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Soil aeration affects the degradation rate of the nitrification inhibitor dicyandiamide.

Introduction

Dicyandiamide (DCD; [C.sub.2][H.sub.4][N.sub.4]) is a nitrification inhibitor. The efficacy of DCD in pasture systems, and of nitrification inhibitors in general, has been reported to vary (Linquist et al. 2012; O'Connor et al. 2012). In soils, DCD is susceptible to biodegradation (Ulpiani 1906; Hauser and Hasclwandter 1990); thus, in soils, the activity of the microbial community and the longevity of DCD are connected. Soil microbial activity is affected by interactions with the physical environment. For example, temperature can govern microbial activity and influence the half-life of DCD in soil (Kim et al. 2012; Kelliher et al. 2014). Microbial activity can also be affected by the availability of water in soils. Orchard and Cook (1983) reported that, under conditions of unlimited substrate availability, soil microbial activity, in the form of respiration rate, was directly proportional to soil gravimetric water content and soil matric potential ([psi]). In general, microbial activity and the respiration rate both decrease with increasing water content (e.g. Franzluebbers 1999; Beare et al. 2009; Gabriel and Kellman 2014). However, interactions between water availability and substrate supply, and other factors such as aeration, can change the relationship (Schjonning et al. 2003; Moyano et al. 2012; Harrison-Kirk et al. 2013; Moyano et al. 2013). Varying soil aeration can change soil microbial community function; denitrifiers are a classic example of organisms that respire under anaerobic conditions, to reduce nitrate (N[O.sub.3.sup.-]). Such changes in microbial function can also apply to the soil microorganisms that degrade synthetic chemicals in soils (e.g. DCD).

The efficacy of DCD as a nitrification inhibitor will depend on its concentration and persistence in the soil. For example, recent trials in New Zealand have shown soil DCD concentrations declining to very low or undetectable levels within 8-12 weeks of DCD application (Kim et al. 2012; de Klein et al. 2014; Ledgard et al. 2014); however, this period has been observed to extend up to 17-18 weeks in some seasons or regions (Gillingham et al. 2012; de Klein et al. 2014). This extended period is assumed to be the result of cooler soil temperatures slowing the degradation of the DCD (Kelliher et al. 2008; de Klein et al. 2014). The degradation of DCD in soils has previously been linked with microbial activity (Reddy 1964).

Controlled and detailed experiments examining the factors affecting the degradation of DCD in soil are few, and there have been no detailed experiments examining the effect of aeration on DCD degradation. The only results relating to soil aeration effects and DCD degradation appear to be from a laboratory experiment suggesting that DCD degraded more slowly in soils under anaerobic than aerobic conditions (Vilsmeier 1991), and a field trial suggesting that DCD degraded faster in soil nearer the surface than deeper in the profile where it was wetter, and where there was less organic matter (Corre and Zwart 1995). Neither of these studies quantified DCD degradation rates. Here we report the results of a laboratory experiment in which DCD concentrations in the soils were measured directly, in order to test the null hypothesis that the rate of DCD degradation in soil would be the same under aerobic and anaerobic conditions.

Material and methods

Experimental design and set-up

Silt loam soil (Wakanui series, Udic Ustochrept; Hewitt 1998) was collected (0-15 cm) from a tillage trial, Lincoln, New Zealand (43[degrees]40'03.91"S, 172[degrees]28'11.76"E 5 m a.s.l.). This trial commenced in 2000 with the aim of identifying tillage and cover-crop practices for maintaining soil organic matter following the conversion of long-term pasture to arable cropping (Fraser et al. 2013). Soil was collected from two sites (A and B) within this trial, which, for the past 14 years, had differing cropping histories. Site A was a control plot maintained under a grass sward, whereas site B was a permanent fallow. The sites were selected to obtain soil samples with contrasting management but the same parent material. At both sites, the soil texture was sand 33%, silt 48%, and clay 19%. Additional soil properties at the two sites are provided in Table 1. Soil from each site was air-dried and sieved to <2 mm. Soil cores were then constructed by packing sieved soil into stainless-steel rings (internal diameter 7.3 cm) to a bulk density of 1.1 Mg [m.sup.-3] and depth of 4.1 cm. Treatments included soil site (A or B) and four levels of matric potential ([psi]: -1.0, -3.0, -6.0 and -10 kPa), replicated four times. Soil cores were arranged in a randomised block design on tension tables. Before placing soil cores on the tension tables at the designated [psi] levels, 232 soil cores were pre-saturated with a DCD solution (30 [micro]g [mL.sup.-]) to obtain soil DCD concentrations, following 24-h drainage, ranging from 6.6 to 11.1 mg [kg.sup.-1] soil. These are typical of concentrations found in the soil following DCD application (Cameron et al. 2014; de Klein et al. 2014). In addition, 64 control cores were saturated with deionised water. Eight of the DCD-treated soil cores (four replicates of each soil, A and B) were destructively sampled on day 0 to measure soil DCD concentrations immediately after saturation. The remaining DCD-treated soil cores (224) were subsampled on days 1, 4, 8, 12, 20, 30 and 40 by taking 32 soil cores (2 sites x 4 levels of [psi] x 4 replicates). Thirty-two control soil cores (2 sites x 4 levels of [psi] x 4 replicates) were destructively sampled on both day 1 and day 40. In total, 296 soil cores were made. During the experiment, the laboratory air temperature (mean [+ or -] s.d.) was 22[degrees]C [+ or -] 2[degrees]C.

Measurements

To assess soil aeration, measurements of relative [O.sub.2] diffusivity (Dp/Do) were performed using the method of Rolston and Moldrup (2002), described by Balaine et al. (2013). In brief, a calibrated [O.sub.2] sensor (KE-25; Figaro Engineering Inc., Osaka, Japan) was placed in a chamber that was then purged until anaerobic by using an Ar (90%) and [N.sub.2] (10%) gas mixture, with the base of the soil core isolated from the chamber. Once anaerobic, the soil core was exposed to the [O.sub.2]-fee chamber atmosphere. Oxygen diffusing through the soil core into the chamber was recorded as a function of change in concentration over time. Consumption of [O.sub.2] was considered negligible (Moldrup et al. 2000). Regression analysis of the log-plot of relative [O.sub.2] concentration v. time enabled Dp ([O.sub.2] diffusion coefficient in soil) to be calculated according to Rolston and Moldrup (2002). All diffusivity calculations were performed at 25[degrees]C and the value of Do ([O.sub.2] diffusion coefficient in air) at 25[degrees]C was calculated to be 0.074 [m.sup.2] [h.sup.-1] (Currie 1960). Relative gas diffusivity was expressed as Dp/Do.

To determine the pore-size distribution, a water-retention curve (WRC) was fitted to a plot of volumetric water content ([theta], [cm.sup.3] [cm.sup.-3]) v. [psi] (kPa). Using the method of Campbell (1974), including logarithmic transformation followed by linear regression, the value of parameter b was determined according to the following equation:

[psi] = [[psi].sub.e]([theta]/[[theta].sub.s]) (1)

where [[psi].sub.e] is the air-entry value and [[theta].sub.s] is the saturated water content. Following Campbell (1974), we combined Eqn 1 with a capillary rise equation, [psi] = -2[gamma]/r, where [gamma] is a ratio of water's surface tension and density, and r is an 'effective' or 'narrowest channel' pore radius (Hillel 1982), to estimate four values of r associated with decreasing [psi] from saturation ([psi] = 0) through each of the four levels applied as treatments.

Measurements of DCD concentration were performed by extracting 5-g subsamples (oven-dry equivalent) of soil with 25 mL of deionised water. The extract was then shaken for 1 h on an end-over-end shaker followed by centrifugation at 4000 rpm for 20 min. The supernatant was then filtered using a Whatman Grade 42 grade filter paper (GE Healthcare, Little Chalfont, UK) with particle retention to 2.5 [micro]m, followed by another filtration with Phenomenex syringe filters (Phenomenex, Torrance, CA, USA) with a particle retention size of 0.22 [micro]m. Then an HPLC system (Prominence; Shimadzu Corp., Kyoto, Japan) comprising a degasser (DGU-20A3), liquid chromatograph (LC-20AB), auto sampler (SIL-20A HT), UV/vis detector (SPD-20A), and column oven (CTO-20A) was used for the analyses. The column was a Rezex RHM-Monosaccharid (50 by 7.80 mm; Phenomenex) and the eluent was 0.0025 m H2S04. The flow rate was 1 mL [min.sup.-1] and the analysis temperature was 45[degrees]C. The detector wavelength was 210 nm and the injection volume 50 [micro]L. The standards were made from high-purity dicyandiamide (99%; Sigma-Aldrich, St. Louis, MO, USA) in a deionised water matrix to establish an appropriate standard curve.

Data analyses

For each treatment, a first-order exponential function was fitted to the time-series of the DCD concentrations as follows:

C(t) = [C.sub.o][e.sup.-kt] (2)

where C is the concentration of DCD (mg kg ') at time t (days), [C.sub.o] is the initial DCD (mg [kg.sup.-1]) concentration, and k is the degradation constant ([day.sup.-1]). The soil cores were initially saturated with either the DCD solution or deionised water, and because it took nearly 4 days to reach the designated [psi] levels, as determined from gravimetric measurements, the DCD concentrations measured on days 0 and 1 were not included when fitting the exponential function to the data. Half-life ([t.sub.1/2]) values were calculated as follows:

[t.sub.1/2] = Ln (0.5)/-k (3)

Data were checked for normality using the Anderson-Darling test in Minitab version 16 (Minitab Inc., State College, PA, USA), and if they deviated from normality, they were log-transformed before analysis. However, the Figures and Tables present the raw data. The 95% confidence level was considered statistically significant. Analysis of variance was performed using the General Linear Model in Minitab version 16.

Results

No DCD was detected in the controls. Initial DCD concentrations in soil cores receiving DCD, measured on days 0 and 1, along with the respective [theta] values are provided in Table 2. Values of [theta] from day 4 to day 40 remained constant for soil from both sites. Mean (and standard deviation) values of [theta] for site A at -10, -6.0, -3.0 and -1.0kPa were 0.24 (0.01), 0.30 (0.01), 0.37 (0.02) and 0.47 (0.02) [cm.sup.3] [cm.sup.-3], respectively; for site B, corresponding values were 0.25 (0.01), 0.30 (0.01), 0.36 (0.01) and 0.47 (0.02) [cm.sup.3] [cm.sup.-3], with no difference due to site.

Because [theta] did not differ with soil site, the WRC was fitted by using data from both sites (Table 3). Fitting Eqn 1 to the WRC data yielded values for [[psi].sub.e] and b of 0.055 [+ or -] 0.009 and -3.514 [+ or -] 0.447, respectively. Pore-size distribution showed that 33% of the soil volume had pores with an 'effective' diameter >30 [micro]m, 6% 30-50 [micro]m, 7% 50-100 [micro]m, 9% 100-300 [micro]m, and 11% >300 [micro]m.

Following Welten et al. (2012), DCD recovery from both sites was estimated in order to check for adsorption due to variation in soil organic matter content. Estimated DCD recovery was 91.2% for soil A with 5.34% organic matter and 92.8% for soil B with 3.44% organic matter. Concentrations of DCD in soil from both sites decreased exponentially with time from day 4 to day 40 for all levels of matric potential (Fig. 1 a, h). Higher DCD concentrations (P<0.05) were observed under wetter soil conditions (-1.0 kPa) throughout the measurement period. Values of the estimated parameters ([C.sub.o] and k) derived from the regression analysis and measured Dp/Do values at different [psi] levels are shown in Table 4. For each site, the soil matric potential ([psi]) affected the degradation (k) constant, with lower values at -1.0kPa (P<0.05). When values of k were compared between sites A and B for each level of [psi], values were higher (P<0.05) for site A at -10 and -6.0 kPa (Fig. 2). Thus the calculated half-life of DCD at site A increased as soil became wetter, with values (mean [+ or -] standard error) of 15.4 [+ or -] 2.4, 16.9 [+ or -] 2.8, 21.0 [+ or -] 3.4, and 27.6 [+ or -] 3.5 days at -10, -6.0, -3.0 and -1.0kPa, respectively. For soil from site B, the DCD half-life also increased as soil became wetter with corresponding values of 22.4 ([+ or -] 5.8), 23.1 ([+ or -] 4.4), 24.7 ([+ or -] 4.8), 31.5 ([+ or -] 5.5) days. Measured values of Dpi Do increased as matric potential became more negative; however, Dp/Do was not affected by soil site (Table 4).

[FIGURE 1 OMITTED]

[FIGURE 2 OMITTED]

Discussion

Soil DCD concentrations measured in the present study were of the same order of magnitude as observed previously under in situ pasture conditions (Wakelin et al. 2013; Cameron et al. 2014; de Klein et al. 2014; Kim et al. 2014; Ledgard et al. 2014). DCD is a chemically stable substance with Henry's constant estimated to be 2.3 x [10.sup.-10] atm [m.sup.3] [mol.sup.-1] (OECD 2003), which suggests that DCD volatilisation from moist soil surfaces should not occur (Lyman et al. 1990). Moreover, comparison of DCD recovery from both sites calculated following Welten et al. (2012) suggests that there was no significant difference due to adsorption of DCD on organic matter. Thus, the disappearance of DCD in soil can be attributed to chemical and/or microbial degradation. Amberger and Vilsmeier (1979a) showed that DCD could be degraded in the presence of metal oxides to guanylurea; therefore, abiotic degradation of the DCD cannot be ruled out in the present experiment, and further sterile treatments would be required to ascertain the importance of such a pathway. It is possible that pre-treatment (drying and sieving) altered the microbial community structure and function, and with no pre-incubation, there may have been an initial flush of microbial activity. However, the DCD degradation rates, calculated from day 4 to day 40, showed no effect of such an initial flush of microbial activity (Fig. 1).

Degradation of DCD in situ is known to be linked to soil temperature and observed degradation rates, and the calculated DCD half-life values for this study at -10kPa and 22[degrees]C in soil from both sites compare well with the value derived from the data synthesis performed by Kelliher et al. (2008). However, the present study also showed that measured DCD degradation rates became lower as Dp/Do--a measure of soil aeration-- decreased. Stepniewski (1981) provided a threshold for anaerobic conditions in soil and suggested that soils start to become anaerobic when Dp/Do is within the range 0.02-0.005. Likewise, Cook et al. (2013) developed an analytical solution to show that as soil air-filled porosity declines, the oxygen concentration reaches zero at progressively shallower depths. Air-filled porosity, soil water content and pore continuity interact to affect Dp/Do, which is a direct measure of a soil's capacity for gaseous exchange. The range of Dp/Do values obtained in the present study at -1.0 and -3.0kPa (0.01-0) fell within the 'anaerobic' range described by Stepniewski (1981). Conversely, the Dp/Do values for soil from sites A and B show that the soil was aerobic at -6.0 and -10kPa (Table 3). Under these aerobic soil conditions, the half-life of DCD was shorter (larger degradation rate constant (k) in soil from site A; Fig. 2). In the present experiment, degradation of DCD clearly increased as soil conditions became more aerobic. Similarly, in wetter soils, DCD degraded more slowly according to Amberger and Vilsmeier (1988) and Kim et al. (2011). Thus, the null hypothesis that the rate of DCD degradation in soil would be the same under aerobic and anaerobic conditions is rejected.

Differences between soils taken from sites A and B included higher pH, soil carbon and organic matter at site A (Table 1), which potentially resulted in differences in soil microbial community structure and function, nutrient availability and microbial biomass. Thus, when conditions were aerobic, one or more of these factors evidently also caused the faster rate of DCD degradation in the soil from site A. Under aerobic soil conditions, oxygen is used as an electron acceptor in biochemical processes to degrade organic matter (Reddy and DeLaune 2008). Consequently, increased soil aeration enhances organic matter decomposition via the promotion of aerobic microorganism activity. Few studies have examined the degradation of DCD under varying levels of organic matter. Puttanna et al. (1999) added fresh organic matter (undecomposed dried and ground residue from steam distillation of citronella, Cymbopogon sp.) to a sandy loam soil of pH 8.3 at a rate of 1000 mg [kg.sup.-1] soil, with DCD applied at a rate of 10 mg [kg.sup.-1] soil, and incubated the mixture at 30[degrees]C. No change in DCD efficacy was observed. However, Amberger and Vilsmeier (19796) found that DCD decomposed faster at high soil organic matter contents. Reddy (1964) also proposed that DCD decomposed faster as organic matter content increased, on the basis that ammonium was found to nitrify faster in a sandy soil with 0.9% organic matter than in a sandy loam with 0.3% organic matter maintained at 27[degrees]C. However, DCD concentration in the soil was not directly measured over time, and faster DCD degradation was inferred by reduced DCD efficacy (Reddy 1964). To clarify this finding, Reddy (1964) ran another experiment using sucrose as a source of organic matter and concluded from the increased rate of nitrification observed in the presence of sucrose that sucrose was able to provide soil microorganisms with energy to utilise the DCD as a source of nitrogen, thus reducing its concentration and efficacy.

The present experimental measurements of DCD degradation rate constants, which appear to be the only such measurements in soils under controlled aeration conditions, clearly show that DCD is degraded faster when conditions are aerobic. The fact that DCD also degraded faster in the soil from site A, which had a higher percentage of organic matter, supports earlier findings showing that DCD efficacy is reduced when more soil organic matter is present. However, controlled studies with soils varying over a wider range of organic matter concentrations are required to verify this supposition.

The possibility cannot be ruled out that the higher soil pH at site A (5.25 v. 5.03 at site B) also promoted DCD degradation. Although microbial processes such as nitrification are enhanced with liming (e.g. Clough et al. 2004), few studies have examined DCD efficacy under liming. Reddy (1964) took a soil of pH 5.4 and limed it to pH 8.2, finding that DCD efficacy decreased with liming; the author speculated that the reduced efficacy was due to increased nitrification activity and/or more rapid degradation of the inhibitor via enhanced microbial activity. In the present study, the pH difference between the soils from sites A and B was only 0.2 units, compared with the difference of 2.8 units in the study of Reddy (1964), and no nitrogen was added to stimulate nitrification activity. Thus, the main influence on the higher degradation rate of DCD in soil from site A under aerobic conditions was probably the variation in soil organic matter and any associated differences in microbial biomass and community structure that ensued.

Nitrification inhibitors such as DCD have been utilised to lessen the deleterious effects of intensive pasture production. Efficacy of DCD has been measured in terms of reductions in nitrous oxide ([N.sub.2]O) emissions and N[O.sub.3.sup.-] leaching. Efficacy of DCD varies; for example, a series of trials over 3 years at four geographically distinct locations in New Zealand found that DCD reduced [N.sub.2]O emissions by 14-82% and N03 leaching by up to 74% (Cameron et al. 2014; de Klein et al. 2014; Kim et al. 2014; Ledgard et al. 2014), and Bameze et al. (2015) found that DCD reduced [N.sub.2]O emissions by 33% under summer grazing conditions in the United Kingdom. Variation in DCD efficacy has been attributed to soil temperature differences (Kelliher et al. 2008), the timing and frequency of DCD applications (Ledgard et al. 2014) and the potential for DCD to leach (Monaghan et al. 2009). The results of the present experiment clearly show that soil aeration is another factor that should also be considered in the efficacy of DCD for reducing N losses from pasture systems. When DCD is applied to well-aerated soils, its lifetime will be shorter than in wet soils, all other factors being constant. In reality, however, drier soils may also be warmer soils and there may be interactive effects influencing DCD longevity and efficacy in soil. Further studies should also examine these environmental interactions.

Conclusions

When the soil was wettest, matric potential was -1.0 kPa, Dp/Do was zero, and the DCD degradation rate was the minimum measured (half-life of 27.6-31.5 days and degradation rate constant of 0.022-0.025 day-1). By decreasing the matric potential to -10kPa, Dp/Do increased to 8% of the free-air value and the DCD degradation rate increased by 80% in a soil with 5.3% organic matter and by 41% in a soil with identical parent material but with 3.4% organic matter (half-life 15.4-22.4 days and degradation rate constant of 0.031-0.045 [day.sup.-1]). These results help to explain the observed variability in the efficacy of the nitrification inhibitor DCD and have implications for predicting efficacy and designing DCD treatments (rates and timing) with respect to soil type and rainfall regimes when seeking optimal nitrification inhibition in agricultural ecosystems.

Received 27 June 2014, accepted 29 September 2014, published online 24 February 2015

http://dx.doi.org/10.1071/SR14162

Acknowledgements

Funding was provided by the Ministry for Primary Industries, New Zealand. We thank Mike Beare and Craig Tregurtha for their help with soil collection. We thank Joy Jiao and Teresa Symon Parayil for their help with DCD analysis.

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N. Balaine (A,C), T. J. Clough (A), F. M. Kelliher (A,B), and C. van Koten (B)

(A) Department of Soil and Physical Sciences, Lincoln University, Lincoln 85084, New Zealand.

(B) AgResearch, Lincoln Research Centre, Private Bag 4749, Christchurch 8140, New Zealand.

(C) Corresponding author. Email: nimleshn@lincoln.ac.nz
Table 1. Selected properties of soil from sites A and B
Values are the mean (n = 4, unless stated otherwise),
with standard deviations in parentheses

Soil properties            Soil A        Soil B

pH                       5.25 (0.03)   5.03 (0.04)
Organic matter (%)       5.34 (0.26)   3.44 (0.09)
Total carbon (%)         3.10 (0.14)   2.00 (0.05)
Total nitrogen (A) (%)      0.30          0.30

(A) Analysis performed on bulk samples at a commercial
laboratory (Hill Laboratory, Hamilton, New Zealand; n = 1).

Table 2. Soil DCD concentrations and volumetric water contents
(6) measured on day 0 and after 1 day at varying matric potentials
Values in parentheses are standard deviations (n = 4)

                                   Day 1

            Day 0         -10 kPa       -6.0 kPa

DCD (mg [kg.sup.-1] soil)

Site A   14.84 (0.86)   7.08 (0.28)   8.41 (0.13)
Site B   15.12 (1.21)   6.63 (0.21)   8.53 (0.34)

[theta] ([m.sup.3] [m.sup.-3])

Site A   0.56 (0.10)    0.37 (0.01)   0.42 (0.01)
Site B   0.52 (0.02)    0.36 (0.01)   0.41 (0.01)

                    Day 1

          -3.0 kPa       -1.0kPa

DCD (mg [kg.sup.-1] soil)

Site A   9.40 (0.33)   11.10 (0.38)
Site B   9.99 (0.38)   10.78 (0.34)

[theta] ([m.sup.3] [m.sup.-3])

Site A   0.44 (0.01)   0.51 (0.02)
Site B   0.44 (0.01)   0.50 (0.01)

Table 3. Volumetric soil water content ([theta]) at five levels of
matric potential ([psi]) and the corresponding 'effective' pore
diameter drained, as explained in the text

[psi] (kPa)   [theta] ([m.sup.3]     Pore diameter
                 [m.sup.-3])       drained ([micro]m)

0                    0.57
-1.0                 0.46                 300
-3.0                 0.37                 100
-6.0                 0.30                  50
-10                  0.24                  30

Table 4. Regression parameters ([C.sub.o] and k) and measured Dp/Do
values for soil from sites A and B

Values in parentheses are standard deviations for Dpi Do, and
standard errors of the estimate derived from the regressions
performed in Fig. 1 for [C.sub.o] and k. Within a column, means
followed by the same letter are not significantly different at P =
0.05

Matric                             Soil A
potential      [C.sub.o]             k
(kPa)       (mg [kg.sup.-1])   ([day.sup.-1])       Dp/Do

-10          7.43a (0.22)      0.045a (0.002)   0.07a (0.008)
-6.0         8.69b (0.26)      0.041a (0.002)   0.03b (0.004)
-3.0         8.90b (0.24)      0.033b (0.002)   0.01c (0.003)
-1.0        11.45c (0.22)      0.025c (0.001)        Od

Matric                             Soil B
potential      [C.sub.o]             k
(kPa)       (mg [kg.sup.-1])   ([day.sup.-1])       Dp/Do

-10           6.96a (0.27)     0.031a (0.003)   0.08a (0.005)
-6.0          7.65b (0.24)     0.029a (0.002)   0.03b (0.003)
-3.0          9.03c (0.24)     0.029a (0.002)   0.01c (0.002)
-1.0         10.52d (0.23)     0.022b (0.001)        Od
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Author:Balaine, N.; Clough, T.J.; Kelliher, F.M.; van Koten, C.
Publication:Soil Research
Article Type:Report
Date:Mar 1, 2015
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