N2O emissions of low input cropping systems as affected by legume and cover crops use

Agriculture, Ecosystems and Environment 224 (2016) 145–156

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N2O emissions of low input cropping systems as affected by legume and cover crops use Céline Peyrarda,* , Bruno Marya , Pierre Perrinb , Grégory Véricelb , Eric Gréhana , Eric Justesb , Joël Léonarda a b

INRA UR 1158 AgroImpact, Site de Laon, F-02000 Barenton-Bugny, France INRA UMR 1248 INRA-INPT AGIR, F-31326 Castanet-Tolosan cedex, France

A R T I C L E I N F O

Article history: Received 30 September 2015 Received in revised form 4 February 2016 Accepted 16 March 2016 Available online xxx Keywords: N2O Legumes Cover crops Soil tillage Residue incorporation Low input cropping systems

A B S T R A C T

Reducing environmental impacts of agriculture is a key issue for preserving water, soil and air quality. Among available options, the incorporation of legumes allows to reduce synthetic N fertilizer use, the use of cover crops is an efficient way to decrease nitrate leaching and recycle nutrients, while mechanical weeding together with crop rotation help to limit the use of pesticides. However, how these options affect N2O emissions remains uncertain. Here we studied N2O emissions of four cropping systems which were designed as low input alternatives to the conventional wheat-sunflower rotation in south-west France and make use of the aforementioned options. The used cropping systems differ by synthetic N fertilizer input: 96 kg N ha
1 year
1 for the Low Input (LI) cropping system and 33 kg N ha
1 year
1 for the Very Low Input (VLI) cropping system which incorporates a grain legume in the rotation. For each of the two systems (LI and VLI), both a variationwith cover crop (+CC) and without cover crop (
CC) were studied. Daily N2O fluxes were measured almost continuously (at least 87% of the 3-year rotation duration) using automatic chambers. Measurements of soil water content, soil temperature, mineral nitrogen (N) content were also carried out. Cumulative N2O emissions over the whole 3-year rotation were in the low range of literature values for all systems but they were significantly higher for the VLI cropping system (1.12 kg N2O-N ha
1 year
1) than for the LI cropping system (0.78 kg N2O-N ha
1 year
1) on average over +CC and
CC. Patterns of emissions were also different between the two systems, with emissions taking place in the form of short-lived peaks only after N fertilization for LI, while peaks occurred more frequently over the whole rotation for VLI. No difference between the +CC and
CC cropping systems could be detected at the scale of the rotation (P = 0.47). Although N2O fluxes increased significantly for a few days after cover crop destruction (P = 0.002), the contribution of such events to cumulative N2O emissions remained negligible (<10 g N2O-N ha
1). The effect of tillage events, especially when they were not associated with crop residues return to soil, was also found to be small. As expected, both temperature and soil water content had a strong influence on N2O emissions, although the underlying relationships often only appear clearly during specific periods, e.g. during summer for the soil moisture effect. Because agronomical practices such as increased use of legume crops and use of cover crops only have a limited effect on N2O emissions, their adoption can be considered on the basis of the benefits they have to address other important agronomic or environmental issues. ã 2016 Elsevier B.V. All rights reserved.

1. Introduction Reducing external inputs is a key issue for designing alternative sustainable cropping systems, with tightened nutrient cycles and expected lower environmental impacts (Edwards, 1987; Poudel

* Corresponding author at: INRA, UR 1158 AgroImpact, Pôle du Griffon, 180 rue Pierre-Gilles de Gennes, 02000 Barenton-Bugny, France. E-mail address: [email protected] (C. Peyrard). http://dx.doi.org/10.1016/j.agee.2016.03.028 0167-8809/ ã 2016 Elsevier B.V. All rights reserved.

et al., 2002). Such alternative systems make large use of three main options: 1) the use of legumes to reduce external N input (Peoples et al., 1995; Tedla et al., 1992); 2) the introduction of cover crops, both as nitrate catch crops to limit N leaching (Constantin et al., 2010; Gabriel and Quemada, 2011; Tonitto et al., 2006) and to produce a N green manure for the succeeding main cash crop (Thorup-Kristensen et al., 2003; Tribouillois et al., 2015) and 3) the use of mechanical weeding to minimize the application of herbicides (Chikowo et al., 2009). Many studies in the literature discuss the efficiency of those alternative systems on the main

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targeted objectives: maintenance of crop yields and grain quality, reduction of nitrate leaching, limitation of pesticides use and their transfer to the environment. However, less is known on how these alternative systems influence the greenhouse gases (GHG) balance, and especially nitrous oxide (N2O) emissions. Nitrous oxide represents the largest contribution to global warming from agriculture (IPCC, 2007). N2O is produced in soils mainly by two coupled microbial processes: i) nitrification in aerobic conditions and ii) denitrification in anaerobic conditions. Both the occurrence and intensity of those processes are strongly affected by soil mineral-N and soluble Carbon (C) availability, water and oxygen contents, temperature, pH and soil texture (Conen et al., 2000; Gu et al., 2013; Smith et al., 1998; Wijler and Delwiche, 1954). As changes in agricultural practices directly influence substrates availability and environmental conditions in the soil, they are expected to have a significant impact on N2O emissions. The effect on N2O emissions of substituting N fixed through biological N2 fixation (BNF) for mineral N fertilization has been matter of strong debate. A review of the literature by Rochette and Janzen (2005) indicated that although legumes may actually conduct to increased N2O emissions, much of this increase may be attributable to the decomposition of crop residues after harvest, rather than from BNF itself. This controversy has led to a revision of the IPCC rules for estimating N2O emissions, and the removal of the initially included specific emission factor for legume crops. The low contribution to N2O emissions of N fixed through BNF has since been confirmed by more recent work (Carter and Ambus, 2006; Zhong et al., 2009), especially on grasslands, where the crop residue contribution is absent (Ingram et al., 2015; Schmeer et al., 2014). The global effect on N2O emissions of introducing legumes in the crop rotation thus seems to be mostly neutral, although it can vary in relation to the nature of crop residues and how they are managed. Cover crops are most often used as catch crops to mitigate nitrate leaching during the autumn and winter fallow periods (Thorup-Kristensen et al., 2003). When legume cover crops are used, either alone or in mixture, they provide an additional N green manure effect for the subsequent crop (Tribouillois et al., 2015). They modify the mineral N availability in the soil, either reducing it during plant growth or increasing it after incorporation into the soil. They can also affect soil water content through increased transpiration compared to bare soil. Existing studies generally show little effect of cover crops (either legume or non-legume) on N2O emissions (Liebig et al., 2010; Sanz-Cobena et al., 2014), especially when results are integrated at year scale (Basche et al., 2014). An influence of cover crops on N2O emission has been observed over more specific periods, in which case their net effect is mainly dependent on the crop C:N ratio (Frimpong and Baggs, 2010), on climate and on how they are managed after destruction. Basche et al. (2014) have for example shown in a meta-analysis that the incorporation of cover crop residues into the soil often results in a short term increase in N2O emissions, especially for legume cover crops. Higher precipitations seem also to favour a deleterious effect of cover crops on N2O emissions. Switching from herbicide based weed management to mechanical weeding implies a significant increase in superficial tillage frequency. Soil tillage strongly influences soil structure and soil water dynamics, redistributes soil nutrients and organic residues, all of which can affect N2O production as well as N2O transfer toward the soil surface (Gregorich et al., 2006). The effect of soil tillage on N2O emissions, especially its reduction or suppression, has been extensively studied. There is a general tendency to observe higher emissions in the absence of tillage than with conventional tillage, especially in the years following conversion, although the effect dampens with time (Plaza-Bonilla et al., 2014; Six et al., 2004; van Kessel et al., 2013). However the

effect of the change in tillage frequency associated to mechanical weeding on N2O fluxes is much less studied. A recent study by Vermue et al. (2013) compared a conventional system to an integrated weed management system with respect to N2O emissions. Emissions were found to be higher in the integrated weed management system, but reasons for the observed difference were difficult to establish. The difference between the two systems was attributed to the presence of a lentil undercover in the integrated weed management system, rather than to differences in tillage. Beyond the individual effect of each management option, the key role played by interactions between practices makes even more uncertain the prediction of the performances of a specific cropping system with regard to N2O emissions. In this work, we focused on the N2O emissions of low input cropping systems that were designed as three-year crop rotation alternatives to the traditional two-year durum wheat-sunflower rotation in southwest France and which make use of the options previously mentioned. Those alternative low input systems have been designed mainly to reduce the dependency on fertilizer-N and pesticide inputs, while keeping good production levels and without drastically modifying the existing agro-food local supply chain. Traditional cash crops such as durum wheat and sunflower were thus conserved. Continuous monitoring of N2O emissions was done during three years with the objective of i) quantifying and comparing N2O emissions of these low input cropping systems at the whole rotation scale and ii) better understanding how the introduction of more legumes and of cover crops, together with environmental conditions, influence N2O emissions. 2. Materials and methods 2.1. Site, field trial and cropping systems description The study site is located at the INRA experimental station of Auzeville, south-west France (43.527 N, 1.506 W), and has a submediterranean climate. Mean annual precipitation and temperature of the last three decades are 685 mm and 13.7  C, respectively. The period of study (December 2010 to July 2013) covered two rather dry years (2011 and 2012, with 538 and 548 mm, respectively) and one wet year (2013, 836 mm). The seasonal distribution of precipitations varied notably between years: in 2011 the heaviest rainfall events occurred during winter and summer, whereas in 2012 they were observed during spring and fall. The soil is a deep calcareous-clay (120 cm). Clay content of the 0–30 cm layer varies between 18.6% and 33.4% and pH between 6.2 and 8.3. Total carbon content is low, ranging from 0.7% to 1.07%. The MicMac field trial was set up in 2010 to study innovative low input cropping systems designed as alternatives to the traditional durum wheat-sunflower rotation under rainfed conditions in south-west France. It compares three main cropping systems with a grade in N fertilizer and pesticide use, combined with the use or absence of cover crops (CC) during fallow. Three repetitions of the main cropping systems were randomly distributed on three blocks, and each of the resulting 9 plots (200 m  30 m) was partitioned into two subplots to which the two cover crop variations (with or without CC) were randomly attributed. The three main crops of each rotation were grown simultaneously every year (one of the crops for each of the 3 repetitions) to take into account the high inter-annual climate variability. In this study, we focused on the N2O emissions of two of the main cropping systems compared and their two cover crop variations. The first cropping system studied (Low Input, LI) was initially designed with two main objectives in mind: reducing nitrate leaching as well as lowering pesticide use. The three years rotation conducted under integrated pest management is the

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VLI. For that reason we consider that we studied well installed cropping systems, established for at least 7 years. 2.2. Soil measurements

Fig. 1. Crop rotations used on the two main cropping system modalities: a) LI (Low Input) and b) VLI (Very Low Input). Cover crops present on the +CC modalities are indicated in italics. Colors used for the LI and VLI cropping systems will be maintained in all figures to represent both modalities.

following (Fig. 1a): durum wheat – mixture of vetch and phacelia – sorghum – regrowth of sorghum – sunflower – undersown egyptian clover. Cover crops are used in the LI + CC modality and include legumes to allow N input from BNF. They are absent from the LI-CC modality. The second cropping system studied (Very Low Input, VLI) puts additional emphasis on reducing synthetic fertilizer-N input. The rotation was adapted to include a legume as main cash crop, and is as follows (Fig. 1b): durum wheat – mixture of vetch and oat – sunflower – oat – winter faba bean – mixture of vetch and mustard, with cover crops present on the VLI + CC modality and absent on the VLI-CC modality. Durum wheat was fertilized two times in spring (before and during rapid growth of the crop), with ammonium nitrate in both systems and an average total N input of 160 kg N ha
1 for LI (+CC and
CC), 135 kg N ha
1 for VLI-CC and 90 kg N ha
1 for VLI + CC. For comparison, usual N input for wheat in the region is 205 kg N ha
1. Sorghum and sunflower were both N fertilized in the LI cropping system (40 and 50 kg N ha
1 respectively) whereas the sunflower and the faba bean in VLI were not fertilized. In all cropping systems studied tillage took place at 3 different periods: i) shallow tillage before sowing plus mechanical weeding in early spring when necessary, ii) stubble incorporation after harvest of main crops, iii) ploughing approximately one month after destruction of the cover crop in late October or early November on +CC or shallow tillage to maintain the bare soil during the same period on
CC. The timing of some of the main events is visible together with N2O fluxes in Fig. 3 at the beginning of the results section. Although the experiment was established in 2010, the studied cropping systems only slightly differ from the cropping systems which were in place since 2003 on the site. The main difference is that a winter faba bean replaced the winter pea crop after 2010 on

Water content, temperature, bulk density and mineral N content in soil are key control variables of N2O emissions. Measurement of these variables was thus undertaken to help explaining the measured fluxes and differences between the studied cropping systems. Soil water content was monitored using water content reflectometers (Campbell Scientific CS616 probes) inserted horizontally at 0.10 m and 0.20 m depth into the soil (2 replicates per plot). Thermistance probes (Campbell Scientific T107 probes, 2 replicates per plot) were inserted similarly to monitor soil temperature at the same depths. Both measurements were done at a 30 min sampling interval. A temperature correction was applied to soil water content measurements using the method of Rüdiger et al. (2010) before calibration using gravimetric water contents and bulk density measurements. The knowledge of bulk density allowed calculating soil porosity, which was in turn necessary to calculate the Water Filled Pore Space (WFPS). Soil samples were collected roughly every month to determine gravimetric water content and mineral N content. NH4+ and NO3
in two layers (0– 0.15 and 0.15–0.30 m) were extracted with 1 M (Maynard et al., 2007). The extract was filtered and analysed for NH4+ and NO3
using a Skalar 5100 continuous flow autoanalyzer (Skalar Analytic, Erkelenz, Germany). 2.3. N2O fluxes measurement N2O flux was determined 4 times per day using automatic chambers as described by Bessou et al. (2010). The main advantage of such quasi continuous measurements is that there is less gapfilling needed. This ensures a good estimate of cumulative N2O emissions, while interpolation of distant manual measurements strongly increases the uncertainty, especially at low sampling frequency (Crill et al., 2000). Other advantages include the possible capture of often short term changes in the dynamics of emissions (Smith and Dobbie, 2001), stronger confidence on the observed variations, and alleviation of experimental work. This last point is especially important as it allows integrating fluxes over multiple years and whole crop rotations, which is seldom done, although necessary according to Groffman et al. (2000) to observe coherent patterns in annual N2O flux at the ecosystem scale and to establish predictive relationships with environmental parameters.

Fig. 2. Timeline of N2O measurements for each main cropping system, cover crop modality and plot. Main crops periods are represented by a white rectangle with indication of the crop. Fallow periods are indicated by dotted rectangles.

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Fig. 3. Daily rainfall (a), daily N2O emissions in the LI + CC and LI-CC cropping system modalities (red lines) on plot F and A (b), (c) and daily N2O emissions in the VLI + CC and VLI-CC cropping system modalities (green lines) on plot D, I and B (d), (e). Horizontal arrows delimitate the different crop and fallow periods. Fertilization (F), crop residue crushing (C) and residue incorporation (I) are indicated by vertical dotted lines. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

We simultaneously used a total of 18 closed dynamic chambers, distributed into 3 sets of 6 chambers. Each set is connected to two infra-red gas analyzers, one for CO2 (LI-COR Biosciences, Li720) and the other for N2O (Thermo Instruments, 46C). A pump and valves system controlled by a datalogger (Campbell Scientific CR1000) allows to successively close each of the 6 chambers during 18 min and to measure CO2 and N2O concentration every 10 s. The measurement of ambient air concentration immediately before and after the 6 chambers cycle allows us to detect any drift in concentration measurements. The accuracy in the measured gas concentration was assessed by computing the standard deviation obtained with the measurement of air outside the chambers or the RMSE (residual mean square error) obtained when fitting the kinetics inside the chambers: both values yielded similar results. The RMSE varied between 2 and 10 ppb N2O, depending on the analyzer. CO2 measurements were used both to detect any problem (e.g. leaks) and to correct the N2O concentration for possible interferences with CO2 concentration. The correction was usually small but eliminated most of the negative fluxes. Chambers were closed every 6 h, which is a good compromise between frequent measurements and minimizing the closing time and thus disturbance of environmental conditions. Daily flux for each chamber was obtained from averaging the 4 measured fluxes a day. Of the 3 sets of 6 chambers, two have dimensions of 0.70  0.40 m, and one of 0.70  0.23 m, the last one being especially adapted to

cereal crops for being used between rows after removing of one row. The height of the chambers was 0.25 m and they were inserted 0.08–0.10 m into the soil, resulting in a headspace height of 0.15– 0.17 m which was systematically measured in order to know the chamber air volume. Both chambers and sensors inserted into the soil were removed periodically, before tillage operations. N2O flux (expressed in g N2O-N ha
1 day
1) was calculated from the slope of concentration vs. time at t0 (ppb min
1):   h  Mm dC F ti ¼ 0:144 dt t¼t0 VM where h (cm) is the headspace height, Mm the molar weight of N in N2O (Mm = 28 g mol
1), VM the molar volume (24.1 L mol
1 at 20  C). The 0.144 coefficient allows the conversion of m
2 min
1 to ha
1 day
1. The slope of concentration vs. time at t0 was estimated using an exponential model (derived from the Fick’s law of diffusion) fitted to the kinetics of gas accumulation when that kinetics was non-linear. A linear model was preferred if either the kinetics of accumulation was very close to linearity (rate constant of the exponential model <0.01 min
1) or the quality of fit of the exponential model was not much better than that of the linear model (RMSEexp/RMSElin > 0.975). In both cases concentration data from the whole 18 min period of accumulation were used. When applying the quality criteria proposed by Rochette and Eriksen-Hamel (2008) for an accurate use of the chamber

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methodology, our setup obtained “very good” scores for all criteria. Only for the smaller chambers and the area/perimeter ratio (A/R) the criteria was estimated to “good”, but with a value of A/R = 9 cm very close to the limit from the “very good” class (A/R = 10 cm). N2O fluxes were monitored from December 2010 to July 2013, which corresponds to a whole rotation (Fig. 2). Because of the constraints imposed by the limited length of the electrical cables (30 m), chambers replicates for a given treatment always had to be installed inside a same plot. Such a design can raise pseudo replication issues that were discussed in Bessou et al. (2010). This is why chambers were not maintained on the same plots over the whole rotation period, different repetitions of a given rotation being followed during successive periods of time (Casler et al., 2015). 2.4. Data analysis Cumulative N2O emissions at the rotation scale (3 years) were calculated for all cropping system modalities through the sum of cumulative emissions (mean of the 3 chambers) of each rotation component: main crop cycle, or fallow period with either cover crop or bare soil. All components of each rotation were measured at least one time on one plot. When several values were available for a given rotation component (another plot-year for example), the average was used which allowed to integrate some spatial and temporal variability and to make the estimate less dependent on inter-annual climate variability or specific properties of a plot. Available data allowed to cover at least 87% of the whole rotation time whatever the cropping system modality. Significant periods without measurements mostly corresponded to short laps of time where chambers were removed for sowing, tillage or harvest and were not immediately put again in place because the time lag before the next operation was too limited to be worth the effort. 2.4.1. Main cropping system effect: LI vs. VLI Mean cumulative emissions obtained for each cropping system at the whole rotation scale allow useful comparisons but do not give information about the significance of the observed differences from a statistical point of view. To go further we defined peer groups inside which the influence of differences in duration of measurement, climatic conditions, fallow period management or crop nature are minimized to allow a more powerful test of the LI vs. VLI effect. Cumulative N2O fluxes of all chambers were then analysed using a multifactor analysis of variance, with the cropping system (LI or VLI) as the main factor and the peer group as a fixed effect. This allows to make a paired comparison analysis of the main effect (LI vs. VLI) with the additional advantage that chambers replicates can be used rather than mean values. The fact that a total of 4 different pairs of plots (Fig. 2: F-D, F-I, A-D, A-B) were involved in comparisons inside peer groups allowed to take advantage of the true replicates existing in the experimental design to draw conclusions about the treatment effect despite the non-interspersion of chambers replicates. Because external N inputs differ between the two main treatments, we were also interested in the relationship between those N inputs and the N2O emissions. Simple regression was used to analyse the relationship between mineral N input at the crop cycle scale and the corresponding cumulative N2O emissions. 2.4.2. Effect of cover crops The frequent simultaneous measurement of N2O flux on the two cover crop modalities of each plot (+CC,
CC), allows a powerful analysis of the cover crop effect on N2O emissions. Peer groups were defined which contain cumulative emissions data sharing the same time sequence, plot and cropping system (LI or VLI) and differ

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by the presence or absence of cover crops. A multifactor analysis of variance with +CC vs.
CC as the main effect and peer group as a fixed effect was then carried out. The systematic presence of cover crops and the use of mechanical weeding resulted in frequent soil tillage operations associated with or without residue incorporation. This allowed the analysis of the short term effect of tillage and residue return to soil, and their interaction, on N2O emissions. At each tillage or crop destruction operation we defined two paired periods, before and after occurrence. We both tested a fixed duration method (10 days) and a flexible duration method (6 to 17 days). The second method allowed to correct for variations in rainfall amount and to manage situations where two tillage operations occurred within a short period of time. Cumulative N2O emissions were calculated for each period and each chamber, as well as the difference in N2O emissions between each pair of periods (DN2O). We used a multifactor analysis of variance to test the effect of four main classes of tillage and residue return combination on DN2O: i) shallow tillage without residue input (TR0; weeding, soil preparation for sowing); ii) shallow tillage associated with mature residue return (TR-; stubble incorporation by disk ploughing); iii) deep tillage combined with fresh residue incorporation (TR+; incorporation of cover crop residues by inversion ploughing); iv) mechanical destruction of the cover crop without incorporation (NTR+). 2.4.3. Effect of environmental conditions and substrates availability Environmental conditions (soil temperature, soil water content) and substrates availability (NH4+, NO3
) are important drivers of N2O emissions. We used a decision tree approach (Therneau et al., 2014) to get insight into the dominant factors and identify thresholds beyond which strong changes in N2O emission behaviour occur. Adequate selection of data subsets was also used to eliminate additional sources of variability and better underline relationship between control variables and N2O fluxes. For example, separating results depending on the season was used to analyse the complex relationship between soil water content and N2O emissions. 3. Results 3.1. Variations in N2O emissions The dynamics of daily N2O emissions is shown for the whole rotation duration (3 years) in Fig. 3. The two main cropping systems (LI and VLI) are distinguished as well as the presence or absence of cover crops in each case. It can be observed that whereas N2O fluxes mainly occur in the form of short lived peaks after fertilization events in the LI system, with emission levels decreasing back to almost zero after that, emissions are much more regular on the VLI system, with few peaks and fluxes remaining close to 5 g N2O-N ha
1 day
1 most of the time. A total of 29 time sequences were identified (17 corresponding to a main crop, 12 to a fallow) for which cumulative N2O emissions were calculated. The coefficient of variation of cumulative N2O emissions in these sequences, calculated from the chamber replicates, ranged from 7 to 113%. Only 4 values out of 29 were higher than 50% and they were all found in VLI cropping system modalities. When measurements were available for the same component of a rotation on different years, very high variation could be observed. This is especially noticeable for durum wheat, the cumulative emissions of which ranged from 284 to 1438 g N2O-N ha
1 for VLI and from 311 to 1195 g N2O-N ha
1 for LI, depending on the year considered. No consistent relationship was however observed between N2O emissions during the considered period and total precipitation or mean temperature.

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3.2. Cumulative N2O emissions affected by main cropping system modalities (LI vs. VLI) The cumulative N2O emissions for each crop or fallow period from the studied rotations (LI + CC, LI-CC, VLI + CC, VLI-CC) are illustrated in Fig. 4. Total cumulative emissions over the whole rotation were higher for the VLI cropping system (mean of the two cover crop modalities: 3375 g N2O-N ha
1) than for the LI cropping system (2342 g N2O-N ha
1). In both systems, the N2O emissions were higher during the main crop cycles than during the other periods. The contribution of the main crop cycles to total emissions was much higher for LI (78%) than for VLI (55%). The occurrence or absence of cover crops did not result in noticeable differences in emissions whatever the cropping system (LI or VLI). Results from the multifactor analysis of variance, with the cropping system (LI or VLI) as the first factor and the peer group as the second factor, are given in Table 1. A total of 95 values of cumulative emissions from individual chambers was used in that analysis. The peer group effect first appears very strong and significant, which was expected given for example the large interannual variations observed for N2O emissions. Once that source of variation isolated, a significant effect of the main treatment could be detected (P = 0.0186), which is consistent with the noticeable difference in cumulative emissions between LI and VLI at the scale of the whole rotation. Over all periods considered, the mean difference VLI-LI is 144 g N2O-N ha
1. Results are different if we consider separately the main crop and the fallow periods. In the first case the main treatment effect vanishes (P = 0.2355) while it is highly significant for fallow periods only (P = 0.0047), with twice

LI+CC clover sunflower 20 478

VLI+CC

wheat 626 (329)

Mustard+vetch wheat 519 675 (581) fababean 776

regrowth 109

phacelia+vetch 444 sorghum 447

oat+vetch oat 938 4 sunflower 398

LI−CC bare soil sunflower 30 1064

bare soil 151 sorghum 275

VLI−CC

wheat 753 (499)

bare soil 381

wheat 847 (757)

fababean 481 bare soil 289

bare soil 14

bare soil 1207

sunflower 512

Fig. 4. Polar histograms of the cumulative N2O emissions (g N2O-N ha
1) obtained for all main crop and fallow periods over the whole three-year rotation for the four cropping systems modalities (LI + CC, LI-CC in red; VLI + CC, VLI-CC in green). Cumulative N2O emissions are proportional to the area figured (duration x intensity of emission). Dark colors correspond to main crops and light colors to fallow periods (bare soil or cover crop). Values in brakets are the standard deviation of N2O emissions obtained from different years of measurement when available. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.)

more emissions for VLI than LI. Finally, the interaction between the cropping system factor and peer group was highly significant (P = 0.0026). When plotting cumulative N2O emissions from each component of the rotation against mineral N input for the same period (Fig. 5), no consistent relationship can be established (R2 = 0.33, P = 0.0327 for LI; R2 = 0.07 for VLI). This conclusion holds even if we only consider the LI cropping system without legumes as main crop, or if we focus on the wheat crop for which we have the highest number of observations. 3.3. Cumulative N2O emissions affected by cover crops and residue management The design of the experiment, with both cover crop modalities (+CC and
CC) present on each plot, makes the study of the effect of cover crops on N2O emissions very powerful. The cumulative emissions were compared on paired treatments (+CC,
CC) which share the same plot, climate and main cropping system modality (LI or VLI). The multifactor analysis of variance of the 83 individual chambers cumulative N2O values, with cover crop modality as the first factor and peer group (same period of measurement, same plot) as the second factor, showed that the effect of conducting a cropping system with or without cover crops was non-significant. That conclusion holds both for main crop and fallow periods combined and for fallow periods only (P = 0.46 and P = 0.92 respectively, Table 2). The linear regression of N2O emission values for +CC vs. N2O emission values for
CC, using data from fallow periods only (LI and VLI combined), yielded a R2 value of 0.89 and a slope of 0.86. It confirms that N2O emissions were comparable in the +CC and
CC modalities and indicates a tendency for slightly lower emissions when a cover crop is present. The same tendency is observed when both main crop periods and fallow periods are considered (R2 = 0.74, slope = 0.85). Separating non legume from mixed (legume + non-legume) cover crops suggests that N2O emissions could depend on the nature of the cover crop, with higher emissions when a legume is present. However the limited number of cases without legume crops (n = 6) does not allow to draw a solid conclusion. Separating sub-periods inside each fallow cycle, i.e. before and after destruction of the cover crop, also suggests higher emissions after destruction. Sustained N2O fluxes were observed in several cases after destruction of the cover-crop during several days (Fig. 3). Short term N2O emissions after the return of crop residues to soil are expected to be influenced by the amount of residues and their management, particularly their incorporation into the soil by tillage. This effect was studied by analysing the difference in N2O emissions (DN2O) between the few days preceding harvest of a main crop, destruction of a cover crop or mechanical weeding, and the days following these events. Fig. 6 shows boxplots of DN2O corresponding to each class of tillage and residue return combination defined in Section 2.4.2 for a 10 days period, knowing that similar results were obtained with the flexible duration method. No significant difference was observed between N2O emissions after and before the TR0 events (P = 0.30). Since the events considered in this class are essentially mechanical weeding interventions, this shows that frequent superficial tillage which is substituted to herbicide use did not result in increased N2O emissions and that the effect of tillage alone, without significant amounts of residues, remains limited. On the contrary, N2O emissions increased significantly in the TR
and NTR+ classes (P = 0.004 and P = 0.002, respectively), together with CO2 emissions, indicating that the presence of residues has a more pronounced effect than tillage itself. The decrease in emissions found in the TR+ class (P = 0.012), i.e. deep tillage (ploughing) with high amounts of crop residues, seems contradictory with the previous results. A careful analysis revealed that this decrease was

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151

Table 1 Effect of main cropping systems modalities (LI and VLI) on cumulative N2O emissions (g N2O-N ha
1). Both main crop and cover crop periods were considered. The peer group variable allowed to eliminate other sources of variation such as climate for example. Values in brackets correspond to the standard deviation of the mean. Mean (Sigma)

Count

Df

P-Value

cropping system modality (LI vs. VLI) peer group*cropping system modality peer group residual TOTAL (corrected)

263 (42) vs. 407 (42)

47 vs. 48

1 13 13 67 94

0.0186 0.0026 0.0000

Cumulative N2O emissions (kg N2O−N ha−1)

Source of variation

2.0 LI VLI

1.5

1.0 yLI = 0.0031xLI + 0.25 R²=0.33, P=0.0327 0.5

0.0 0

50

100

N−fertiliser (kg N ha−1)

150

Fig. 5. Relationship between the cumulative N2O emissions measured for each crop or fallow period and the mineral N fertilizer applied during the same period. The two main cropping systems (LI, VLI) are differentiated whereas both cover crop modalities (+CC,
CC) are confounded. The dashed line represents the linear regression of cumulative N2O emissions vs. N input for LI. Errors bars are the standard deviation of N2O emission obtained from the chamber replicates.

mainly due to an interference with the effect observed for NTR+: the tillage events considered in class TR+ indeed most often followed the mechanical destruction of the cover crop which has increased N2O fluxes. The decrease observed for TR+ is thus simply related to N2O fluxes coming back to the baseline. N2O emissions thus seem to be enhanced when crop residues appear at or near the soil surface. 3.4. Influence of environmental conditions and mineral nitrogen availability on emissions We used a decision tree approach to explore how soil water content and temperature in the top soil (0–0.10 m) influenced daily N2O emissions and to identify possible thresholds in processes behaviour, keeping in mind that such an approach remains essentially descriptive and can be quite sensitive to options such

as the minimum number of observations in a leaf. Only a limited fraction of the variance in daily N2O fluxes (6%) could be explained by combining the effects of soil water content (0–0.10 m), soil temperature (0–0.15 m) and LI vs. VLI differentiation (Fig. 7). This result points out the difficulty in predicting daily N2O emissions on this site. However some interesting observations can be done. First, the WFPS in the upper soil layer (calculated at
0.10 m) had a dominant effect on daily N2O fluxes: the highest fluxes were obtained for WFPS ranging from 32% to 69%, while they were lower below 32% and even lower above 69%. Furthermore, temperature was found to be another explaining factor interacting with WFPS: daily N2O fluxes increased when temperature exceeded a 13  C threshold and when WFPS was in the medium range (between 32 and 69%). The effect was greater in the LI than in the VLI rotation which was less affected by temperature. Plotting daily N2O emissions versus daily WFPS allowed to get a more continuous view of the effect of soil water content on emissions. We separated the different seasons to exclude the temperature effect and distinguished the two rotations to eliminate additional sources of variation. Results shown in Fig. 8 confirmed the existence of a strong but complex WFPS effect. This effect appeared very clearly in summer, during which the relationship between WFPS and N2O emissions is non-linear (particularly for VLI) with high emissions occurring above 60% WFPS. Important emissions also occurred in VLI during the other seasons when WFPS varied between 50% and 70%. The pattern of emissions is less clear in spring, the highest values being more evenly distributed over the whole WFPS range. However the highest peaks were observed when WFPS was around 40%. In the LI cropping system, emissions were concentrated in spring and summer with very low emissions in autumn and winter. On the contrary, emissions occurred all the year round in the VLI system. Soil mineral N (NH4+, NO3
) was measured less frequently (every month) which hampers a detailed analysis of its relationship with N2O emissions. However, some conclusions can be drawn (Fig. 9). The ammonium concentration (not shown) in the upper layer (0–0.15 m) strongly and briefly increased after N fertilization and then came back to very low values (<2 mg NH4-N kg
1), both for LI and VLI cropping systems. Basal values remained however slightly higher in the VLI cropping system. Nitrate concentration was more variable and generally higher: about 50% of the values were between 2 and 8 mg NO3-N kg
1, with no significant difference between LI and VLI. Nitrate concentration was of the same order of magnitude in the second layer (0.15–0.30 m), again with little

Table 2 Effect of cover crop modalities (+CC,
CC) on cumulative N2O emissions (g N2O-N ha
1). Both main crop and cover crop periods were considered. The peer group variable allowed to eliminate other sources of variation such as climate and plot for example. Values in brackets correspond to the standard deviation of the mean. Source of variation

LS Mean (LS Sigma)

Count

Df

P-Value

cover crop modality (+CC vs.
CC) peer group * cover crop modality peer group residual TOTAL (corrected)

509 (33) vs. 543 (32)

41 vs. 42

1 13 13 55 82

0.4562 0.0746 0.0000

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4.1. Variations in N2O emissions and role of climatic conditions

4.2. Levels of emissions and fertilization effect

The coefficient of variation of cumulative emissions, calculated from replicate chambers inside a plot, was low with most values below 50%. Such low values are due to both i) the smoothing effect of integrating fluxes over a long period of time: larger values of the coefficient of variation are generally observed at a daily scale (Barton et al., 2015; Dobbie et al., 1999; Grossel et al., 2014) and ii) the large area of the chambers which allows to integrate a high proportion of the often substantial fine scale variability in N2O emissions (Bessou et al., 2010). On the contrary, large variations have been observed when the same component of a rotation was measured on different years, which could indicate a strong influence of the climatic conditions. Soil moisture was actually shown to have a strong influence on emissions. Emissions were generally stimulated by an increase in WFPS. This is especially clear in summer for example, with a strong increase in emissions above 50% WFPS. That kind of relationships and threshold value is close to what was expected either from

N2O emissions at the scale of the whole three-year rotation were of 0.78 and 1.12 kg N2 O-N ha
1 year
1 respectively for the LI and VLI system (on average over +CC and
CC). These values are in line with the findings of Bouwman et al. (2002), who reported in arable crops rather stable N2O emissions, of the order of 1 kg N2ON ha
1, for N input between 25 and 150 kg N ha
1. Similar results were found by Van Groenigen et al. (2010), with emissions remaining essentially stable between 1 and 2 kg N2O-N ha
1 up to a fertilizer application rate of 187 kg ha
1 before increasing strongly. In more arid arable crop areas, lower emissions levels have been reported: Tellez-Rio et al. (2015) reported for example cumulative emissions less than 0.2 kg N2O-N ha
1 year
1 on a fallow-wheat, while N2O emissions ranged between 0.18–0.77 kg N2O-N ha
1 year
1 in the Kessavalou et al. (1998) study and 0.10–0.65 kg N2ON ha
1 year
1 in the case of Dusenbury et al. (2008). Dryer conditions and the low N input associated to the reduced yield potential might explain these lower values. The same trend could

∆ N2O (g N2O−N ha−1) −4 −2 0 2 4 6 4. Discussion

other field results (Dobbie et al., 1999) or modelling (Metivier et al., 2009), although when denitrification is involved the WFPS threshold is often higher. In fall and winter, higher emissions also occurred preferentially between 50 and 70% WFPS. Above 70% WFPS, emissions tend to decrease, which was also highlighted by the decision tree analysis. Such a decrease was rather expected at WFPS values in the 80–90% range if associated to emissions induced by denitrification, when the anoxic volume of soil is important and favours the reduction of N2O to N2 (Metivier et al., 2009). In spring, the highest peaks were observed when WFPS was around 40%. They might be linked to a strong nitrification activity associated to the application of mineral fertilizers containing ammonium. Globally, the fact that N2O emissions increase with WFPS in the low to medium range but decrease above WFPS values as low as 70% suggests dominance of the nitrification N2O production process over the denitrification one, which was also proposed by Menéndez et al. (2008) for similar cropping systems under Mediterranean conditions. The effect of temperature was less visible. Emissions were higher above 13  C for the LI cropping system in the intermediate range of WFPS, as shown by the decision tree. However, it may be only the indirect consequence of the fact that on LI, high N availability mainly occurs during the post-fertilization period in spring, which is also warmer.

216 24

54 24

TR0

TR−

TR+

NTR+

Fig. 6. Change in 10-day cumulative N2O emissions (DN2O) induced by different types of events: TR0 = shallow tillage without residue input; TR- = shallow tillage with moderate residue input; TR+ = deep tillage with high residue input; NTR + = mechanical destruction of cover crops without tillage. Numbers represent the number of observed situations.

difference between LI and VLI. It was however higher in the VLI system during the fallow period following the faba bean crop compared to the corresponding fallow period of the LI system.

3.1 n=4815 100% yes WFPS >= 69 no

3.4 n=4063 84% WFPS < 32 3.7 n=3545 74% 3.2 n=1579 33% Tsol < 13 rotation = LI

1.3 n=752 16%

1.7 n=518 11%

1.1 n=423 9%

4 n=1156 24%

4.1 n=1966 41%

Fig. 7. Decision tree classifying daily N2O fluxes (g N2O-N ha
1 day
1) according to environmental conditions (WFPS and temperature) and main cropping system (LI or VLI). The number of observations in each class (n) is indicated, as well as the proportion of the total number of observations in each class. Color intensity is proportional to mean N2O flux in the class.

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153

Fig. 8. Daily N2O emissions versus water filled pore space (WFPS) at
10 cm for each main cropping system (LI, VLI) and season.

Fig. 9. Daily rainfall (a) and evolution of nitrate concentration (mg NO3-N kg
1 soil) in the upper soil layer (0–15 cm) for each main cropping system: LI + CC and LI-CC (b, c), VLI + CC and VLI-CC (d, e). Horizontal arrows delimitate the different crop and fallow periods. Fertilization (F), crop residue crushing (C) and residue incorporation (I) are indicated by vertical dotted lines.

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be observed for yield scaled emissions: mean values for wheat were similar for both LI and VLI systems (120 and 128 g N2O-N t DM
1), which is less than values published by Lebender et al. (2014) for winter wheat over a range of N rates in six sites in northwest Germany (177–191 g N2O-N t DM
1) but close to values obtained by Zhu-Barker et al. (2015) in drier conditions and when wheat was fertilized. The weak dependency of N2O fluxes on N input, even in the LI cropping system with mineral fertilizing only (96 kg N ha
1 year
1 in average), is also consistent with the previously cited studies (Bouwman et al., 2002; Van Groenigen et al., 2010). The fact that a weak relationship is often reported when N input is in the low range might be related to less opportunity for N2O losses due to excessive fertilization. Here, another possible reason for such a weak relationship could be the important range of variation in emissions observed during bare soil periods, when there is no N input, with quite high fluxes occurring occasionally especially on the VLI system. The already discussed strong influence of climatic conditions might explain for part such variations. Whatever the causes of the weak relationship between N inputs and emissions, the applicability of IPCC Tier 1 approaches to the studied systems is severely limited. 4.3. Influence of management practices The studied cropping systems mainly differed by legume contribution to N input and use of cover crops. We have confirmed the very limited effect of cover crops on N2O emissions, especially at the scale of the whole rotation. This is consistent with the results of Negassa et al. (2015) for rye cover crop in North America or from the recent meta-analysis conducted by Basche et al. (2014). The latters showed that on average, cover crops only lead to negligible increase in N2O emissions when measured for time periods of one year or greater. Their analysis also indicated that legume cover crops were more susceptible to increase N2O emissions, which fits with our observation despite the limited number of cases without legume cover crops in our study. At short term, we observed some increase in N2O fluxes after the destruction of the cover crop. That destruction was not immediately followed by tillage, and residues were thus not incorporated into the soil. Such increase in N2O emissions is consistent with results suggesting an important effect of mulches on emissions (Shan and Yan, 2013), but not with findings from the Basche et al. (2014) meta-analysis, where incorporation was found to stimulate N2O emissions. However, it is important to keep in mind that the observed changes in N2O fluxes generally lasted a few days and represented small quantities of N2O (order of magnitude: 10 g N2O-N ha
1), which is why differences associated to the presence or absence of cover crops are not noticeable at the scale of a crop cycle or a rotation. Other short term events involving the combination of tillage and incorporation of main crop residues or weeds did not have any significant influence. The LI and VLI cropping systems differ regarding the contribution of symbiotic fixation to N inputs. Total mineral N input over the whole rotation is 288 kg N ha
1 for the LI cropping system, while it is 100 kg N ha
1 for the VLI cropping system. We used the relationship between N fixed and shoot dry matter proposed by Herridge et al. (2008) in their meta-analysis of the global input of biological nitrogen fixation in agricultural systems to estimate N input from legumes in the VLI system to about 150 kg ha
1. Total N input in the VLI cropping system is thus of the same order of magnitude than in the LI cropping system: 250 kg N ha
1 vs. 288 kg N ha
1. N losses in the form of N2O represent 0.8% of total N input on LI vs. 1.3% of total N input on VLI which in both cases is close to the default IPCC emission factor. However we already discussed the fact that little relationship seems to exist between fertilization and N2O emissions on the site and that emissions vary

widely between bare soil periods. That suggests that background emissions and emissions due to the turnover of soil organic matter or crop residue might have a dominant influence and that fertilizer induced emissions are actually much lower than 1% N input. Numerous recent studies indeed suggest emissions factors values close to the lower limit of the IPCC (2007) Tier 1 EF1 uncertainty (0.03% to 3%): 0.14–0.42% in Venterea et al. (2011), 0.17% in the meta-analysis of Buckingham et al. (2014), 0.1–0.37% in Lebender et al. (2014), 0.09–0.64 in Zhu-Barker et al. (2015), among others. The strong development of intensive measurements (1 per day or more) may be one reason of the downwards adjustment of emission factors, as suggested by Bouwman et al. (2002). Whatever the way we look at the difference in N2O emissions between the LI and VLI cropping systems (per unit surface area, yield or N input), emissions are always slightly higher in the VLI cropping system, which is consistent with results obtained by Menéndez et al. (2008) for similar cropping systems and under Mediterranean climate. High values of the coefficient of variation of cumulative emissions are also more frequent. The contribution to emissions of the main crop periods, during which fertilization takes place, was found to be much higher for the LI system (78%) than for the VLI system (55%). Emissions were actually more evenly distributed over the whole rotation, including fallow periods, in the VLI cropping system. Emissions during the legume crop period were not higher than for wheat during the same period. Schwenke et al. (2015) reported that most (75%) of the annual N2O losses from the legumes occurred post-harvest in their study. Rochette and Janzen (2005) also suggested that the increased N2O release associated with legume crops could be attributed to enhanced N release from decomposing leguminous residues, including roots and nodules, both during crop growth and after harvest. The more persistent significant N2O fluxes in the VLI cropping system together with the higher soil nitrate content found in this system during the 6 month after the faba bean harvest may support that hypothesis. The same behaviour was observed by Menéndez et al. (2008) for a wheat-faba bean rotation compared to a wheatsunflower rotation. The strong difference in the pattern of emissions between the LI and VLI cropping systems might indicate that the dominant processes at the origin of emissions differs. Short pulses of N2O emissions occurring only in the days following fertilization in the LI system are likely to correspond to a very active nitrification, which is comforted by WFPS values in the 30– 50% range. This is less clear for the sustained fluxes over long periods on the VLI system. However the range of WFPS corresponding to the higher fluxes also rather supports a strong contribution of nitrification activity. The steadiness of N2O fluxes on the VLI cropping system as well as the scarcity of very high flux values, the low soil carbon content, also argue against a strong denitrification activity. That assumption of a dominant contribution of nitrification, which was also suggested by Menéndez et al. (2008) for similar cropping systems under Mediterranean conditions, is worth being more effectively tested as it could help to evaluate whether the results obtained here in the context of the south of France would hold in more humid climates or in irrigated situations. It would also help to imagine how to make those systems more efficient through changes in practices, for example using nitrification inhibitors or controlled or slow release fertilizers which could be an efficient way to reduce emissions on the LI system. Globally, the effect on N2O emissions of the studied practices (integration of legume crops, use of cover crops and the associated management of residue) is rather limited. When combined to the only weak observed relationship between N2O emissions and fertilization, even for the LI system which relies more strongly on N fertilizer input, it suggests that the adoption of such practices should be considered mainly on the basis of the benefits they have

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to address other important agronomic or environmental issues rather than their impact on N2O emissions. 5. Conclusion We have completed a solid evaluation of the N2O emissions of four cropping system alternatives which aim at reducing the environmental footprint of the conventional wheat-sunflower rotation in southern France. The studied systems mainly differed by legume contribution to N input and use of cover crops. N2O emissions have been monitored quasi-continuously during the three-year rotation in each system. Results showed that for all cropping systems considered emissions remained limited (0.71 to 1.15 kg N2O-N ha
1 year
1) and fell within the range of values expected for similar N input and climatic conditions. As anticipated, climatic conditions and in particular soil water content had a strong influence on emissions and induced a large inter-annual variability. We confirmed the very limited effect of cover crops on N2O emissions, especially at the scale of the whole rotation. Finally, substituting N from symbiotic fixation for mineral fertilization in the VLI cropping system did not result in a decrease in N2O emissions: N2O emissions were slightly higher than on the LI cropping system without legume main crop and they were also more regular over time. Acknowledgments This study was supported by the French National Research Agency (project ANR-09-STRA-06; MicMac-design, Programme STRA 2009) and the French Agency for the Environment and Energy Management (ADEME, Reacctif Research Program, EFEMAIR-N2O Project). The authors would like to thank D. Raffaillac, D. Chesneau, M. Labarrère and B. Gleizes at INRA, UMR AGIR, for their efficient technical help, and A. Gavaland, E. Bazerthe and P. Bruno at the INRA Auzeville experimental unit for technical assistance on the cropping system experiment. References Barton, L., Wolf, B., Rowlings, D., Scheer, C., Kiese, R., Grace, P., Stefanova, K., Butterbach-Bahl, K., 2015. Sampling frequency affects estimates of annual nitrous oxide fluxes. Nat. Sci. Rep. 5, 15912. doi:http://dx.doi.org/10.1038/ srep15912. Basche, A.D., Miguez, F.E., Kaspar, T.C., Castellano, M.J., 2014. Do cover crops increase or decrease nitrous oxide emissions? A meta-analysis. J. Soil Water Conserv. 69, 471–482. doi:http://dx.doi.org/10.2489/jswc.69.6.471. Bessou, C., Mary, B., Léonard, J., Roussel, M., Gréhan, E., Gabrielle, B., 2010. Modelling soil compaction impacts on nitrous oxide emissions in arable fields. Eur. J. Soil Sci. 61, 348–363. doi:http://dx.doi.org/10.1111/j.1365-2389.2010.01243.x. Bouwman, A.F., Boumans, L.J.M., Batjes, N.H., 2002. Emissions of N2O and NO from fertilized fields: summary of available measurement data. Global Biogeochem. Cycles 16 (4), 6-1-6-13. doi:http://dx.doi.org/10.1029/2001GB001811. Buckingham, S., Anthony, S., Bellamy, P.H., Cardenas, L.M., Higgins, S., McGeough, K., Topp, C.F.E., 2014. Review and analysis of global agricultural N2O emissions relevant to the UK. Sci. Total Environ. 487, 164–172. doi:http://dx.doi.org/ 10.1016/j.scitotenv.2014.02.122. Carter, M.S., Ambus, P., 2006. Biologically fixed N2 as a source for N2O production in a Grass–clover mixture, measured by 15N2. Nutr. Cycling Agroecosyst. 74, 13– 26. doi:http://dx.doi.org/10.1007/s10705-005-4111-0. Casler, M.D., Vermerris, W., Dixon, R.A., 2015. Replication concepts for bioenergy research experiments. BioEnergy Res. 8, 1–16. doi:http://dx.doi.org/10.1007/ s12155-015-9580-7. Chikowo, R., Faloya, V., Petit, S., Munier-Jolain, N.M., 2009. Integrated Weed Management systems allow reduced reliance on herbicides and long-term weed control. Agric. Ecosyst. Environ. 132, 237–242. doi:http://dx.doi.org/ 10.1016/j.agee.2009.04.009. Conen, F., Dobbie, K.E., Smith, K.A., 2000. Predicting N2O emissions from agricultural land through related soil parameters. Global Change Biol. 6, 417–426. doi:http:// dx.doi.org/10.1046/j.1365-2486.2000.00319.x. Constantin, J., Mary, B., Laurent, F., Aubrion, G., Fontaine, A., Kerveillant, P., Beaudoin, N., 2010. Effects of catch crops, no till and reduced nitrogen fertilization on nitrogen leaching and balance in three long-term experiments. Agric. Ecosyst. Environ. 135, 268–278. doi:http://dx.doi.org/10.1016/j.agee.2009.10.005.

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