (0.034 mg N kg–1 soil d–1) in the fumigated soils as compared with the unfumigated soils, but this difference was not significant (P > 0.1). Again, the values of kl,f – kl,u between soils were highly variable, but no significant correlations were found between these differences and basic soil properties. Fumigation had a dramatic effect on N mineralization for some soils, but in other soils there was no effect at all. In the silt loams (Soils 5 and 6), long-term mineralization rates were identical in both fumigated and unfumigated soils. In the light-textured soils, fumigation effects seemed to be dependent on soil organic matter contents, stimulating long-term N mineralization in soils with high organic matter content (Soils 1 and 3), but reducing the mineralization rate in low organic matter soils (2 and 4). In the loam soil (Soil 7), fumigation caused a very large increase in long-term N mineralization.
When we assume that no N losses occurred, the difference in mineral N concentrations between fumigated and unfumigated treatments at the end of the incubation represents the overall effect of fumigation on N mineralization. The average mineral N concentrations in the fumigated soils at the end of the incubation were significantly larger (18.6 mg N kg–1 soil, P = 0.018 for paired samples t test) from the concentrations in the unfumigated soils, but with large variations between soil types; for example, in Soil 4 the mineral N concentrations in both treatments at the end of the incubation were identical, that is, the increase in short-term N mineralization was compensated by a decrease in long-term N mineralization. These results suggest that fumigation would need to be considered, even over long periods (>20 wk), when calculating the contribution of organic N mineralization of a particular soil to the N supply of a subsequent crop. Again, no significant correlations could be found between soil properties and the difference in mineral N between fumigated and unfumigated soils at the end of the incubation, hence it will not be easy to predict the actual effect of fumigation on increase in available soil N in a particular soil.
Effect on Nitrification
In normal, well-aerated soils the ammonification is the rate-limiting step in the mineralization process, and only trace amounts of NH+4–N are found. In the unfumigated soils practically all NH+4–N (derived from added NH4NO3 and from N mineralization) had been nitrified within 1 wk, and NH+4–N levels fell back to below 2.5 mg N kg–1 throughout the rest of the incubation (data not shown). Only in the loam soil (Soil 7) was there a slightly higher NH+4–N content at the end of the first week. Fumigation depressed nitrification in all treated soils compared with the untreated soils, although there were important differences in duration of nitrification inhibition between the soils (Fig. 3). Draycott and Last (1971) reported a nitrification inhibition lasting up to 4 mo under field conditions on the addition of a dichloropropane- and dichloropropene-containing fumigant in a loamy sand soil. Tu (1993)(1994) observed an inhibition of nitrification of only 3 wk in a sandy loam soil fumigated with a dichloropropane–dichloropropene mixture during incubations in the laboratory. These differences in period of inhibition reported in literature were probably associated with differences in soil properties. In this study, nitrification was completely inhibited for at least 3 wk in all soils (complete inhibition lasted up to 7.5 wk in Soil 3) when the 10-d preincubation period was taken into account (Fig. 3). It took a minimum of 9 wk before the effect of fumigation on nitrification had disappeared completely, but an effect on nitrification was observed up to 17 wk after the fumigation in Soil 6. In general, nitrifying organisms tended to recover faster in soils that had higher organic matter content or were heavier textured, with Soil 3 as a notable exception to this general trend.
It is important in many situations to be able to quantify the partitioning of the mineral N in soil between NH+4 and NO–3 forms as a function of time, for example, in relation to NO–3 content in vegetable crops and risks of NO–3 leaching. To reveal quantitative relationships between soil properties and inhibition of nitrification we described the nitrification in the fumigated soils mathematically.
However, to assess the effect of fumigation on nitrification, first we isolated the nitrification of the NH+4–N present in the soil at the start of nitrification from the additional nitrification of NH+4–N produced as a result of mineralization of soil organic N. Indeed, the evolution of NO–3–N concentrations as given in Fig. 3 not only depends on nitrification of NH+4–N present at the start of the incubation, but also on the mineralization rate of organic N in the different soils. The soils had very different mineralization rates (Fig. 1 and 2), and these could mask the pure nitrification effect. To compare nitrification in the fumigated soils without interference of additional N mineralization during the incubation, the NO–3–N concentrations in Fig. 3 were transformed as follows: the mineralization at a given time t from the start of the incubation (t0 = 0) was calculated as the difference between mineral N at the time t (Nmin,t) and mineral N at time 0 (Nmin,0) using the data from Fig. 2. The NO–3–N concentrations were corrected using these mineralization data, but only starting from the point of maximum NH+4–N content, that is, starting from the onset of nitrification (Fig. 3). The correction was done by subtracting a fraction of the mineralized N at time t, namely a fraction proportional to the amount of NH+4–N already nitrified at t, hence proportional to the ratio:
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where NH+4–Nmax is the maximum NH+4–N content, NH+4–Nt is the NH+4–N content at time t, and NH+4–Nmin is the background NH+4–N content (for t values large enough). The results of this transformation are given in Fig. 4. These graphs represent the nitrification of the NH+4–Nmax present in the soils, excluding the confounding effects of additional N mineralization. An S-shaped function was fitted to the transformed data of NO–3–N in fumigated soils (Fig. 4):
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where 
(mg N kg–1 soil) is the total amount of N nitrified excluding nitrification of N mineralized during the incubation, ß is a dimensionless quantity that determines the position of the inflection point, (wk–1) is a rate constant, and NO–3–N
(mg N kg–1 soil) is the NO–3–N content at the start of the incubation, that is, at t = 0 (Table 3). The time at which maximum nitrification occurred (tmax) was calculated by taking the second-order derivative of Eq. [4] and yielded:
 | [5] |
Substitution of tmax in the first-order derivative of Eq. [4] yielded the maximum nitrification rate (mg N kg–1 soil wk–1):
 | [6] |
The time of maximum nitrification is an important parameter to evaluate the length of the effect of fumigation on nitrification inhibition, which could be used to predict effects of soil fumigation on NO–3 contents in crops or on NO–3 leaching risks. The maximum nitrification rate and the time at which the maximum nitrification rate is reached are inversely related, which seems logical. In soils where fumigation has the longest effect on nitrifying bacteria, nitrification appears to restart more gradually (smaller maximum nitrification rate), and at a later time (longer time before maximum nitrification rate is reached).
Regression analysis was used to evaluate the influence of basic soil properties on the nitrification parameters in the fumigated soils. We used a stepwise linear regression procedure with the following criteria: the probability of the statistic F to enter a variable was set at 0.05, the probability of F to remove a variable was set at 0.1. As the parameter in Eq. [4] depends on the initial amount of NH+4–N present in the soil, this parameter was disregarded. The parameter ß could not be correlated to any of the measured soil properties. For the rate parameter , the regression analysis showed that the pH (KCl) alone explained a very large portion of the variance:
 | [7] |
The other soil properties included in the regression analysis explained only a very small additional portion of the residual variance, and did not improve the regression significantly. The value of the parameter tmax was also determined almost completely by the pH (KCl) (showing a negative correlation), and other soil properties again did not improve the regression significantly:
 | [8] |
Although the soils used in this study had normal pH values encountered in agricultural soils, the pH was still the main determining soil property in the prediction of the parameters and tmax. This means that, while the pH did not limit nitrification in unfumigated soils, it determined the recovery of nitrifying organisms in the fumigated soils. Including more soils may yield predictive relations for the parameter ß as well, which would allow us to predict the partitioning between NO–3–N and NH+4 as a function of time based on basic soil properties.
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CONCLUSIONS
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We can conclude that both mineralization of N and nitrification were strongly affected by fumigation in the soils studied here. Although the effect of fumigation on N mineralization strongly varied between the soils, this effect could not be related to basic soil properties, and it will therefore not be easy to take full account of fumigation in N fertilizer advice systems. Key parameters of the S-shaped nitrification model were strongly related to soil pH, but if the effect of fumigation on ammonification in soil cannot be predicted first, then the prediction of the partitioning between NH+4–N and NO–3–N concentrations by the nitrification model only has a relative value.
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ACKNOWLEDGMENTS
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This research has been carried out through a research grant in the framework of the Flemish–Hungarian Bilateral Agreement on Higher Education, granted by the Department of Education of the Ministry of the Flemish Community.
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ABSTRACT
INTRODUCTION
