Soil Biology & Biochemistry 111 (2017) 44e59

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Soil Biology & Biochemistry

journal homepage: www.elsevier.com/locate/soilbio

Quantifying in situ and modeling net nitrogen mineralization from soil

organic matter in arable cropping systems
Hugues Clivot a, *, Bruno Mary a, Matthieu Vale
b, Jean-Pierre Cohan c, Luc Champolivier d,
Franois Piraux c, Franois Laurent c, Eric Justes e, **
a
INRA, UR 1158 AgroImpact, site de Laon, F-02000 Barenton-Bugny, France
b
AUREA, F-45160 Ardon, France
c
ARVALIS - Institut du V
eg

etal, F-91720 Boigneville, France
d
Terres Inovia, Centre INRA de Toulouse, CS 52627, F-31326 Castanet-Tolosan Cedex, France
e
INRA, UMR INRA/INPT 1248 AGIR, Auzeville, CS 52627, F-31326 Castanet-Tolosan Cedex, France

a r t i c l e i n f o a b s t r a c t

Article history: Improved assessment and prediction of net nitrogen mineralization (NNM) from soil organic matter in
Received 24 October 2016 eld conditions are essential for a better management of nitrogen (N) in arable cropping systems and an
Received in revised form accurate simulation of its seasonal dynamics. The rst objective of this study was to quantify accurately
6 March 2017
NNM rates by combining measurements of soil water and mineral N contents in soil prole, daily
Accepted 15 March 2017
weather data and the LIXIM calculation model (Mary et al., 1999). The second objective was to develop a
predictive model of in situ NNM rates based on basic soil properties and to evaluate if additional factors
related to cropping history, organic matter fractions or microbial biomass could improve the model
Keywords:
Modeling
performance.
Nitrogen mineralization We selected a set of 65 eld experiments representative of arable cropping systems in France which
Soil organic matter were carried out in bare fallow soils without recent addition of crop residue (minimal delay of 4 months)
Field experimental dataset or organic amendment. In these experiments, soil water and mineral N contents were monitored over
LIXIM model the soil prole (0e90 to 0e150 cm depth, 3 to 5 layers) during 100e555 days (median value of 272 days).
Cropping history LIXIM was able to satisfactorily simulate water (EF 0.58) and mineral N contents (EF 0.80) in the
several layers, allowing to disentangle the two main processes involved in mineral N changes: NNM
(occurring in the upper soil layer) and nitrate transfer (through the whole soil prole). The actual NNM
rates varied widely between sites from 0.13 to 1.10 kg N ha1 day1. The potential NNM rates (Vp),
calculated under standard conditions of water and temperature, varied between 0.17 and
1.67 kg N ha1 nday1 (nday normalized day at 15  C and eld capacity).
A novel model with a multiplicative structure and a sequential approach was developed by including
functions explaining the relationship between mineralization rate Vp (predicted variable) and explana-
tory variables. Soil organic N (SON) was the most correlated variable with Vp (r 0.51, p < 0.001) and the
rst variable introduced in the model as a linear function. Non-linear functions of soil clay content, pH, C/
N ratio and CaCO3 content were successively introduced, leading to a soil model based on ve basic soil
parameters that allowed explaining 61% of the variance in Vp. Two functions relative to the frequency of
rapeseed and legumes in rotations were found to further improve the predictive quality of the soil model,
explaining nally 72% of Vp variance (soil-history model). Organic matter fractions (particulate or
extractible organic matter) did not explain signicantly more variance of Vp due to their strong corre-
lations with SON. Microbial biomass explained only 2% additional variance in Vp compared to the soil-
history model. The predictive error of prediction (RMSEP) varied between 0.22, 0.19 and
0.17 kg N ha1 nday1 for the soil (n 65), soil-history (n 65) and soil-history-biological (n 47)
models. This multiplicative, non-linear approach performed better than a multiple linear regression
approach which explained 10e15% less variance of Vp when using the same explanatory variables.

* Corresponding author.
** Corresponding author.
E-mail addresses: clivot.hugues@hotmail.fr (H. Clivot), eric.justes@inra.fr (E. Justes).

http://dx.doi.org/10.1016/j.soilbio.2017.03.010
0038-0717/ 2017 Elsevier Ltd. All rights reserved.
 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
The models based on soil properties and cropping history could be further implemented in multi-
disciplinary soil-crop models and decision support systems in order to enhance the prediction of N
dynamics in soils and improve fertilizer recommendations.
1. Introduction
Prediction of soil nutrient supply to crops is still a major eco-
nomic and environmental concern in agriculture management. In
particular, an accurate simulation of soil Nitrogen (N) mineraliza-
tion is crucial to improve N management in order to match fertilizer
timing and rates with crop N demand, maximize economic effec-
tiveness and minimize mineral N losses to the environment.
In agroecosystems, soil organic matter (SOM) is intimately
linked to many physical, chemical and biological properties
participating in soil quality and productivity (Doran and Parkin,
1994). SOM plays a central role in soil structure, plant available
water capacity (Reeves, 1997) and in sustaining soil fertility
(Kononova, 1966; Tiessen et al., 1994) as the major supplier of N and
other limiting nutrients for plant growth (Smith et al., 2015). N
mineralization from SOM is a process mainly mediated by the ac-
tivities and communities of microorganisms (Bartholomew, 1965;
Jansson and Persson, 1982) which are inuenced by edaphic and
environmental factors and by complex interactions with soil micro-
and meso-fauna (Scheu et al., 2005). Soil physico-chemical pa-
rameters, biological characteristics (Hassink et al., 1993) and cli-
matic conditions, more particularly temperature and moisture
(Cassman and Munns, 1980; Curtin et al., 2012; Guntin ~ as et al.,
2012; Stanford et al., 1973; Stanford and Epstein, 1974), are
known to be important factors to take into account in order to
predict N mineralization from SOM. Agricultural practices such as
tillage, mineral or organic fertilization and residue management
can impact soil N supply (Shari et al., 2014; Spargo et al., 2011; St.
Luce et al., 2011), as well as crop rotation (Carpenter-Boggs et al.,
2000; Senwo and Tabatabai, 2005; Shari et al., 2008; St. Luce
et al., 2016).
Net N mineralization (NNM) resulting from the balance between
gross N mineralization and immobilization by soil microorganisms
is commonly assessed by measuring the rate of inorganic N accu-
mulation in soil. This mineral N pool constitutes both the main
source of N available for crops and the potential N losses through
leaching and gaseous emissions from soil. Laboratory incubations
and chemical indices have been and are still the most common
approaches conducted to determine potential mineralizable N or
NNM rates in soils (Grifn, 2008; Shari et al., 2007). However,
previous works highlighted the difculties to extrapolate results
obtained from these methods to eld conditions (Connell et al.,
1995; Hart and Binkley, 1985). Indeed, differential responses have
been previously observed between eld measurements and incu-
bation methods that have sometimes overestimated (Adams and
Attiwill, 1986; Honeycutt, 1999) or underestimated in situ N
mineralization (Abril et al., 2001). In laboratory experiments, the
diverse soil pretreatments (e.g. sieving, drying, rewetting) applied
prior to incubations under controlled conditions (e.g. temperature
and water content) can strongly inuence SOM mineralization rates
(Benbi and Richter, 2002; Jarvis et al., 1996). As a consequence,
some models with parameters calibrated using laboratory incuba-
tion experiments were found to be poor predictors of both N
mineralization and nitrate leaching under eld conditions (Cabrera
and Kissel, 1988; Johnson et al., 1999). Realistic estimations of N
mineralization are required to improve or develop models able to
45
2017 Elsevier Ltd. All rights reserved.
predict more accurately N supply to plants.
In situ eld experiments appear more labor-intensive but are
needed to provide more realistic estimations of soil N mineraliza-
tion under ambient conditions and by taking into account the ef-
fects of soil architecture. In situ N mineralization can be estimated
from N balance in agricultural elds by determining N uptake by
plants and mineral N variations in soil (Constantin et al., 2011;
Meisinger, 1984). However this method is restricted to the
growing season and is complicated by the need to evaluate accu-
rately N losses to the environment, N remaining in unharvested
parts of crops, in particular roots but also the effects of root exu-
dates, which are rarely measured (Jarvis et al., 1996). Furthermore,
the large uncertainty on measurements does not allow to obtain
accurate estimates of N mineralization kinetics.
Other in situ approaches have been proposed including the
closed buried bags (Eno, 1960; Lehrsch et al., 2016), the covered-
cylinder (Adams et al., 1989; Adams and Attiwill, 1986; Salazar
et al., 2015) and the ion-exchange resins methods (DiStefano and
Gholz, 1986; Turner and Henry, 2010) and more generally in situ
core methods proposed by Raison et al. (1987) and commented in
the review done by Khanna and Raison (2013). The in situ incu-
bation of undisturbed soil samples in bare fallow conditions
cannot integrate the effects of a vegetation cover, but could
represent a good compromise between the objectives of main-
taining realistic eld conditions and reducing the uncertainty of N
mineralization estimates. In this approach, the measured variation
in soil mineral N is attributed mainly to two processes: i) net N
mineralization and ii) N losses, the latter being generally domi-
nated by nitrate leaching. Preventing or assessing nitrate leaching
can be achieved by three methods: a) preventing leaching by
covering the cores, b) using ion exchange resins at the bottom of the
core; c) calculating nitrate leaching using measurements and a
calculation model. Methods a) and b) have been discussed by
Hanselman et al. (2004) who indicated that covering the cores can
modify the water regimes whereas resins may vary in their ef-
ciency for trapping the leached nitrate. Method c) has been
developed by Mary et al. (1999) in another approach combining
measurements and model calculations. The LIXIM calculation
model proposed by these authors was used later in order to
calculate net mineralization and leaching using in situ measure-
ments of water and mineral N contents (Beaudoin et al., 2005; Lesur
et al., 2014; Oorts et al., 2007; Vale
et al., 2007).
In this study, we propose to use the calculation model LIXIM to
estimate NNM rates under actual eld conditions and in
conventional-till cropping systems. LIXIM relies on frequent mea-
surements of water and mineral N contents to calculate minerali-
zation kinetics against true time (i.e. under the climatic conditions
encountered in situ) and normalized time (equivalent time under
standard moisture and temperature conditions; for details, see
Mary et al., 1999). These corrections for soil temperature and
moisture are essential to analyze the role of soil properties on NNM
without the confounding effects of climatic factors. They also allow
the comparison of NNM estimates between eld experiments and
laboratory incubations, as suggested by Ros et al. (2011).
This study was conducted on a network of 65 dedicated eld
experiments representative of most French arable pedo-climatic
46 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59

situations. The rst objective was to calculate the actual N miner-
alization rates derived from soil organic matter expressed per unit
of true time and the potential N mineralization rates expressed per
unit of normalized time (Vp), by combining water and mineral N
content measurements and the LIXIM calculation model. The sec-
ond objective was to design a novel model of Vp prediction based
on simple and routinely measured soil properties and to evaluate if
additional factors related to cropping history or other variables
more complex to acquire, such as organic matter fractions and
microbial biomass, could improve the predictive quality of the
model.
2. Material and methods
The approach used in this study to quantify and model the po-
tential NNM rates (Vp) is presented in Fig. 1.
2.1. Experimental sites and datasets
The 65 eld experiments were carried out between 1990 and
2008. Their location and climate zone are shown in Figure S1. The
mean daily temperature measured during the duration of eld
experiments ranged from 9.1 to 17.8  C and the daily precipitation
ranged from 1.0 to 4.3 mm (Table 1).
The 65 experimental sites exhibited contrasting soil parameters
(Table 1). The clay content of soils ranged from 24 to 396 g kg1
(median value of 191 g kg1), silt content from 55 to 814 g kg1
(median value of 539 g kg1) and sand content from 22 to
895 g kg1 (median value of 184 g kg1). The CaCO3 content of soil
ranged between 0 and 436 g kg1 (median value of 4 g kg1). Soil
pH varied between 5.7 and 8.4 (median value of 7.7). Soil organic C
and N stocks in the topsoil (0e30 cm) also varied widely: from 27.0
to 147.2 t C ha1 (median value of 45.8 t ha1) and 2.6 to
12.6 t N ha1 (median value of 5.0 t ha1), respectively. A com-
parison of the range covered by these pedological conditions with
the French Gis Sol database (estrada.orleans.inra.fr/geosol/)
showed that soils selected in this study were rather well repre-
sentative of the French agricultural conditions (Figure S2).
Since our objective was to assess N mineralization derived from
stabilized SOM and avoid the temporary mineralization/immobili-
zation processes due to organic residues decomposition, the eld
experiments were performed in bare fallow soils without recent
crop residue or organic amendment. They were initiated mostly
between the end of summer and the beginning of winter, either
soon after harvest when crop residues were exported or long time
after returning crop residues to soil (at least 4 months), in order to
avoid the N immobilization phase (e.g. Garnier et al., 2003). Bare
fallow conditions were obtained primarily with herbicides and
secondarily with supercial tillage. All elds had been managed
previously with tillage and regular ploughing over an average
depth of 30 5 cm. Cropping histories varied among elds.
Depending on available information, we were able to retrieve 3 to
10 years of past cropping history. Crops were classied into 6
groups: cereals (wheat, barley, triticale), spring crops (maize,
sorghum, sunower), legumes (pea, soybean, fababean), sugar-
beet, rapeseed and others for minor crops (tomato, onion,
ryegrass). In our study, these groups represented 48%, 29%, 11%, 8%,
3% and 1% of cultivated crops, respectively. Wheat, maize, barley
and pea contributed respectively to 39%, 19%, 8% and 8% of total
crops in rotations.

Table 1
Climatic conditions of eld-experiments and physicochemical, organic matter and
microbial associated characteristics for the upper soil layer (0e30 cm) of the study
sites.

Units Min Max Median Mean SD

Climatic conditions (n 65)


Mean daily temperature C 9.1 17.8 11.7 12.6 2.3
Daily precipitation mm 1.0 4.3 1.9 2.1 0.7
Soil properties (n 65)
Clay g kg1 24 396 191 201 76
Silt g kg1 55 814 539 502 198
Sand g kg1 22 895 184 218 174
CaCO3 g kg1 0 436 4 64 123
pH 5.7 8.4 7.7 7.5 0.8
SOC t ha1 27.0 147.2 45.8 51.7 24.4
SON t ha1 2.6 12.6 5.0 5.3 1.9
C/N 7.2 15.3 9.3 9.6 1.5
Organic matter fractions (n 47)
POM-C t ha1 3.0 25.8 7.0 8.6 5.1
POM-N t ha1 0.17 1.88 0.39 0.50 0.36
EOM-C t ha1 2.7 26.4 7.0 8.3 4.8
EOM-N t ha1 0.39 2.91 0.97 1.12 0.54
Microbial biomass C t ha1 0.32 1.58 0.72 0.75 0.32

Fig. 1. Overall approach used in this study for assessing and modeling potential net SOC: soil organic carbon, SON: soil organic nitrogen, POM: particulate organic
nitrogen mineralization (NNM) rates Vp. matter (>50 mm), EOM: extractable organic matter.
 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
Soil physico-chemical characteristics and cropping history were
recorded for the 65 eld experiments constituting a set of data
called dataset 65. For 47 of these eld experiments, results from
organic matter fractionation and microbial biomass were also
recovered from the top-soils constituting a subset of data called
data subset 47 which includes these additional parameters. De-
tails on climatic conditions, soil parameters and cropping fre-
quencies are provided in Clivot et al. (submitted).
2.2. Soil analyses
2.2.1. Physico-chemical analyses
2.2.1.1. Upper soil layer (0e30 cm). The upper soil layer was
sampled at the beginning of each experiment to measure basic
soil properties. Five to six soil cores were mixed together to obtain a
representative composite soil sample. Particle-size distribution was
determined by the pipette method (NF ISO 11277). Soil carbonate
content was determined by a volumetric method according to NF
ISO 10693. Soil bulk density was measured by the cylinder method
(Blake, 1965) or estimated according to the pedological soil class.
Soil pH was measured in water (1:5 soil/water ratio) (NF ISO
10390). Soil organic C (SOC) was measured by colorimetry after
sulfochromic oxidation (NF ISO 14235). The quantitative determi-
nation of soil organic N (SON) was performed using the modied
Kjeldahl method after sulfuric acid digestion (NF ISO 11261). The
last two methods are well adapted to calcareous soils and previous
work showed that these methods gave similar results as total C and
N measured by the more commonly used Dumas combustion
method (Dimassi et al., 2014). SOC and SON contents as well as
stocks of organic fractions were calculated over the 0e30 cm depth.
This calculation is consistent with the fact that most soils were
frequently moldboard ploughed down to this depth.
2.2.1.2. All soil layers (0e150 cm). Soil water and mineral N con-
tents were regularly measured in 3 to 5 soil layers (30 cm thick)
down to 90, 120 or 150 cm depth, depending on subsoil material.
The duration of the monitoring period varied from 100 to 555 days
(median value of 272 days). The number of sampling dates ranked
from 5 to 23 sampling dates depending on the duration (median
number of 10). Five to six soil cores were mixed to obtain a
representative sample for each replicate, and two or three repli-
cates (i.e. independent blocks) were performed at each sampling
date. Water contents were determined gravimetrically (NF ISO
11465). Soil water content at permanent wilting point (Wwp) was
measured using the Richards pressure plate method at the poten-
tial of 1.6 MPa (NF ISO 11274). Water content at eld capacity
(Wfc) was estimated as the mean of the highest values measured
under eld conditions in winter as described in Mary et al. (1999).
Soil inorganic N was extracted during 30 min with 1 M KCl (1:2 w/v
ratio). Ammonium and nitrate concentrations were determined by
colorimetry using a continuous ow analyzer (Skalar Analytical).
Soil bulk density was measured as described for the upper soil layer
in part 2.2.1.1.
2.2.2. Organic matter fractions
Additional analyses of organic matter fractions were performed
on the upper soil layer collected at the start of experiment in the
subset of 47 eld experiments. Measurements were made on a
representative composite sample made of ve to six soil cores
mixed together. Soil samples were fractionated by wet sieving
under water on a 50 mm sieve. The particulate organic matter
(POM) fraction was recovered on the sieve and separated manually
from the sand particles. It was dried, weighed and crushed before
analyzing C and N contents by the Dumas dry combustion method
using a NA 2000 elemental analyzer (Thermo Electron
47
Corporation). C and N contents of the ne SOM fraction (<50 mm)
were determined by subtracting C and N contents of the POM
fraction from those of the total soil.
The fumigation-extraction method was used to estimate soil
microbial biomass C (Vance et al., 1987). Chloroform-fumigated and
non-fumigated soil subsamples (25 g oven-dry equivalent) were
extracted during 30 min using 25 mM K2SO4 (1:4 w/v ratio) and
ltered (0.45 mm). Dissolved organic C concentrations in extracts
were determined by persulfate oxidation at 100  C with a 1010
Analyzer (OI Analytical). A kEC conversion factor of 0.45 was applied
to convert measured data into microbial biomass (Joergensen,
1996).
Extractable organic matter (EOM) was determined as proposed
by Lemaitre et al. (1995). Soil subsamples (20 g oven-dry equiva-
lent) were extracted during 45 min using 25 mM K2SO4 (1:4 w/v
ratio) and then autoclaved at 121  C and 1 bar during 16 h. After
centrifugation (5 min at 6000g), soluble organic C in supernatant
extracts was determined by UV-persulfate oxidation (Dohrmann
DC 80) yielding EOM-C. Total soluble N (EOM-N) was assessed by
high-temperature combustion with a TN 3000 Analyzer (Euroglas-
Apollo Instruments).
2.3. Calculation of in situ net N mineralization rates
NNM rates were determined by combining measurements of
water and mineral N contents, weather data and calculations by the
model LIXIM, as described by Mary et al. (1999). This daily time-
step model simulates water drainage and evaporation and nitrate
transfer in soil and provides estimates of nitrate leaching and NNM
through time by inverse modeling. Water and solute transport are
modeled using the mixing-cells concept (Van Ommen, 1985),
each soil layer being characterized by its water properties Wwp and
Wfc. An optimization procedure embedded in LIXIM allows looking
for the best t between observed and simulated soil water and
mineral N contents in each layer at each sampling date, by opti-
mizing a few parameters. It allows to disentangle the effects of
nitrate transfer and N mineralization on the variations of soil
mineral N in each layer through time. Denitrication is supposed to
be negligible because no fertilizer-N is added and because nitrate
usually accumulates at soil surface only when the soil gets dry. The
LIXIM model application requires i) the absence of plant cover, ii) a
rather rapid nitrication as commonly encountered in the condi-
tions prevailing in soils of our study sites and iii) multiple mea-
surements of water and mineral N contents through time in at least
three soil layers.
In our study, four parameters were optimized specically for
each experiment: i) the maximum depth affected by soil evapora-
tion (Ze), ii) the evaporation distribution coefcient (a), iii) the
depth of soil layers linked to the dispersivity length (l), and iv) the
maximum depth contributing to mineralization (Zm) which is close
to the ploughing depth. A sensitivity analysis was conducted to test
the effect of varying these parameters on the simulated minerali-
zation rate. It showed that the actual N mineralization rate in soils
Vm (expressed in kg N ha1 day1) was little dependent on the
value of these four parameters as long as the quality of t was close
to the best one.
The actual N mineralization rate in soils is known to be strongly
dependent on soil moisture and temperature. LIXIM model trans-
forms this variable Vm into a potential mineralization rate Vp
(expressed in kg N ha1 nday1) at a specic reference temperature
(15  C) and water content (Wfc). LIXIM simulates the daily soil
water content in the biologically active layer (0-Zm). The normal-
ized time is calculated by taking into account both daily air tem-
perature and simulated soil water content and the temperature and
moisture functions of the LIXIM model (f(T) and g(W), respectively).
48 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
Both rates are linked by the equation:
t Pearson correlation analysis was used rst to identify variables
Vp Vm$
tn
where t represents the true time (day) and tn the normalized time
(nday) dened as follows:
X
t X
Zm
tn f T $g W (2)
n1 z1
Further details can be found in the paper of Mary et al. (1999).
The variable Vp provides estimates of potential N mineralization
rates which are comparable to incubation conditions.
2.4. Data analysis and modeling approach
R Software version 3.3.0 was used for all statistical analyses (R
Core Team, 2016).
2.4.1. LIXIM evaluation and calculation of N mineralization rate
To evaluate the performance of LIXIM model, i.e. the simulated
water and mineral N contents compared to experimental obser-
vations, the root mean squared error (RMSE), the modeling ef-
ciency (EF) (Smith et al., 1996) and the index of agreement (d1)
(Willmott et al., 1985) were calculated as statistical evaluation
criteria for water and nitrogen. The model errors, RMSEs, were also
compared to the measurement errors represented by the standard
deviations (SDs) measured on eld replicates. The cumulative net N
mineralization, M(t) in kg N ha1, calculated by LIXIM was then
tted to each of two models:
- a linear model
Mt Vm$t (3a)
or
Mtn Vp$tn (3b)
- an exponential model
Mt No$1  expk$t (4a)
or
Mtn No$1  expk$tn (4b)
The results showed that the quality of t of both models was
much better described by equations (b) corresponding to Vp than
by equations (a) for Vm, showing that the N mineralization rates
were clearly affected by the variations in water and temperature
regimes and that the effect of these factors was well accounted for
by LIXIM using the functions included in the algorithm. In the
subsequent analysis, we only consider equations (b), i.e. cumulative
mineralization vs normalized time (Vp). Vp is calculated as the slope
of the linear regression between cumulative N mineralized and
normalized time (Equation (3b)) together with its 95% condence
interval. Detailed information on statistical evaluation of LIXIM
simulations and NNM rate calculations is given in Clivot et al.
(submitted).
2.4.2. Designing a novel model for predicting potential N
mineralization rate
(1)
signicantly correlated to potential NNM rates (Vp). These pre-
liminary correlations associated with graphical analyses showed
that either linear or non-linear relationship can perform well
depending on the explanatory variable investigated. We thus chose
to develop an empirical model based on the analysis of the rela-
tionship patterns found between Vp and each explanatory variable
(Vi). We assumed that a model with a multiplicative structure
would be better adapted to reect the nature of the interactive
effects of explanatory variables on soil N mineralization than an
additive linear model used for example in multiple linear regres-
sion (MLR) model. This assumption was tested at the end of the
modeling process by comparing multiplicative and MLR models,
both modeling approaches using the same explanatory variables.
A step-by-step approach was used to include sequentially one
function per step, each function describing the relationship be-
tween Vp and the best remaining explanatory variable to nally
obtain an empirical model with a multiplicative structure as
follows:
b p f V $f V ,,,f V
V (5)
i 1 1 2 2 i i
At each step i, linear and non-linear relationships were assessed
and compared for each newly introduced function Vi. An optimi-
zation procedure (with 10,000 iterations) was used to determine
the parameters associated with each linear or non-linear function
by minimizing the differences between observed and simulated
values. It was performed using the quasi-Newton method of
Broyden, Fletcher, Goldfarb and Shanno (BFGS) implemented in the
general-purpose optimization function optim in R (R Core Team,
2016). After step i, the ratio of observed to simulated N minerali-
Vp
zation rates R (6) was plotted vs each remaining variable Vj
bV pi
(j i 1, n) to identify the variables which could improve both
explanatory and predictive qualities of the model. We selected the
variable Vj which provided the best (linear or non-linear) correla-
tion with the ratio R.
Using this approach, a model was designed by considering
successively variable categories ordered by increasing acquisition
complexity (approach A). We rst developed a model based on
basic and routinely measured soil properties as explanatory vari-
ables (step A1). After reaching the best soil model according to
statistical criteria, optimized parameters were set at xed values
and were further inserted into two additional models. The soil-
history model was developed by adding functions relative to
cropping history variables (step A2). Qualitative data relative to
cropping history were transformed into quantitative variables to
assess the inuence of preceding crops on potential NNM rates.
Two different quantitative variables were calculated and used for
modeling N mineralization rates: i) the crop type frequency in
rotation and ii) an indicator based on the presence or absence of the
crop type in the two preceding years, called Preceding Crop Index
(PCI). Three values were attributed to PCI: 1 for the presence as
preceding crop, 0.5 for ante-preceding crop and 0 for absence
during the two preceding years. As previously performed, param-
eters optimized for cropping history functions were set at xed
values after obtaining the best soil-history model. We chose to
calibrate the soil and soil-history models using data from all ex-
periments (dataset 65) in order to obtain a more robust estimation
of parameters that were set at xed values and further applied to
the subset of 47 eld experiments (data subset 47). Finally, we
attempted to develop a third model including additional variables
related to organic matter fractions and microbial biomass (step A3).
 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
It was evaluated against the data subset 47 which contained these
measurements.
The approach A was confronted to a second sequential multi-
plicative approach in which all explanatory variables were
considered together without categorizing (approach B). The com-
parison was made on the data subset 47 which included all
measurements.
2.4.3. Predictive model evaluation: statistical criteria and
sensitivity analysis
Several statistical measurements of agreement between obser-
vations and model predictions were performed. The coefcient of
determination (r2), the mean difference (Bias), the modeling ef-
ciency (EF) and the root mean squared error (RMSE) were calculated
to select the models according to their explanatory quality
(Wallach, 2006). The Akaike Information Criterion (AIC) (Sakamoto
et al., 1986) was also applied to compare and select the models
according to their performance and by limiting over-
parameterization. All data were used for model calibration allow-
ing a more robust estimation of parameters. The predictive quality
of models was therefore assessed by calculating the root mean
squared error of prediction (RMSEP) estimated by leave-one-out
cross-validation (Stone, 1974).
The sensitivity analysis of outputs of the novel model predicting
NNM was based on the analysis of variance (ANOVA) decomposi-
tion. For the simulations, a complete factorial design was used with
5 modalities for each soil parameter. Three levels of values were
used for the two-year PCI and 6 frequency values were used for the
observed proportion of a crop type in rotation. For data generation,
we dened lower and upper limits according to those observed in
our database and equidistant values were generated for each
parameter. The generated data were used to perform simulations of
Vp by the models. ANOVA were performed to determine the con-
tributions of explanatory variables and their two-factor in-
teractions to the variability of potential N mineralization rates (Vp)
calculated by the predictive models. ANOVA main effects and
interaction Sensitivity Indices (SI) were calculated by dividing the
sums of squares by the total variability (Monod et al., 2006).
3. Results
3.1. Quantication of in situ net N mineralization
LIXIM calculation model was applied to each of the 65 experi-
ments in order to assess actual (Vm) and potential (Vp) N miner-
alization rates. Fig. 2 shows one example of the evolution of
measured and simulated water and nitrate contents within the soil
prole in Boulancourt site (#8). LIXIM was able to reproduce
correctly the evolution of water (Fig. 2A) and mineral N (Fig. 2B) in
each of the three layers. It simulated a curvilinear net mineraliza-
tion kinetics vs actual time (Fig. 2C) and a quasi linear kinetics vs
normalized time (Fig. 2D). In fact, the amount of mineral N in the
whole prole varied little during autumn, winter and early spring
due to the simultaneous occurrence of N mineralization and nitrate
leaching whereas it increased markedly in late spring and summer
due the dominant N mineralization process.
LIXIM was also able to mimic satisfactorily the evolution of
water and mineral N contents in the 65 eld experiments, as
indicated by the statistical criteria (Table 2). The mean modeling
efciency (EF) and mean index of agreement (d1) for the 65 sim-
ulations were EF 0.58 and d1 0.69 for water content and
EF 0.80 and d1 0.79 for mineral N content. The higher efciency
found for mineral N is attributed to the greater temporal variation
of mineral N compared to water contents. LIXIM provided unbiased
predictions of soil moisture and mineral N contents since the mean
49
difference was 0.3% and 0.1 kg N ha1, respectively. The model
errors (RMSE) were quite comparable to the measurement errors
(standard deviations): 1.5% and 1.3% for water content, 7.1 and
7.0 kg N ha1 for mineral N content, respectively. Finally, a good
agreement was found between measured and simulated variations
of mineral N stocks from the beginning to the end of experiments,
both being related by the following equation: Y 0.96X (r 0.97,
p < 0.001).
The sensitivity analysis performed on the maximum depth
contributing to mineralization (Zm) indicated that the best quality
of t was obtained when Zm was equal to the ploughing depth
which was close to 30 cm for most situations. This suggests that the
ploughed layer is the main contributor to total N mineralization in
the soil prole, justifying the calculation of SON stocks in the 0e30
soil layer in this study. This corresponds to the depth usually
sampled in eld plots for routine soil analysis.
Cumulative NNM varied from 23 to 307 kg N ha1, with a mean
of 140 kg N ha1. The actual NNM rate (Vm) varied from 0.13 to
1.10 kg N ha1 day1 with an average of 0.52 0.20 kg N ha1 day1.
The average normalized time calculated by LIXIM at the end of
experiments was 229 108 ndays and was smaller than the actual
duration (282 93 days), the ratio of normalized to actual time was
0.80 0.27. The cumulative amounts of mineralized N were tted to
a linear or exponential model vs normalized time, as indicated
before. As expected, the exponential model gave a slightly better t
than the linear model with an average model error (RMSE) of 6.3 vs
8.5 kg N ha1. The longer the experiment duration, the better was
the exponential compared to linear model, in accordance with
previous ndings (e.g. Mary et al., 1999). However, we selected the
linear model for its simplicity and for the fact that the two pa-
rameters of the exponential model (No and k) are strongly corre-
lated and cannot be determined each other accurately but only as
their product (Wang et al., 2003). The two models produced
strongly correlated parameters, with the following linear regres-
sion: k.No 1.20 Vp (r 0.90, p < 0.001).
Among the whole dataset of 65 eld experiments, the potential
mineralization rate Vp varied between 0.17 and
1.67 kg N ha1 nday1, with an average of
0.72 0.32 kg N ha1 nday1. The 95% condence interval calcu-
lated with the linear regression ranged between 0.01 and
0.14 kg N ha1 nday1.
3.2. Potential mineralization rate vs soil properties and cropping
history
Pearson correlations and graphical analyses identied that SON
content was the most highly correlated variable (r 0.51 and
r 0.62 for the dataset 65 and the data subset 47, respectively,
p < 0.001) with Vp (Table 3). Vp was also signicantly positively
correlated with SOC content (r 0.48 and r 0.56 for the dataset
65 and the data subset 47, respectively, p < 0.001), as well as the
other fractions of SOM: POM-C and -N, ne SOM-C and -N, EOM-C
and -N and microbial biomass-C (0.48 < r < 0.64, p < 0.001). All
these variables were also highly correlated with SON
(0.76 < r < 0.99, p < 0.001) (Tables S1 and S2).
Weaker correlations were observed between Vp and other soil
parameters: a positive relationship with silt content (r 0.39,
p < 0.01 for the dataset 65) and negative relationships with clay
content (r 0.27, p < 0.05 for the dataset 65), CaCO3 content
(r 0.26, p < 0.05 for the dataset 65) and pH (r 0.36, p < 0.05
for the data subset 47) (Table 3).
Lower but signicant correlations were also found between
potential NNM rates and cropping history variables: i) positive re-
lationships with the frequency of cereals (r 0.33 and 0.41 for the
dataset 65 and the data subset 47, respectively, p < 0.01) and
50 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59

Fig. 2. Example of evolution of measured and simulated water (A) and nitrate (B) contents obtained with LIXIM in each of the three soil layers of a eld experiment (Boulancourt,
site #8) and calculated cumulative amounts of net N mineralized against time (C) and against normalized time (D). Vertical bars are standard errors (n 3).
 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59 51

Table 2
Statistical evaluation criteria for model simulation of soil water and mineral N contents and net N mineralization rates calculated with LIXIM.

Units Min Max Median Mean SD

Experiment duration days 100 555 272 282 93

Water and mineral N simulations
Water RMSE % 0.5 2.9 1.3 1.5 0.5
EF 0.32 0.97 0.58 0.58 0.24
d1 0.37 0.93 0.70 0.69 0.11
Mineral N RMSE kg N ha1 2.2 16.9 6.7 7.1 3.1
EF 0.04 0.99 0.85 0.80 0.16
d1 0.49 0.95 0.80 0.79 0.08
Dstock Mineral N Observed kg N ha1 89 228 82 77 69
Simulated kg N ha1 88 223 76 77 65
Net N mineralization rates
Cumulative net N mineralized kg N ha1 23 307 135 140 59
Vm kg N ha1 day1 0.13 1.10 0.50 0.52 0.20
Normalized time days 49 535 227 229 108
Vp Mean kg N ha1 nday1 0.17 1.67 0.67 0.72 0.32
Vp Condence Interval kg N ha1 nday1 0.01 0.14 0.02 0.04 0.03

RMSE: root mean squared error of the model, EF: modeling efciency, d1: index of agreement, Vm: actual net nitrogen mineralization rate, Vp: potential net nitrogen
mineralization rate.

Table 3
Pearson correlations between potential net N mineralization rates (Vp) and introduced in the soil model (Table 4, step A11). Vp was also highly
explanatory variables for the 65 experiment dataset (dataset 65) and for the data
correlated with SOC content. However, SOC content did not explain
subset of 47 experiments (data subset 47).
further variance of Vp once SON was introduced in the soil model as
Vp dataset 65 Vp data subset 47 an explanatory variable. At the second step (A12), soil clay content
Clay 0.27* 0.27 was found to be the best explanatory variable of Vp when a
Silt 0.39** 0.21 decreasing exponential function was considered. It slightly
Sand 0.14 0.02
improved the performance of the soil model, EF increasing from
CaCO3 0.26* 0.11
pH 0.20 0.36*
0.18 to 0.22. Soil pH was introduced at the third step (A13) using a
SOC 0.48*** 0.56*** gaussian function. This function increasing up to pH 8.5 was the
SON 0.51*** 0.62*** more appropriate for simulating the pH effect. It signicantly
C/N 0.21 0.23 improved the soil model: the model efciency reached 0.43 and the
bias decreased from 0.03 to 0.00 kg N ha1 nday1. This function
Cereals Freq 0.33** 0.41**
Spring crops Freq 0.26* 0.24
Legumes Freq 0.31* 0.45** allows simulating the expected decrease in N mineralization rate in
Sugarbeet Freq 0.23 0.01 very alkaline soils. The C/N ratio of SOM was introduced in the soil
Rapeseed Freq 0.17 0.36* model at step A14 using another gaussian function which peaked at
Others Freq 0.09 0.10 a C/N ratio of 11 and decreased afterwards. With these four
PCI Cereals 0.20 0.18
PCI Spring crops 0.25* 0.19
explanatory variables, the model explained 56% of Vp variance
PCI Legumes 0.16 0.25 without any bias. Soil CaCO3 content was found to be the last soil
PCI Sugarbeet 0.23 0.08 parameter that could still improve the soil model: the efciency
PCI Rapeseed 0.19 0.34* increased to 0.61 with the introduction of a decreasing hyperbolic
PCI Others 0.02 0.12
function. The parameter values that were optimized at step A15
POM-C 0.48***
POM-N 0.52*** were maintained in the soil model and in the following models,
Fine SOM-C 0.57*** except for parameter a which is a proportionality coefcient
Fine SOM-N 0.62*** allowing to avoid model bias at each modeling step. Fig. 3 displays
BiomassMic 0.54*** the pattern of the ve functions constituting the nal soil model
EOM-C 0.60***
EOM-N 0.64***
over the range of physico-chemical characteristics encountered in
the dataset 65. It shows that the amplitude of response of Vp model
Signicant correlations are indicated in bold. (levels of signicance: *p < 0.05,
to each variable is highest for SON, intermediate for clay content,
**p < 0.01 and ***p < 0.001).
Freq: frequency of crop group in rotation, PCI: Preceding Crop Index. pH and C/N ratio, and lowest for CaCO3 content.
SOC: soil organic carbon, SON: soil organic nitrogen, POM: particulate organic The introduction of potentially explanatory variables related to
matter (>50 mm), SOM: soil organic matter, EOM: extractable organic matter, cropping history was then investigated to design a soil-history
BiomassMic: microbial biomass. model. We found that the introduction of an increasing linear
rapeseed frequency (r 0.36, p < 0.05 for the data subset 47) and ii) function of rapeseed frequency during the two preceding years (PCI
negative relationships with legumes frequency (r 0.31, p < 0.05 Rapeseed) and a decreasing linear function of legume frequency in
for the dataset 65 and r 0.45, p < 0.01 for the data subset 47) and the rotation allowed to explain 11% more variance in Vp than the
spring crop frequency (r 0.26, p < 0.05 for the dataset 65). soil model, EF increasing from 0.61 to 0.72 after steps A26 and A27
(Table 4). The soil-history model was dened by these two addi-
tional functions and their parameters determined at step A27.
3.3. Modeling potential N mineralization rate
We tested whether the introduction of additional variables
related to organic matter fractionation and microbial biomass could
In the rst empirical approach (A), a predictive model was
improve the prediction of in situ N mineralization rates. This was
designed by considering successively variable categories ordered
conducted on the data subset 47 in which all these variables had
by increasing acquisition complexity. SON being the most corre-
been measured. Since the whole dataset (n 65) had been
lated variable with Vp, a linear relationship was the rst function
52 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59

Table 4
Prediction functions, model parameters and evolution of statistical evaluation criteria of predictive models during the modeling approaches.

Step Dataset Explanatory Generic model Introduced function Optimized/xed parameter r2 EF AIC Bias RMSE RMSEP
variable values

i n Vi bp V
V b p $f V fi Vi kg N ha1 nday1
i i1 i i

A. Modeling approach by considering successively each variable category

A1. Soil model
A11 65 SON Vb p f SON f1 SON a$SON a 0.26 0.18 160 0.03 0.29 0.29
1 1
0.130
A12 65 Clay bp V
V b p $f Clay f2 Clay expb$Clay1000 a b 0.30 0.22 161 0.03 0.28 0.29
2 1 2
0.158 1.009
A13 65 pH bp V
V b p $f pH f3 pH exp  c$pH  8:52 a b c 0.43 0.43 179 0.00 0.24 0.26
3 2 3
0.279 2.770 0.089
A14 65 C/N bp V
V b p $f C=N f4 C=N 0:8$exp  d$CN  112 0:2 a b c d 0.56 0.56 195 0.00 0.21 0.23
4 3 4
0.330 2.732 0.099 0.055
A1 5 65 CaCO3 bp V
V b p $f CaCO f5 Ca 1=1 e$CaCO3 1000 a b c d e 0.61 0.61 199 0.00 0.20 0.22
5 4 5 3
0.346 2.519 0.112 0.060 1.114
47 bp
V 0.55 0.55 138 0.01 0.21 0.23
5

A2. Soil-history model

A26 65 PCIRa bp V
V b p5 $f PCIRa f6 PCIRa 1 f $PCIRa a f b, c, d, e 0.70 0.70 215 0.00 0.18 0.22
6 6
0.327 0.516 xed
A2 7 65 LegF bp V
V b p $f LegF f7 LegF 1  g$LegF a f g b, c, d, e 0.72 0.72 218 0.00 0.17 0.19
7 6 7
0.341 0.497 0.494 xed
47 bp
V 0.75 0.75 162 0.01 0.15 0.18
7

A3. Soil-history-biological model

A3 8 47 Bio% bp V
V b p $f Bio% f8 Bio 0:8 h$Bio% a h b, c, d, e, f, g 0.77 0.77 164 0.00 0.15 0.17
8 7 8
0.333 14.77 xed

B. Modeling approach by considering simultaneously all variable categories

B1 47 EOM-N Vb p f EOMN f1 EOMN i$EOMN i 0.42 0.30 126 0.05 0.26 0.26
1 1
0.549
B2 47 PCIRa bp V
V b p $f PCIRa f2 PCIRa 1 j$PCIRa i j 0.61 0.55 145 0.04 0.21 0.21
2 1 2
0.495 0.886
B3 47 EOM-C bp V
V b p $f EOMC f3 EOMC 1  k$EOMC i j k 0.60 0.59 147 0.01 0.20 0.21
3 2 3
0.591 0.749 0.011

SON: soil organic nitrogen, PCIRa: Preceding Crop Index Rapeseed, LegF: Legume Frequency, Bio%: microbial biomass % (relative to soil organic carbon), EOM: extractable
organic matter. Final models obtained with the different approaches are indicated in bold.

intentionally used to calibrate the soil and soil-history models in
order to obtain a more robust estimation of parameters, both
models were rst evaluated against the data subset 47. They per-
formed almost as well for the subset as for the complete dataset,
showing a relatively good representativeness of this subset: the
model efciency was 0.55 vs 0.61 for the soil model and 0.75 vs 0.72
for the soil-history model.
Although Vp was signicantly and positively correlated with the
different organic matter fractions (POM and EOM, -C and -N), these
variables did not explain much additional variance of Vp and did
not further decrease the AIC criterion. This result is explained by
the strong correlation between these organic fractions and SON.
The introduction of microbial biomass slightly improved the pre-
vious models. Adding a linear function of the percentage of mi-
crobial biomass relative to SOC raised the explained variance of Vp
to 77% for the data subset 47 in the soil-history-biological model
(Table 4, step A38).
The very small variance explained by the microbial biomass at
nal step might result from the order of introducing variables. This
hypothesis was tested using the approach B in which all potential
explanatory variables were not a priori categorized. Using the data
subset 47, EOM-N was found to be the most correlated variable with
Vp and rst introduced in the B model (step B1, Table 4). Including a
function of PCI Rapeseed at step B2 allowed to explain 19% addi-
tional variance of Vp and increased model efciency from 0.30 to
0.55. Thirdly, a negative linear function of EOM-C was introduced,
increasing slightly the model efciency to 0.59 and decreasing the
bias from 0.04 to 0.01. The predictive model obtained at this third
step (B3) explained 17% less variance of Vp than the soil-history-
biological model obtained with the approach A. We also found
that integrating microbial biomass instead of SON or EOM-N at the
beginning of the modeling process did not allow to obtain a better
predictive model (data not shown).
Comparisons between novel models obtained with the
approach A and MLR modeling approach using the same explana-
tory variables revealed that MLR procedure explained between 10
and 15% less variance of Vp than the models designed with a
multiplicative structure. Similar (i.e. negative or positive) effects of
explanatory variables on Vp were nevertheless found for both types
of models. We conclude that models developed with approach A
perform better than those obtained with MLR or B approach.
3.4. Evaluation of the predictive models
The predicted Vp values are displayed vs observed values for the
three models developed with the approach A in Fig. 4. The close-
ness of t to the 1:1 line conrms the absence of bias for all novel
proposed models. The predictive quality of the models, evaluated
by the method of cross-validation over the whole dataset (n 65),
provided RMSEP estimates of 0.22 and 0.19 kg N ha1 nday1 for the
soil and soil-history models, respectively. The range of Vp values,
both observed and predicted, is as important in the data subset 47
as in the whole dataset, justifying the relevance of this subset to
compare the soil-history-biological model with the other two
models. RMSEP estimate for the soil-history-biological was
0.17 kg N ha1 nday1. It is slightly smaller than the RMSEP
 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
Fig. 3. Representation of linear and non-linear functions introduced in the predictive soil model of Vp with their nal parameter values. Points correspond to calculated values by
each function for the basic soil parameters of the 65 eld-experiments. Function f1 vs SON was normalized between 0 and 1 in order to compare it with the other functions f2 to f5
already normalized.
calculated over the same data subset (n 47) for the soil and soil-
history models, which were 0.23 and 0.18 kg N ha1 nday1
respectively. The RMSEP estimates correspond to a relative model
error comprised between 26 and 30% of the average Vp value.
The ANOVA-based sensitivity analyses of the three models ob-
tained with the approach A were conducted by comparing the
contributions of explanatory factors to the variability of predicted
potential NNM rates. The sensitivity indices (SI) relative to the main
effects and the two factor interactions are represented in Fig. 5.
Small differences were observed between models. The most
inuent factor for the three models was SON which contributed to
0.31e0.36 as main effect SI and 0.10e0.11 as interaction SI. It was
followed by clay, pH and C/N ratio, which accounted for 0.11e0.18 as
main effect and 0.04e0.07 as interaction SI, for each variable. The
other variables had less inuence on model outputs, both for their
main and interactive effects.
4. Discussion
4.1. Reliability of N mineralization estimates and validity of
predictive models
In this study, we chose to use an alternative method to assess in
situ net N mineralization in arable elds by combining a monitoring
of soil water and mineral N contents and a calculation model. LIXIM
model was able to reproduce satisfactorily the evolution of water
and mineral N contents in the soil prole, therefore providing
53
reliable estimates of NNM under eld conditions. Our study was
conducted in the framework of arable cropping systems in
conventional-tillage. For these systems, the actual NNM rates
calculated by LIXIM, varying between 0.13 and 1.10 kg N ha1 day1,
are lower but comparable to those estimated from in situ core
methods in grasslands: 0.20e2.30 kg N ha1 day1 as compiled in
Jarvis et al. (1996) and 0.50e1.50 kg N ha1 day1 measured by
Hatch et al. (2000). The range of our results is very similar to that
obtained in Sweden (0.10e0.93 kg N ha1 day1) by Delin and
Linde
n (2002) who used a N balance approach during a 3-year
experiment within a heterogeneous arable eld.
Field estimates of NNM, which are essential for N management,
can be strongly affected by climatic conditions and particularly by
soil moisture and temperature (Cassman and Munns, 1980). Cor-
rections for these environmental factors have been performed by
LIXIM to produce potential NNM rates. The calculation of these
potential rates is required to disentangle the role of other driving
factors of N mineralization and obtain NNM estimates comparable
to results obtained under controlled conditions. This provides op-
portunities to compare our predictive models to those designed in
laboratory incubation studies and also to test their predicting per-
formance on previously published datasets, which mainly derived
from in vitro experiments.
In term of performance, the proposed soil model is compa-


rable to the prediction function developed by Dessureault-Rompre
et al. (2015, 2016) which include three soil parameters (soil total N,
a labile mineralized N pool and soil pH): their function accounted
54 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
Fig. 4. Observed vs predicted potential net N mineralization rates (Vp) for the three
predictive models designed with the approach A. Black and grey circles correspond to
the whole dataset; grey circles correspond to the data subset 47 alone.
for 67% of the variance in the rate constant of the stable N pool
whereas our soil model could explain 61% of the Vp variance. We
applied the soil model to the data reported by Schomberg et al.
(2009) obtained from a 41 week incubation and found that it was
able to explain 59% of the variance of measured NNM rates. Even
though total N alone could account for the same level of variance,
our model did not deteriorate the prediction compared to this
Fig. 5. Main effect and interaction sensitivity indices (SI) based on the analysis of
variance of the Vp simulations made by the three models designed with the approach
A on randomly generated datasets of explanatory variables.
single factor. The data obtained during a 29 week incubation made
by Springob and Kirchmann (2003) were also used to assess the
ability of our model to predict NNM in sandy soils with a high C/N
ratio (up to 30). The soil model explained 30% (for 23 soils) and 48%
(when excluding one outlier) of the variance of NNM rates
measured in this incubation study. Therefore, our model produced
consistent predictions of NNM rates measured in varied soils and
laboratory conditions. Further studies would be needed to obtain
extended datasets of eld experiments to perform an independent
validation of the proposed predictive models. However, this type of
study is costly and time-consuming, explaining why so few refer-
ences are available under in situ conditions.
In the following of this discussion, the effects of the different
factors that could inuence N mineralization are discussed in the
light of results obtained in this work.
4.2. Basic soil parameters inuencing in situ N mineralization
Results obtained showed that the most inuencing factor of in
situ NNM rates was the SON stock. The strong correlation observed
between both variables is consistent with the majority of soil
 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
incubation studies made in various ecosystems demonstrating that
SON is a good predictor of NNM (e.g. Dessureault-Rompre
et al.,
2015; McDonald et al., 2014; Schomberg et al., 2009) and even
gross N mineralization (Booth et al., 2005). The sensitivity analyses
of factors inuencing model outputs highlight the need for an ac-
curate characterization of soil parameters, and particularly SON
stocks. Therefore, a particular attention must be paid to the
assessment of soil bulk density and the choice of depth (Z) used to
calculate SON stocks. In this study, the sensitivity analysis per-
formed with LIXIM on Zm revealed that the ploughing depth
appeared to be the most appropriate value of Z. This conclusion
should be recommended to regularly ploughed soils. Results ob-
tained in reduced tillage systems suggest that N mineralization
decreases with depth but remains signicant down to the old
ploughing depth (e.g. Oorts et al., 2007). Therefore, in these systems
Z should be greater than the current tillage depth and optimally
equal to the past maximum tillage depth.
Among important soil parameters, clay concentration has been
identied as driving factor of SOM decay rates (Adu and Oades,
1978; Hassink et al., 1993; Kleber et al., 2007) and NNM rates
(Colman and Schimel, 2013; Delin and Linde
n, 2002). Simulation
models of SOM turnover such as CENTURY (Parton et al., 1987;
Parton, 1996), DAISY (Hansen et al., 1991), ROTHC (Coleman and
Jenkinson, 1996) or STICS (Brisson et al., 2003) include equations
reecting a negative effect of clay content (or clay silt content) on
these rates. The clay function introduced in the soil model is similar
to that used in a previous study simulating the consequences of
straw residues export on SOC stocks, relating carbon mineralization
rate and clay content (Safh-Hdadi and Mary, 2008). The optimized
parameter at the end of our modeling process (b 2.52) is close to
that obtained in the latter study (between 2.00 and 2.68, depending
on the stable pool size).
To a lesser extent than clay, negative effects of CaCO3 content
have been evidenced on potential NNM rates. The decreasing
relationship could be explained by the protective effects of ne
CaCO3 on SOM mineralization (Delphin et al., 1986), CaCO3 acting as
a stabilizing agent (Duchaufour, 1976).
The proposed soil model predicts that soil pH inuences N
mineralization rates. It simulates that NNM rates increased with pH
over the range of the present study (5.7e8.4) but the gaussian
function chosen allows to simulate a decrease in N mineralization
at very high pH, shown in some studies such as Pathak and Rao
(1998). Surprisingly, there was no signicant simple correlation
between NNM and pH in our study because pH inuence is prob-
ably masked by the effects of other correlated factors. This apparent
contradiction may explain why controversial results have been
reported in the literature about the specic role of soil pH on NNM.
Curtin et al. (1998) did not observe signicant relationship between
soil pH and N mineralization in a 24 week incubation study per-
formed on 61 soils from Canada. However, after manipulating soil
pH by adding Ca(OH)2 in two soils, they found that raising the pH
from 5.7 to 7.4 linearly increased C and N mineralization measured
during a 100-day incubation. Bertrand et al. (2007) found apparent
but not true effects of pH on C and N mineralization in an acidic soil
which had been limed 20 years earlier whereas Andersson and
Nilsson (2001) observed a stimulation of C mineralization with
liming. Raising up soil pH with liming could increase both the
amount of negatively-charged groups on the humus colloids and
the SOM solubility (Andersson et al., 2000). Kemmitt et al. (2006)
analyzed two long-term eld experiments in which pH had been
manipulated. They concluded that changes in soil pH signicantly
affected soil microbial activity and the rate of soil C and N cycling.
Aciego Pietri and Brookes (2008) also found that pH can markedly
inuence soil microbial biomass and activities. Cookson et al.
(2007) compared ve acidic soils varying in land use and found
55
that pH was the main factor positively correlated with gross N
mineralization rates.
The C/N ratio of SOM was the fourth inuent driving factor in
the soil model. A gaussian function with a maximum value at C/
N 11 was found to be relevant to describe its effect on N miner-
alization rates. We hypothesize that the predicted decrease in NNM
rate when the C/N ratio decreases from 11 to 7 could be attributed
to a shift in SOM quality towards more highly processed SOM
such as that present in subsoil (Jenkinson et al., 2008; Rumpel and
Kogel-Knabner, 2010) with lower mineralization rates. Conversely,
in soils with high C/N ratio (greater than 11), N availability could
become a limiting factor for SOM decomposers and NNM rates
could decrease due to higher microbial N immobilization. This
result is consistent with a previous work which showed a negative
exponential relationship between NNM and the C/N ratio of soils
whose C/N ratios varied between 10 and 30 (Springob and
Kirchmann, 2003).
4.3. Contribution of additional factors to improve N mineralization
prediction
Previous studies demonstrated the inuence of crop rotation on
N mineralization (Carpenter-Boggs et al., 2000; Senwo and
Tabatabai, 2005; Shari et al., 2008). Integrating the inuence of
agricultural practices into models in combination with climatic and
soil predictors could help to better predict N supply for agro-
ecosystems (St. Luce et al., 2011). In our study, cropping history
variables allowed to explain additional Vp variance. The positive
correlation observed between Vp and the frequency of cereals in
the rotation could result from the larger amounts of crop residues
(straw) returned to soils on the long term in these rotations. Indeed,
Powlson et al. (1987) showed that the incorporation of straw exerts
long-term effects on SOM and microbial biomass, increasing the
quantity of mineralizable N in soils. Surprisingly, the frequency of
cereals did not improve our predictive model when basic soil pa-
rameters were already introduced. This could result from correla-
tions between explanatory variables since crop types and rotations
are more or less specic to pedo-climatic conditions. Integrating
soil parameters at rst in our modeling approach could have helped
to avoid at least partly these confounding effects.
The proposed soil-history model identied a positive effect of
rapeseed frequency on N mineralization. This short term effect,
which concerned the last two years before measurements, might be
related to the large amounts of leaves produced by rapeseed and
falling during its growth period (Justes et al., 2000). These leaves
decompose rapidly at soil surface and could enhance soil N
mineralization after rapeseed harvest. Conversely, the model
pointed out a slight negative effect of legume frequency on Vp.
Plaza-Bonilla et al. (2016) showed that cropping grain legumes in
rotations can lead within a few years to signicant losses of SOC
and SON. They showed that increased legume frequency reduced
carbon inputs to soil. These smaller inputs could result in a further
depletion of the soil mineralizable N pool on the long-term and a
reduction of the specic N mineralization rate (i.e. per unit of SON).
Organic matter fractions and microbial biomass did not appear
to greatly improve the prediction of Vp when parameters such as
SON were previously introduced in the model. A similar conclusion
was suggested by Ros et al. (2011) who showed that extractable
organic N, although well correlated with mineralizable N, did not
explain additional variance compared to total N. The extraction
conditions can strongly inuence the amount and characteristics of
the analyzed organic nitrogen pools. In our study, the high tem-
perature pretreatment used for EOM analysis could have extracted
readily decomposable fractions but also solubilized recalcitrant
compounds (Ros et al., 2009), so that EOM fractions could reect
56 H. Clivot et al. / Soil Biology & Biochemistry 111 (2017) 44e59
the quantity of SOM rather than a specic bioavailable fraction (Ros,
2012).
The small explanatory power of microbial biomass on Vp vari-
ation observed in our study might seem paradoxical. However it is
consistent with the conclusion of Kemmitt et al. (2008) who
demonstrated that the mineralization of humied organic matter
was not inuenced by the size, activity or composition of the mi-
crobial biomass. These authors suggested that SOM mineralization
was primarily governed by abiotic processes controlling its acces-
sibility to microorganisms and introduced the Regulatory Gate
hypothesis. Our results could support this hypothesis, even though
the importance of biotic regulation of SOM mineralization is still
debated (Kuzyakov et al., 2009; Paterson, 2009). The results of Birge
et al. (2015) also suggest that the amount of available SOM is the
limiting factor of SOM mineralization rather than the size of
enzyme pool or microbial biomass. Investigating the active portion
of soil microorganisms instead of total microbial biomass could be a
best way forward to link microbial parameters and soil functioning
(Blagodatskaya and Kuzyakov, 2013). Fujita et al. (2014) also
showed that an improved prediction of N mineralization can be
obtained by combining microbial biomass measurements and C/N
stoichiometry effects in a mechanistic and more complex model
than that developed here.
4.4. Relevance of the modeling approach
Microbial biomass and organic matter fractions were shown to
be well correlated with NNM rates. However, they did not add to
the prediction of Vp when more simple parameters associated with
SOM (e.g. SON), which are less costly and time-consuming to
determine, were integrated rst in the predictive model.
Comparing the two multiplicative approaches (A and B) empha-
sized the importance of the order of introducing variables on the
selected variables and the model performance. In model B, SON was
replaced by EOM-N (both highly correlated, r 0.92) as the main
factor, but the predictive quality of model B remained smaller than
that of model A. We cannot exclude that the lower number of
samples in the data subset 47 could have inuenced the results,
even though this subset was representative of the whole dataset.
The predictive models designed with a multiplicative structure
were shown to provide better explanation of NNM rates than ad-
ditive linear models with the same explanatory variables. This
conrms our assumption that a model with a multiplicative
structure reects the nature of the interactive effects of factors
inuencing N mineralization better than additive models. The non-
linear functions considered in the multiplicative models also
contributed to improve NNM rates prediction, supporting the hy-
pothesis that many soil processes are better represented by non-
linear models (Archontoulis and Miguez, 2015). Our attempt was
not to design a process-based model, but to identify the main
driving factors of N mineralization and determine their response
functions.
In a functional interpretation of the soil-history-biological
model obtained here, N mineralization rate is the result of SOM
decomposition process under the inuence of: i) the amount of
substrate (SON) and its quality (C/N), ii) edaphic factors that affect
SOM physico-chemical protection (clay, CaCO3) or the activity of
microorganisms (pH), iii) the specic effect of some crop residues
returned to soil (rapeseed) and iv) soil microorganisms which are
the major actors of SOM decomposition.
5. Conclusions
This study showed that the calculation model LIXIM was able to
satisfactorily represent changes through time of water and mineral
N contents in bare soils from 65 eld-experiments representative of
French arable situations. This calculation model provided reliable
estimates of in situ NNM rates under actual eld conditions in
arable conventional-till cropping systems. The models predicting in
situ NNM rates proposed in this paper revealed that basic soil
characteristics can explain 61% of the variance in potential NNM
rates. The subsequent introduction of two variables relative to crop
type frequency (i.e. rapeseed and legume) helped to improve the
explanatory and predictive qualities of the soil model, explaining
72% of the variance in Vp. Integrating variables more complex to
acquire such as organic matter fractions and microbial biomass
hardly improved the model performance, when soil parameters
such as SON had been previously introduced. Furthermore, these
variables did not allow to obtain a better prediction when they
were introduced rst in the model. The soil-history model (A2)
provided the best compromise between efciency and complexity.
Each of the three proposed models (A1eA3) was developed with
variables that are routinely measured or easily accessible with,
maybe, the exception of soil microbial biomass. These operational
models could then be implemented in multidisciplinary models in
order to improve their capacity to simulate N dynamics in soils and
help N fertilization management.
Acknowledgements
We wish to acknowledge the technical staff of ARVALIS as well
as Francis Barois, Eric Bazerthe, Didier Chesneau, Thierry Morvan,
Pierre Mortreux and Jean-Marie Nolot for their contribution to eld
experiments. We thank Patrick Petibon for soil analysis. This
research was supported by ARVALIS, CETIOM (Terres Inovia) and
INRA. This work was performed, in partnership with the SAS PIV-
ERT, within the frame of the French Institute for the Energy Tran-
sition PIVERT (www.institut-pivert.com). This work was supported,
as part of the Investments for the Future, by the French Govern-
ment under the reference ANR-001-01, and was funded within the
frame of the Genesys WP1 P13 Solebiom project. We also thank the
anonymous reviewers for their constructive evaluation of the
manuscript.
Appendix A. Supplementary data
Supplementary data related to this article can be found at http://
dx.doi.org/10.1016/j.soilbio.2017.03.010.
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