- Email: [email protected]
Nitrous Oxide Emission by Agricultural Soils: A Review of Spatial and Temporal Variability for Mitigation
Pedosphere 22(4): 426–433, 2012 ISSN 1002-0160/CN 32-1315/P c 2012 Soil Science Society of China Published by Elsevier B.V. and Science Press
Nitrous Oxide Emission by Agricultural Soils: A Review of Spatial and Temporal Variability for Mitigation∗1 1,2,∗2 3 ´ ´ C. HENAULT , A. GROSSEL1 , B. MARY3 , M. ROUSSEL3 and J. LEONARD 1 INRA,
UR 272 Science du Sol, Centre de Recherches d’Orl´ eans, CS 40001 Ardon, 45075 Orl´ eans cedex 2 (France) de Bourgogne, UMR 1229 Microbiologie du sol et de l’Environnement, 17 rue Sully, BP 86510, 21065 Dijon cedex
2 INRA-Universit´ e
(France) 3 INRA, US 1158 Agro-Impact, Pˆ ole du Griffon, 180 rue Pierre-Gilles de Gennes, 02000 Barenton-Bugny (France) (Received February 4, 2012; revised May 2, 2012)
ABSTRACT This short review deals with soils as an important source of the greenhouse gas N2 O. The production and consumption of N2 O in soils mainly involve biotic processes: the anaerobic process of denitrification and the aerobic process of nitrification. The factors that significantly influence agricultural N2 O emissions mainly concern the agricultural practices (N application rate, crop type, fertilizer type) and soil conditions (soil moisture, soil organic C content, soil pH and texture). Large variability of N 2 O fluxes is known to occur both at different spatial and temporal scales. Currently new techniques could help to improve the capture of the spatial variability. Continuous measurement systems with automatic chambers could also help to capture temporal variability and consequently to improve quantification of N2 O emissions by soils. Some attempts for mitigating soil N2 O emissions, either by modifying agricultural practices or by managing soil microbial functioning taking into account the origin of the soil N2 O emission variability, are reviewed. Key Words:
agricultural practices, fertilization, greenhouse gas, N2 O fluxes, soil-atmosphere interface
Citation: H´ enault, C., Grossel, A., Mary, B., Roussel, M. and L´eonard, J. 2012. Nitrous oxide emission by agricultural soils: A review of spatial and temporal variability for mitigation. Pedosphere. 22(4): 426–433.
INTRODUCTION On the issue of global warming and its causes, the Working Group I Summary for Policymakers of the Intergovernmental Panel on Climate Change (IPCC) recently stated that 1) “warming of the climate system is unequivocal”, and 2) “most of the observed increase in globally averaged temperatures since the mid-20th century is very likely (the assessed likelihood, using expert judgment, are over 90%) due to the observed increase in anthropogenic greenhouse gas concentrations” (IPCC, 2007). The three long-lived greenhouse gases carbon dioxide, methane and nitrous oxide have indeed increased markedly as a result of human activities since 1750 and now far exceed pre-industrial values. The concentration in nitrous oxide, which has a very high radiative forcing per unit mass or molecule (296 times higher than the one of CO2 on a 100 years period), have risen from a pre-industrial value of 270 ppb to a 2005 value of 319 ppb, mainly due to human activities, primarily through agriculture and the increase in use of industrial fertilizers. Beyond its ∗1 Supported
greenhouse effect, N2 O is now also the major ozonedepleting substance in the stratosphere (Ravishankara et al., 2009). Agricultural soils are assessed to produce 2.8 (1.7–4.8) Tg N2 O-N year−1 and thus appear as the main anthropogenic source of this gas (IPCC, 2007). Amongst the greenhouse gases, nitrous oxide is estimated to contribute to 8% of the radiative forcing at the global scale while amongst the human activities, agriculture is estimated to contribute to 14% of the radiative forcing. At the national scale, in France, recent estimations indicated that agriculture contributes to 21% of the radiative forcing and to 84% of the anthropogenic N2 O emission (CITEPA, 2011). It is thus a key issue to be able to understand how N2 O emissions by agricultural soils occur and to derive mitigation strategies from this knowledge. BACKGROUND ON PROCESSES AND EFFECTS OF AGRICULTURAL PRACTICES ON N2 O FLUXES Soils can act both as a source and a sink of
by the Region Centre, the Fonds Europ´een de D´ eveloppement R´ egional and the INRA, France, through the SpatioFlux Program. ∗2 Corresponding author. E-mail: [email protected].
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
N2 O (Syakila and Kroeze, 2011). However on the global scale, the source activity largely dominates the sink one. The production and consumption of N2 O in soils mainly involve biotic processes. Nevertheless, small amounts of N2 O may be produced through nonbiological processes, i.e., the chemical decomposition of nitrite (or chemodenitrification) and the chemical decomposition of hydroxylamine (Bremner, 1997). As far as biological processes are concerned, numerous groups of microorganisms contribute to the production and consumption of N2 O (Conrad, 1996), but biological nitrification and denitrification are considered as the dominant processes involved (Fig. 1). Only denitrification is recognized as a significant biological consumptive fate for N2 O (Vieten et al., 2008). The nitrification process, classically observed in aerobic conditions, is the successive biological oxidation of ammonium to nitrite and nitrate. It is well known that the nitrification process can be performed by some autotrophic bacteria. For example, Nitrosomonas oxidize ammonium to nitrite and Nitrobacter oxidize nitrite to nitrate (Bremner, 1997). Evidence of the contribution of Crenarchaea in ammonia oxidation in soil ecosystems has recently been reported (Leininger et al., 2006). Beyond nitrite and nitrate, the nitrification process can also lead to the release of greenhouse gases N2 O as demonstrated by laboratory studies on pure cultures (Blackmer et al., 1980) or on soil samples (Garrido et al., 2002). Mechanisms leading to the release of N2 O during nitrification are not clearly understood. Some authors proposed that N2 O is formed during the oxidation of ammonium while the mechanisms of nitrification/denitrification, i.e., the production of N2 O from NO− 2 produced through nitrification, is more and more mentioned in the literature. Under oxygen limited conditions, nitrifiers could use NO− 2 as a terminal electron acceptor (Ritchie and Nicholas, 1972; Bremner, 1997). Denitrification refers to the dissimilatory reduction, by essentially aerobic bacteria placed in anaerobic conditions, of one or both of the ionic
Fig. 1
427 − nitrogen oxides (nitrate, NO− 3 , and nitrite, NO2 ) to the gaseous oxides (nitric oxide, NO and nitrous oxide, N2 O), which may themselves be further reduced to dinitrogen (N2 ). During denitrification, the nitrogen oxides act as terminal electron acceptors in the absence of oxygen (Knowles, 1982). Denitrification capacity is present in many prokaryotic families, including phototrophs, lithotrophs and organotrophs like the species of Pseudomonas or Alcaligenes. The first step of the denitrification process, i.e., the utilization of nitrate as an electron acceptor, is widespread in the environment and could be carried out by a large proportion of soil microorganisms. In contrast, organisms able to reduce nitrite into N2 O or N2 would represent only 0.1% to 5% of the soil bacteria (Philippot and Germon, 2005). Driving denitrification to its term (N2 , inert form of nitrogen) is of great environmental interest because it results in the elimination, without transfer of pollution, of the soluble forms of nitrogen (NO− 3, ) that may i) interfere with public health through NO− 2 high concentrations in drinking water and food and ii) contribute to the eutrophication through elevated concentrations in surface water. However, when the reduction step of denitrification is slowed down, NOx , and N2 O are released into the atmosphere and are involved in the atmospheric pollution. As a result of the usual coexistence of aerobic and anaerobic zones in soils (Arah, 1990), nitrification and denitrification can occur simultaneously, and the contribution of each process varies with soil water content (Bateman and Baggs, 2005). Recently, Stehfest and Bouwman (2006) summarized information from 1 008 published N2 O emissions for agricultural fields. The meta-analysis they performed indicates that the factors that significantly influence agricultural N2 O emissions deal with agricultural practices (N application rate, crop type, fertilizer type) and soil conditions (soil organic C content, soil pH and texture). At the global scale, Bouwman (1996) as well as Stehfest and Bouwman (2006) observed a
Main processes involved in N2 O budget. Adapted from H´enault et al. (2005).
´ C. HENAULT et al.
428
linear relationship between N2 O emission and N application rate. This relationship allows to calculate a fertilizer-induced emission (FIE) indicator which is often used to estimate anthropogenic N2 O emission from fertilizer, animal manure and other N inputs (IPCC, 2007). This FIE is estimated to 0.91% (with a large uncertainty) which means that globally 0.91% of the N applied on soil is directly lost as N2 O. The influence of crop type is mainly visible for flooded rice systems, which could produce rather low fluxes of N2 O due to more complete denitrification (FAO, 2001) and, to a lesser extent, cereals and grass which have lower emissions compared to legumes. Concerning fertilizer types, Stehfest and Bouwman (2006) observed higher emissions for the calcium ammonium nitrate form and lower emissions for the ammonium phosphate form, and Eichner (1990) observed higher emissions for anhydrous ammonia fertilizers. Contradictory results have often been observed about the effect of soil tillage, despite a general trend of greater emissions in no till (or low till) systems. However, the difference observed between tillage modalities for short-term studies seems to disappear when long-term field trials, with a long history of differentiation, are considered (Six et al., 2004). The difficulty to draw solid conclusions about the effect of agricultural practices, beyond the effect of nitrogen inputs, is for a large part due to the interaction with factors related to soil conditions. The large effect of soil water content on N2 O emissions, especially through denitrification, has also been underlined by numerous authors (Conen et al., 2000; Farquharson and Baldock, 2008). Stehfest and Bouwman (2006) also found soil organic C content, soil pH and soil texture to have a significant influence on N2 O emis-
sions. Emissions were observed to increase with soil organic C content, which reflects the positive correlation between soil organic C content and the rates of denitrification and nitrification (Tiedje, 1988). Lowest emissions were observed for pH values > 7.3. The N2 O emissions from acidic soils generally exceed those from alkaline soils and probably reflect the reported higher N2 O emission from nitrification (Martikainen and De Boer, 1993) or higher N2 O:N2 ratio (Alexander, 1977) at low pH compared to high pH. Emissions are also generally higher for fine-textured soil than for coarse- and medium-textured soils, because of the more frequent occurrence of anaerobic conditions associated with higher water contents (Parton et al., 1996; FAO, 2001). PATTERNS OF N2 O EMISSIONS BY AGRICULTURAL SOILS AND PERSPECTIVES FOR IMPROVING THE CAPTURE OF VARIABILITY Most approaches for measuring N2 O emissions in field conditions fall into two main categories: chamber and micrometeorological techniques, whose benefits and limits are presented in Table I. Using the database compiled by Stehfest and Bouwman (2006) and available at http://www.mnp.nl/images/stehfest data tcm61-29733.xls, daily N2 O fluxes appeared to be comprised between −2 (Goossens et al., 2001) and 5 400 g N ha−1 d−1 (Abbasi and Adams, 2000), both values being obtained under temperate climate. The variability of N2 O fluxes is known to occur both at different spatial and temporal scales. Specific studies have shown a very high spatial variability of N2 O emissions at different scales, from the
TABLE I Complementarities of chambers and micrometeorological methods for measuring greenhouse gas emissions at the soil-atmosphere interfacea)
Equipment constraints Cost of installation Technical level required Human labor charge Use constraints Methodological bias
Performances Limit of detection Representativity Use a) Adapted
Chambers
Micrometeorology
About 50 000 Euros Basic Very important Could be used anywhere Disturbance of microclimate in chambers Change in gas concentration in chambers Exploring of a small spatial and temporal proportion of systems
About 200 000 Euros Very high Important Could only be used on large and flat surfaces Make sure to take into account the conditions of atmospheric stability and wind circulation to consider fairly the different emission sources and provide the correct values of flux
< 1 g N ha−1 d−1 Punctual measures in time and space Comparison of agricultural practices
Few g N ha−1 d−1 Integrative measures in time and space Estimation of gas fluxes in situations representative of ecosystems
from H´enault et al. (2005).
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
microscale one to the regional one (Parkin, 1987; Groffman and Tiedje, 1989) with coefficients of variations ranging between 50% and 200% (Ambus and Christensen, 1994; Yanai et al., 2003; Mathieu et al., 2006; Konda et al., 2008). van den Heuvel et al. (2009) compared N2 O fluxes at scales ranging from 0.000 13 to 0.31 m2 and found that “spatial variation was highest at the smallest scale”. At the fine scale < 1 m2 , this variability was observed to be linked to the presence of denitrifying microsites in soils (Parkin, 1987; Ambus and Christensen, 1994; Clemens et al., 1999). R¨over et al. (1999) and Yates et al. (2006) established variograms of N2 O emission and observed that the nugget effect was very important compared to the sill, indicating that most of the variability occurred at short distance (< 10 m). At distances beyond a few meters, the spatial variability can be linked to the mineral nitrogen availability or to topographic or micro-topographic effects. Local depressions at the soil surface can maintain soil moisture and lead to large N2 O emissions (Ball et al., 1997). The variability at the plot scale is often due to the presence of some very high fluxes on “hot spots”, which account for a significant part of the whole flux. For example, van den Heuvel et al. (2009) observed, during two campaigns in a riparian buffer zone, that 1% and 4% of the sampled surface were, respectively, responsible for 17% and 33% of the whole N2 O emissions during the measurement period. The presence of hot spots which emit at rates several orders of magnitude above the background N2 O fluxes was also reported in cultivated fields (e.g., Ball et al., 1997). Mathieu et al., 2006 (Fig. 2) studied 36 soil samples on a 20 m × 20 m cultivated field plot. They observed a high spatial variability without any spatial dependence at the scale of the experimental plot. Only a tenuous relationship was observed between N2 O emission and nitrate concentration amongst different soil properties. Spatial patterns of N2 O emissions are also very variable in time (Yates et al., 2006). Currently new techniques could help for improving the capture of the spatial variability. The development of fast analysers based on infrared spectrometry with quantum cascade laser (Neftel et al., 2010; Guimbaud et al., 2011) will allow to re-investigate the spatial variability either by increasing the number of replicates when coupled with simplified chambers like fast box (Hensen et al., 2006), or by covering larger area when used in association with micro-meteorological methods which integrates the spatial variability over large surfaces. These analysers also provide a very high sensitivity for gas analysis, which will be helpful for studying low fluxes and N2 O uptake by soils.
429
Fig. 2 Spatial distribution of N2 O fluxes on a 20 m × 20 m cultivated field plot. Adapted from Mathieu et al. (2006).
In a previous work, we studied the spatial variability of N2 O emissions at the regional scale, by analysing the respective effects of agronomic (type of crop, dose and nature of fertilizers), climatic and pedologic conditions, including 3 different soil types: a rendzina on a cryoturbed material, a hydromorphic leached brown soil and a superficial soil on a calcareous plateau (H´enault et al., 1998a, b, 1999). We observed a very marked effect of soil type on N2 O emissions. Two main factors, i.e., soil hydrology and the ability of the soil to reduce N2 O, appeared to play an essential role on this variability. In particular, the hydromorphic leached brown soil showed the highest emissions, 3 500 g N ha−1 over a 5 month period. This behaviour could be explained by a low drainage capacity and consequently high water filled pore space (Linn and Doran, 1984) associated with a very low N2 O reductase activity, i.e., a high N2 O:N2 ratio of the gas emitted during the denitrification process. We then developed a simple laboratory methodology to characterize soil N2 O reduction capacity. This approach, which can be used routinely, proved to be useful to discriminate soils with potentially high levels of N2 O emission at the field scale (H´enault et al., 2001; Hergoualc’h et al., 2009). A high temporal variability of soil N2 O fluxes is also observed at different scales (hours, days, seasons, years), which is expected since N2 O fluxes respond to climatic and agronomic events (Laville et al., 2011). Despite this temporal variability, measurements are most discontinuous in time (weekly to monthly measurements) and often realized over short periods. The discontinuous nature of the measurement strongly impacts the estimation of cumulative emissions (Smith and Dobbie, 2001; Parkin, 2008), and it was shown
430
that the uncertainty on cumulative emissions rose very quickly when the sampling interval changed from 4 to 10 days. With a sampling interval of 10 days, estimated cumulative emissions can fluctuate within a 50% interval around the expected value. Measurements restricted to periods extending over only a few months raise the problem of the representativity of the chosen period, given that the difference between N2 O emissions associated with different treatments such as tillage modalities can largely change during a crop rotation (unpublished results). Gregorich et al. (2005) also suggested that annual N2 O emissions based on growing-season measurements in Canada could be underestimated due to the concentrated N2 O emissions during freeze/thaw periods in winter and spring. Continuous measurement systems with automatic chambers can help to override these limitations, and have in addition some other positive consequences. For example, as chambers remain in place for long durations, it is possible to use chambers covering larger areas because they do not need to be moved frequently. So far, Bessou et al. (2010) proposed to use large chambers to integrate the heterogeneity of fluxes at a fine scale as they obtained systematically rather low coefficient of variation between replicate measurements (always less than 30%) with a sampling area of 0.5 m2 . Moreover, as concentration is measured frequently during chamber closure, the form of the N2 O accumulation kinetics is generally well apparent, and non-linear models can be used if necessary to better estimate the N2 O flux. Fig. 3 compares N2 O estimations obtained with respectively a linear and an exponential model. The inappropriate use of a linear model, i.e., when the
Fig. 3 Cumulative N2 O emissions estimated using either linear or exponential model during a whole sugarbeet growth cycle, in two years (2007 and 2008) and two soils (compacted and uncompacted). The data are from Bessou et al. (2010).
´ C. HENAULT et al.
the decrease in the concentration gradient between the soil and the atmosphere is progressive, results in a systematic underestimation of fluxes of about 35% with the linear model. Moreover, a generalization of continuous measurements allows detecting some quite unpredictable fluxes of N2 O. For example, Bessou et al. (2010) were able to measure significant N2 O fluxes during summer in sugarbeet fields in spite of dry conditions and low water contents in soil. However, economic or power supply constraints may prevent using continuous measurement systems. In these situations manual chambers remain the only accessible technique and the sampling frequency should be optimized. It has often been suggested that postfertilization periods, which generally exhibit high N2 O fluxes especially when they coincide with important rainfall, may require more frequent measurements (two per week during 3 weeks for example). However each situation is very specific, and numerical experiments have shown that increasing the sampling frequency during the post-fertilization period does not systematically improve N2 O emissions estimation. The use of N2 O emission models (Chen et al., 2008) may be a possible strategy for optimizing the sampling frequency and has to be tested. DEVELOPMENT OF MITIGATION STRATEGIES Oenema (1999) suggested that there are basically two strategies to decrease N2 O emissions from agriculture: 1) increasing the N use efficiency concomitantly to the lowering of the total N input, and 2) decreasing the release of N2 O per unit of nitrogen from nitrification and denitrification processes. Field tests have shown that nitrification inhibitors can limit N2 O from the application of ammonium-based fertilizers (Clough et al., 2007). Mosier et al. (1996) also proposed to adapt the nature of the fertilizer to the expected dominant process. For example, if nitrification is supposed to be the main contributor to N2 O fluxes, using a nitrate based fertilizer rather than an ammonium based one should limit N2 O production. Nevertheless, this methodology has not yet been tested in realistic conditions. The use of control traffic farming to mitigate N2 O emissions by minimizing the compacted soil area was also investigated in few studies. For example, Vermeulen and Mosquera (2009) obtained a 20% to 50% N2 O emission reduction with seasonally controlled traffic farming. This result is consistent with the known effect of compaction on the intensity of N2 O emissions: increasing by 20% to 50% on average (Hansen et al. 1993; Ruser et al. 1998; Ball et al., 1999; Sitaula et al., 2000; Yamulki and Jarvis, 2002;
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
Teepe et al., 2004). Temporal and spatial hotspots of N2 O fluxes represent a large part of the total emissions. Some targeted intervention on these hotspots could be of great interest for mitigating N2 O emissions, but this requires to identify the location in space and time of these hotspots as well as to understand their origin (soil conditions, agricultural practices). For example, important N2 O fluxes could be observed in specific situations, typically due to a poor capacity of soils to reduce N2 O into N2 . In these situations some innovating methodologies need to be proposed for increasing soils’ capacities to reduce N2 O. Sameshima-Saito et al. (2006) demonstrated that soybean roots nodulated with Bradyrhizobium japonicum USDA110, carrying the nosZ-gene, were able to reduce N2 O even at low concentration (Sameshima-Saito et al., 2006), suggesting that such soybean nodules could scavenge N2 O in soil and thereby lessen N2 O emission from soybean fields to the atmosphere. This could be a promising perspective for the mitigation of N2 O emission, especially in soils that are basically inefficient in reducing N2 O into N2 . CONCLUSIONS Large spatial and temporal variability of N2 O emissions by agricultural soils at different scales make it difficult to measure and predict the fluxes. Rough estimations can be obtained from total nitrogen inputs using the IPCC fertilizer-induced emission indicator but the development and evaluation of mitigation strategies imply a deeper understanding of the determinism of these emissions. Recent advances concerning the measurement of emissions and the development of indicators of soil N2 O emission potential will probably be of great help to improve and apply our knowledge. The development and generalization of continuous emission measurements will help to improve the estimation of fluxes and the integration over long periods such as a complete rotation. It will also allow to focus on processes often neglected because of their fleetingness, such as N2 O uptake by soils or N2 O peaks distant from fertilization events. Some analytical improvements for determining N2 O concentration in the atmosphere are also emerging. This will enable a best characterisation of the spatial variability of N2 O fluxes at different scales. Easily measurable indicators of soil N2 O emission potential will also help to detect situations that can potentially emit large level of N2 O. At the end, the spatial variability of N2 O emission, which makes it difficult to quantify the N2 O fluxes, may turn
431
to an opportunity for mitigation if we are able to understand it. REFERENCES Abbasi, M. K. and Adams, W. A. 2000. Gaseous N emissions during simultaneous nitrification-denitrification associated with mineral N fertilization to a grassland soil under field conditions. Soil Biol. Biochem. 32: 1251–1259. Alexander, M. 1977. Introduction to Soil Microbiology. 2nd Edition. John Wiley & Sons, New York. Ambus, P. and Christensen, S. 1994. Measurement of N2 O emission from a fertilized grassland: an analysis of spatial variability. J. Geophysic. Res. 99: 16549–16555. Arah, J. R. M. 1990. Diffusion-reaction models of denitrification in soil microsites. In Revsebech, N. P. and Sørensen, J. (eds.) Denitrification in Soil and Sediment. Plenum Press, New York. pp. 245–258. Ball, B. C., Horgan, G. W., Clayton, H. and Parker, J. P. 1997. Spatial variability of nitrous oxide fluxes and controlling soil and topographic factors. J. Environ. Qual. 26: 1399–1409. Ball, B. C., Parker, J. P. and Scott, A. 1999. Soil and residue management effects on cropping conditions and nitrous oxide fluxes under controlled traffic in Scotland. 2. Nitrous oxide, soil N status and weather. Soil Till. Res. 52: 191– 201. Bateman, E. J. and Baggs, E. M. 2005. Contributions of nitrification and denitrification to N2 O emissions from soils at different water-filled pore space. Biol. Fert. Soils. 41: 379–388. Bessou, C., Mary, B., L´ eonard, J., Roussel, M., Gr´ehan, E. and Gabrielle, B. 2010. Modelling soil compaction impacts on nitrous oxide emissions in arable fields. Eur. J. Soil Sci. 61: 348–363. Blackmer, A. M., Bremner, J. M. and Schmidt, E. L. 1980. Production of nitrous oxide by ammonia-oxidizing chemoautotrophic microorganisms in soil. Appl. Environ. Microb. 40: 1060–1066. Bouwman, A. F. 1996. Direct emission of nitrous oxide from agricultural soils. Nutr. Cycl. Agroecosys. 46: 53–70. Bremner, J. M. 1997. Sources of nitrous oxide in soils. Nutr. Cycl. Agroecosys. 49: 7–16. Chen, D., Li, Y., Grace, P. and Mosier, A. R. 2008. N2 O emissions from agricultural lands: a synthesis of simulation approaches. Plant Soil. 309: 169–189. Centre Interprofessionnel Technique d’Etude de la Pollution Atmosph´erique (CITEPA). 2011. Inventaire des ´emissions de polluants atmosph´eriques en France—s´eries sectorielles et analyses ´etendues (in French). Available online at http: //www.citepa.org/publications/Inventaires.htm#inv1 (verified on April 10, 2012). Clemens, J., Schillinger, M. P., Goldbach, H. and Huwe, B. 1999. Spatial variability of N2 O emissions and soil parameters of an arable silt loam—a field study. Biol. Fert. Soils. 28: 403–406. Clough, T. J., Di, H. J., Cameron, K. C., Sherlock, R. R., Metherell, A. K., Clark, H. and Rys, G. 2007. Accounting for the utilization of a N2 O mitigation tool in the IPCC inventory methodology for agricultural soils. Nutr. Cycl. Agroecosys. 78: 1–14. Conen, F., Dobbie, K. E. and Smith, K. A. 2000. Predicting N2 O emissions from agricultural land through related soil parameters. Glob. Change Biol. 6: 417–426.
432
Conrad, R. 1996. Soil microorganisms as controllers of atmospheric trace gases (H2 , CO, CH4 , OCS, N2 O, and NO). Microbiol. Rev. 60: 609–640. Eichner, M. J. 1990. Nitrous oxide emissions from fertilized soils: summary of available data. J. Environ. Qual. 19: 272–280. FAO. 2001. Global Estimates of Gaseous Emissions of NH3 , NO, N2 O from Agricultural Land. FAO and IFA. Farquharson, R. and Baldock, J. 2008. Concepts in modelling N2 O emissions from land use. Plant Soil. 309: 147–167. Garrido, F., H´ enault, C., Gaillard, H., P´erez, S. and Germon, J. C. 2002. N2 O and NO emissions by agricultural soils with low hydraulic potentials. Soil Biol. Biochem. 34: 559–575. Goossens, A., De Visscher, A., Boeckx, P. and Van Cleemput, O. 2001. Two-year field study on the emission of N2 O from coarse and middle-textured Belgian soils with different land use. Nutr. Cycl. Agroecosys. 60: 23–34. Gregorich, E. G., Rochette, P., VandenBygaart, A. J. and Angers, D. A. 2005. Greenhouse gas contributions of agricultural soils and potential mitigation practices in Eastern Canada. Soil Till. Res. 83: 53–72. Groffman, P. M. and Tiedje, J. M. 1989. Denitrification in north temperate forest soils: relationships between denitrification and environmental factors at the landscape scale. Soil Biol. Biochem. 21: 621–626. Guimbaud, C., Catoire, V., Gogo, S., Robert, C., Chartier, M., Laggoun-D´ efarge, F., Grossel, A., Alb´eric, P., Pomathiod, L., Nicoullaud, B. and Richard, G. 2011. A portable infrared laser spectrometer for flux measurements of trace gases at the geosphere-atmosphere interface. Meas. Sci. Technol. 22: 75601–75617. Hansen, S., Maehlum, J. E. and Bakken, L. R. 1993. N2 O and CH4 fluxes in soil influenced by fertilization and tractor traffic. Soil Biol. Biochem. 25(5): 621–630. H´ enault, C., Ch` neby, D., Heurlier, K., Garrido, F., Perez, S. and Germon, J.-C. 2001. Laboratory kinetics of soil denitrification are useful to discriminate soils with potentially high levels of N2 O emission on the field scale. Agronomie. 21: 713–723. H´ enault, C., Devis, X., Lucas, J. L. and Germon, J. C. 1998a. Influence of different agricultural practices (type of crop, form of N-fertilizer) on soil nitrous oxide emissions. Biol. Fert. Soils. 27: 299–306. H´ enault, C., Devis, X., Page, S., Justes, E., Reau, R. and Germon, J. C. 1998b. Nitrous oxide emission under different soil and land management conditions. Biol. Fert. Soils. 26: 199–207. H´ enault, C., Laville, P., Garrido, F. and Germon, J. C. 1999. Nitrous oxide emissions from cultivated soils in France. In Desjardins, R. L., Keng, J. C. and Haugen-Kozyra, K. (eds.) Reducing Nitrous Oxide Emissions from Agroecosystems. International N2 O Workshop, March 3–5, Banff, Alberta, Canada. pp. 44–50. H´ enault, C., Roger, P., Laville, P., Gabrielle, B. and Cellier, P. 2005. Les ´emissions par les sols des gaz ` a effet de serre CH4 et N2 O. In Girard, M. C. et al. (eds.) Sols et Environnement (in French). Dunod, Paris. pp. 326–344. Hensen, A., Groot, T. T., Van den Bulk, W. C. M., Vermeulen, A. T., Olesen, J. E. and Schelde, K. 2006. Dairy farm CH4 and N2 O emissions, from one square metre to the full farm scale. Agric. Ecosyst. Environ. 112: 146-152. Hergoualc’h, K., Harmand, J.-M., Cannavo, P., Skiba, U., Oliver, R. and H´ enault, C. 2009. The utility of process-based models for simulating N2 O from soils: a case study based on Costa Rican coffee plantations. Soil Biol. Biochem. 41: 2343–2355.
´ C. HENAULT et al.
International Panel on Climate Change (IPCC). 2007. Climate Change 2007—The Physical Science Basis: Working Group I Contribution to the Fourth Assessment Report of the IPCC. Cambridge University Press, Cambridge, UK. Knowles, R. 1982. Denitrification. Microbiol. Rev. 46: 43–70. Konda, R., Ohta, S., Ishizuka, S., Arai, S., Ansori, S., Tanaka, N. and Hardjono, A. 2008. Spatial structures of N2 O, CO2 , and CH4 fluxes from Acacia mangium plantation soils during a relatively dry season in Indonesia. Soil Biol. Biochem. 40: 3021–3030. Laville, P., Lehuger, S., Loubet, B., Chaumartin, F. and Cellier, P. 2011. Effect of management, climate and soil conditions on N2 O and NO emissions from an arable crop rotation using high temporal resolution measurements. Agr. Forest Meteorol. 151: 228–240. Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G. W., Prosser, J. I., Schuster, S. C. and Schleper, C. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 442: 806–809 Linn, D. M. and Doran, J. W. 1984. Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci. Soc. Am. J. 48: 1267– 1272. Martikainen, P. J. and De Boer, W. 1993. Nitrous oxide production and nitrification in acidic soil from a Dutch coniferous forest. Soil Biol. Biochem. 25: 343–347. Mathieu, O., L´ evˆ eque, J., H´ enault, C., Milloux, M. J., Bizouard, F. and Andreux, F. 2006. Emissions and spatial variability of N2 O, N2 and nitrous oxide mole fraction at the field scale, revealed with 15 N isotopic techniques. Soil Biol. Biochem. 38: 941–951. Mosier, A. R., Duxbury, J. M., Freney, J. R., Heinemeyer, O. and Minami, K. 1996. Nitrous oxide emissions from agricultural fields: assessment, measurement and mitigation. Plant Soil. 181: 95–108. Neftel, A., Ammann, C., Fischer, C., Spirig, C., Conen, F., Emmenegger, L., Tuzson, B. and Wahlen, S. 2010. N2 O exchange over managed grassland: Application of a quantum cascade laser spectrometer for micrometeorological flux measurements. Agr. Forest Meteorol. 150: 775–785. Oenema, O. 1999. Strategies for decreasing nitrous oxide emissions from agricultural sources. In Desjardins, R. L., Keng, J. C. and Haugen-Kozyra, K. (eds.) Reducing Nitrous Oxide Emissions from Agroecosystems. International N2 O Workshop, March 3–5, Banff, Alberta, Canada. pp. 175–191. Parkin, T. B. 1987. Soil microsites as a source of denitrification variability. Soil Sci. Soc. Am. J. 51: 1194–1199. Parkin, T. B. 2008. Effect of sampling frequency on estimates of cumulative nitrous oxide emissions. J. Environ. Qual. 37: 1390–1395. Parton, W. J., Mosier, A. R., Ojima, D. S., Valentine, D. W., Schimel, D. S., Weier, K. and Kulmala, A. E. 1996. Generalized model for N2 and N2 O production from nitrification and denitrification. Global Biogeochem. Cy. 10(3): 401– 412. Philippot, L. and Germon, J. C. 2005. Contribution of bacteria to initial input and cycling of nitrogen in soils. In Buscot, E. and Varma, A. (eds.) Microorganisms in Soils: Roles in Genesis and Functions. Springer-Verlag GmbH, Heidelberg, Germany. Ravishankara, A. R., Daniel, J. S. and Portmann, R. W. 2009. Nitrous oxide (N2 O): the dominant ozone-depleting substance emitted in the 21st century. Science. 326: 123–125. Ritchie, G. A. and Nicholas, D. J. D. 1972. Identification of the sources of nitrous oxide produced by oxidative and reduc-
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
tive processes in Nitrosomonas europaea. Biochem. J. 126: 1181–1191. R¨ over, M., Heinemeyer, O., Munch, J. C. and Kaiser, E. A. 1999. Spatial heterogeneity within the plough layer: high variability of N2 O emissions rates. Soil Biol. Biochem. 31: 167–173. Ruser, R., Flessa, H., Schilling, R., Steindl, H. and Beese, F. 1998. Soil compaction and fertilization effects on nitrous oxide and methane fluxes in potato fields. Soil Sci. Soc. Am. J. 62: 1587–1595. Sameshima-Saito, R., Chiba, K., Hirayama, J., Itakura, M., Mitsui, H., Eda, S. and Minamisawa, K. 2006. Symbiotic Bradyrhizobium japonicum reduces N2 O surrounding the soybean root system via nitrous oxide reductase. Appl. Environ. Microb. 72: 2526–2532. Sitaula, B. K., Hansen, S., Sitaula, J. I. B. and Bakken, L. R. 2000. Effects of soil compaction on N2 O emission in agricultural soil. Chemosphere-Glob. Change Sci. 2: 367–371. Six, J., Ogle, S. M., Breidt, F. J., Conant, R. T., Mosier, A. R. and Paustian, K. 2004. The potential to mitigate global warming with no-tillage management is only realized when practised in the long term. Glob. Change Biol. 10: 155– 160. Smith, K. A. and Dobbie, K. E. 2001. The impact of sampling frequency and sampling times on chamber-based measurements of N2 O emissions from fertilized soils. Glob. Change. Biol. 7: 933–945. Stehfest, E. and Bouwman, A. F. 2006. N2 O and NO emission from agricultural fields and soils under natural vegetation: summarizing available measurement data and modelling of global annual emissions. Nutr. Cycl. Agroecosys. 74: 207– 288.
433
Syakila, A. and Kroeze, C. 2011. The global nitrous oxide budget revisited. Greenhouse Gas Meas. Manage. 1: 17–26. Teepe, R., Brumme, R., Beese, F. and Ludwig, B. 2004. Nitrous oxide emission and methane consumption following compaction of forest soils. Soil Sci. Soc. Am. J. 68: 605– 611. Tiedje, J. M. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In Zehnder, A. (ed) Biology on Anaerobic Microorganisms. John Wiley & Sons, New York. pp. 179–244. van den Heuvel, R. N., Hefting, M. M., Tan, N. C. G., Jetten, M. S. M. and Verhoeven, J. T. A., 2009. N2 O emission hotspots at different spatial scales and governing factors for small scale hotspots. Sci. Total Environ. 407: 2325–2332. Vermeulen, G. D. and Mosquera, J. 2009. Soil, crop and emission responses to seasonal-controlled traffic in organic vegetable farming on loam soil. Soil Till. Res. 102(1): 126–134. Vieten, B., Conen, F., Seth, B. and Alewell, C. 2008. The fate of N2 O consumed in soils. Biogeosciences. 5: 129–132. Yamulki, S. and Jarvis, S. C. 2002. Short-term effects of tillage and compaction on nitrous oxide, nitric oxide, nitrogen dioxide, methane and carbon dioxide fluxes from grassland. Biol. Fert. Soils. 36: 224–231. Yanai, J., Sawamoto, T., Oe, T., Kusa, K., Yamakawa, K., Sakamoto, K., Naganawa, T., Inubushi, K., Hatano, R. and Kosaki, T. 2003. Spatial variability of nitrous oxide emissions and their soil-related determining factors in an agricultural field. J. Environ. Qual. 32: 1965–1977. Yates, T. T., Si, B. C., Farrell, R. E. and Pennock, D. J. 2006. Probability distribution and spatial dependence of nitrous oxide emission: temporal change in hummocky terrain. Soil Sci. Soc. Am. J. 70: 753–762.
Nitrous Oxide Emission by Agricultural Soils: A Review of Spatial and Temporal Variability for Mitigation∗1 1,2,∗2 3 ´ ´ C. HENAULT , A. GROSSEL1 , B. MARY3 , M. ROUSSEL3 and J. LEONARD 1 INRA,
UR 272 Science du Sol, Centre de Recherches d’Orl´ eans, CS 40001 Ardon, 45075 Orl´ eans cedex 2 (France) de Bourgogne, UMR 1229 Microbiologie du sol et de l’Environnement, 17 rue Sully, BP 86510, 21065 Dijon cedex
2 INRA-Universit´ e
(France) 3 INRA, US 1158 Agro-Impact, Pˆ ole du Griffon, 180 rue Pierre-Gilles de Gennes, 02000 Barenton-Bugny (France) (Received February 4, 2012; revised May 2, 2012)
ABSTRACT This short review deals with soils as an important source of the greenhouse gas N2 O. The production and consumption of N2 O in soils mainly involve biotic processes: the anaerobic process of denitrification and the aerobic process of nitrification. The factors that significantly influence agricultural N2 O emissions mainly concern the agricultural practices (N application rate, crop type, fertilizer type) and soil conditions (soil moisture, soil organic C content, soil pH and texture). Large variability of N 2 O fluxes is known to occur both at different spatial and temporal scales. Currently new techniques could help to improve the capture of the spatial variability. Continuous measurement systems with automatic chambers could also help to capture temporal variability and consequently to improve quantification of N2 O emissions by soils. Some attempts for mitigating soil N2 O emissions, either by modifying agricultural practices or by managing soil microbial functioning taking into account the origin of the soil N2 O emission variability, are reviewed. Key Words:
agricultural practices, fertilization, greenhouse gas, N2 O fluxes, soil-atmosphere interface
Citation: H´ enault, C., Grossel, A., Mary, B., Roussel, M. and L´eonard, J. 2012. Nitrous oxide emission by agricultural soils: A review of spatial and temporal variability for mitigation. Pedosphere. 22(4): 426–433.
INTRODUCTION On the issue of global warming and its causes, the Working Group I Summary for Policymakers of the Intergovernmental Panel on Climate Change (IPCC) recently stated that 1) “warming of the climate system is unequivocal”, and 2) “most of the observed increase in globally averaged temperatures since the mid-20th century is very likely (the assessed likelihood, using expert judgment, are over 90%) due to the observed increase in anthropogenic greenhouse gas concentrations” (IPCC, 2007). The three long-lived greenhouse gases carbon dioxide, methane and nitrous oxide have indeed increased markedly as a result of human activities since 1750 and now far exceed pre-industrial values. The concentration in nitrous oxide, which has a very high radiative forcing per unit mass or molecule (296 times higher than the one of CO2 on a 100 years period), have risen from a pre-industrial value of 270 ppb to a 2005 value of 319 ppb, mainly due to human activities, primarily through agriculture and the increase in use of industrial fertilizers. Beyond its ∗1 Supported
greenhouse effect, N2 O is now also the major ozonedepleting substance in the stratosphere (Ravishankara et al., 2009). Agricultural soils are assessed to produce 2.8 (1.7–4.8) Tg N2 O-N year−1 and thus appear as the main anthropogenic source of this gas (IPCC, 2007). Amongst the greenhouse gases, nitrous oxide is estimated to contribute to 8% of the radiative forcing at the global scale while amongst the human activities, agriculture is estimated to contribute to 14% of the radiative forcing. At the national scale, in France, recent estimations indicated that agriculture contributes to 21% of the radiative forcing and to 84% of the anthropogenic N2 O emission (CITEPA, 2011). It is thus a key issue to be able to understand how N2 O emissions by agricultural soils occur and to derive mitigation strategies from this knowledge. BACKGROUND ON PROCESSES AND EFFECTS OF AGRICULTURAL PRACTICES ON N2 O FLUXES Soils can act both as a source and a sink of
by the Region Centre, the Fonds Europ´een de D´ eveloppement R´ egional and the INRA, France, through the SpatioFlux Program. ∗2 Corresponding author. E-mail: [email protected].
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
N2 O (Syakila and Kroeze, 2011). However on the global scale, the source activity largely dominates the sink one. The production and consumption of N2 O in soils mainly involve biotic processes. Nevertheless, small amounts of N2 O may be produced through nonbiological processes, i.e., the chemical decomposition of nitrite (or chemodenitrification) and the chemical decomposition of hydroxylamine (Bremner, 1997). As far as biological processes are concerned, numerous groups of microorganisms contribute to the production and consumption of N2 O (Conrad, 1996), but biological nitrification and denitrification are considered as the dominant processes involved (Fig. 1). Only denitrification is recognized as a significant biological consumptive fate for N2 O (Vieten et al., 2008). The nitrification process, classically observed in aerobic conditions, is the successive biological oxidation of ammonium to nitrite and nitrate. It is well known that the nitrification process can be performed by some autotrophic bacteria. For example, Nitrosomonas oxidize ammonium to nitrite and Nitrobacter oxidize nitrite to nitrate (Bremner, 1997). Evidence of the contribution of Crenarchaea in ammonia oxidation in soil ecosystems has recently been reported (Leininger et al., 2006). Beyond nitrite and nitrate, the nitrification process can also lead to the release of greenhouse gases N2 O as demonstrated by laboratory studies on pure cultures (Blackmer et al., 1980) or on soil samples (Garrido et al., 2002). Mechanisms leading to the release of N2 O during nitrification are not clearly understood. Some authors proposed that N2 O is formed during the oxidation of ammonium while the mechanisms of nitrification/denitrification, i.e., the production of N2 O from NO− 2 produced through nitrification, is more and more mentioned in the literature. Under oxygen limited conditions, nitrifiers could use NO− 2 as a terminal electron acceptor (Ritchie and Nicholas, 1972; Bremner, 1997). Denitrification refers to the dissimilatory reduction, by essentially aerobic bacteria placed in anaerobic conditions, of one or both of the ionic
Fig. 1
427 − nitrogen oxides (nitrate, NO− 3 , and nitrite, NO2 ) to the gaseous oxides (nitric oxide, NO and nitrous oxide, N2 O), which may themselves be further reduced to dinitrogen (N2 ). During denitrification, the nitrogen oxides act as terminal electron acceptors in the absence of oxygen (Knowles, 1982). Denitrification capacity is present in many prokaryotic families, including phototrophs, lithotrophs and organotrophs like the species of Pseudomonas or Alcaligenes. The first step of the denitrification process, i.e., the utilization of nitrate as an electron acceptor, is widespread in the environment and could be carried out by a large proportion of soil microorganisms. In contrast, organisms able to reduce nitrite into N2 O or N2 would represent only 0.1% to 5% of the soil bacteria (Philippot and Germon, 2005). Driving denitrification to its term (N2 , inert form of nitrogen) is of great environmental interest because it results in the elimination, without transfer of pollution, of the soluble forms of nitrogen (NO− 3, ) that may i) interfere with public health through NO− 2 high concentrations in drinking water and food and ii) contribute to the eutrophication through elevated concentrations in surface water. However, when the reduction step of denitrification is slowed down, NOx , and N2 O are released into the atmosphere and are involved in the atmospheric pollution. As a result of the usual coexistence of aerobic and anaerobic zones in soils (Arah, 1990), nitrification and denitrification can occur simultaneously, and the contribution of each process varies with soil water content (Bateman and Baggs, 2005). Recently, Stehfest and Bouwman (2006) summarized information from 1 008 published N2 O emissions for agricultural fields. The meta-analysis they performed indicates that the factors that significantly influence agricultural N2 O emissions deal with agricultural practices (N application rate, crop type, fertilizer type) and soil conditions (soil organic C content, soil pH and texture). At the global scale, Bouwman (1996) as well as Stehfest and Bouwman (2006) observed a
Main processes involved in N2 O budget. Adapted from H´enault et al. (2005).
´ C. HENAULT et al.
428
linear relationship between N2 O emission and N application rate. This relationship allows to calculate a fertilizer-induced emission (FIE) indicator which is often used to estimate anthropogenic N2 O emission from fertilizer, animal manure and other N inputs (IPCC, 2007). This FIE is estimated to 0.91% (with a large uncertainty) which means that globally 0.91% of the N applied on soil is directly lost as N2 O. The influence of crop type is mainly visible for flooded rice systems, which could produce rather low fluxes of N2 O due to more complete denitrification (FAO, 2001) and, to a lesser extent, cereals and grass which have lower emissions compared to legumes. Concerning fertilizer types, Stehfest and Bouwman (2006) observed higher emissions for the calcium ammonium nitrate form and lower emissions for the ammonium phosphate form, and Eichner (1990) observed higher emissions for anhydrous ammonia fertilizers. Contradictory results have often been observed about the effect of soil tillage, despite a general trend of greater emissions in no till (or low till) systems. However, the difference observed between tillage modalities for short-term studies seems to disappear when long-term field trials, with a long history of differentiation, are considered (Six et al., 2004). The difficulty to draw solid conclusions about the effect of agricultural practices, beyond the effect of nitrogen inputs, is for a large part due to the interaction with factors related to soil conditions. The large effect of soil water content on N2 O emissions, especially through denitrification, has also been underlined by numerous authors (Conen et al., 2000; Farquharson and Baldock, 2008). Stehfest and Bouwman (2006) also found soil organic C content, soil pH and soil texture to have a significant influence on N2 O emis-
sions. Emissions were observed to increase with soil organic C content, which reflects the positive correlation between soil organic C content and the rates of denitrification and nitrification (Tiedje, 1988). Lowest emissions were observed for pH values > 7.3. The N2 O emissions from acidic soils generally exceed those from alkaline soils and probably reflect the reported higher N2 O emission from nitrification (Martikainen and De Boer, 1993) or higher N2 O:N2 ratio (Alexander, 1977) at low pH compared to high pH. Emissions are also generally higher for fine-textured soil than for coarse- and medium-textured soils, because of the more frequent occurrence of anaerobic conditions associated with higher water contents (Parton et al., 1996; FAO, 2001). PATTERNS OF N2 O EMISSIONS BY AGRICULTURAL SOILS AND PERSPECTIVES FOR IMPROVING THE CAPTURE OF VARIABILITY Most approaches for measuring N2 O emissions in field conditions fall into two main categories: chamber and micrometeorological techniques, whose benefits and limits are presented in Table I. Using the database compiled by Stehfest and Bouwman (2006) and available at http://www.mnp.nl/images/stehfest data tcm61-29733.xls, daily N2 O fluxes appeared to be comprised between −2 (Goossens et al., 2001) and 5 400 g N ha−1 d−1 (Abbasi and Adams, 2000), both values being obtained under temperate climate. The variability of N2 O fluxes is known to occur both at different spatial and temporal scales. Specific studies have shown a very high spatial variability of N2 O emissions at different scales, from the
TABLE I Complementarities of chambers and micrometeorological methods for measuring greenhouse gas emissions at the soil-atmosphere interfacea)
Equipment constraints Cost of installation Technical level required Human labor charge Use constraints Methodological bias
Performances Limit of detection Representativity Use a) Adapted
Chambers
Micrometeorology
About 50 000 Euros Basic Very important Could be used anywhere Disturbance of microclimate in chambers Change in gas concentration in chambers Exploring of a small spatial and temporal proportion of systems
About 200 000 Euros Very high Important Could only be used on large and flat surfaces Make sure to take into account the conditions of atmospheric stability and wind circulation to consider fairly the different emission sources and provide the correct values of flux
< 1 g N ha−1 d−1 Punctual measures in time and space Comparison of agricultural practices
Few g N ha−1 d−1 Integrative measures in time and space Estimation of gas fluxes in situations representative of ecosystems
from H´enault et al. (2005).
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
microscale one to the regional one (Parkin, 1987; Groffman and Tiedje, 1989) with coefficients of variations ranging between 50% and 200% (Ambus and Christensen, 1994; Yanai et al., 2003; Mathieu et al., 2006; Konda et al., 2008). van den Heuvel et al. (2009) compared N2 O fluxes at scales ranging from 0.000 13 to 0.31 m2 and found that “spatial variation was highest at the smallest scale”. At the fine scale < 1 m2 , this variability was observed to be linked to the presence of denitrifying microsites in soils (Parkin, 1987; Ambus and Christensen, 1994; Clemens et al., 1999). R¨over et al. (1999) and Yates et al. (2006) established variograms of N2 O emission and observed that the nugget effect was very important compared to the sill, indicating that most of the variability occurred at short distance (< 10 m). At distances beyond a few meters, the spatial variability can be linked to the mineral nitrogen availability or to topographic or micro-topographic effects. Local depressions at the soil surface can maintain soil moisture and lead to large N2 O emissions (Ball et al., 1997). The variability at the plot scale is often due to the presence of some very high fluxes on “hot spots”, which account for a significant part of the whole flux. For example, van den Heuvel et al. (2009) observed, during two campaigns in a riparian buffer zone, that 1% and 4% of the sampled surface were, respectively, responsible for 17% and 33% of the whole N2 O emissions during the measurement period. The presence of hot spots which emit at rates several orders of magnitude above the background N2 O fluxes was also reported in cultivated fields (e.g., Ball et al., 1997). Mathieu et al., 2006 (Fig. 2) studied 36 soil samples on a 20 m × 20 m cultivated field plot. They observed a high spatial variability without any spatial dependence at the scale of the experimental plot. Only a tenuous relationship was observed between N2 O emission and nitrate concentration amongst different soil properties. Spatial patterns of N2 O emissions are also very variable in time (Yates et al., 2006). Currently new techniques could help for improving the capture of the spatial variability. The development of fast analysers based on infrared spectrometry with quantum cascade laser (Neftel et al., 2010; Guimbaud et al., 2011) will allow to re-investigate the spatial variability either by increasing the number of replicates when coupled with simplified chambers like fast box (Hensen et al., 2006), or by covering larger area when used in association with micro-meteorological methods which integrates the spatial variability over large surfaces. These analysers also provide a very high sensitivity for gas analysis, which will be helpful for studying low fluxes and N2 O uptake by soils.
429
Fig. 2 Spatial distribution of N2 O fluxes on a 20 m × 20 m cultivated field plot. Adapted from Mathieu et al. (2006).
In a previous work, we studied the spatial variability of N2 O emissions at the regional scale, by analysing the respective effects of agronomic (type of crop, dose and nature of fertilizers), climatic and pedologic conditions, including 3 different soil types: a rendzina on a cryoturbed material, a hydromorphic leached brown soil and a superficial soil on a calcareous plateau (H´enault et al., 1998a, b, 1999). We observed a very marked effect of soil type on N2 O emissions. Two main factors, i.e., soil hydrology and the ability of the soil to reduce N2 O, appeared to play an essential role on this variability. In particular, the hydromorphic leached brown soil showed the highest emissions, 3 500 g N ha−1 over a 5 month period. This behaviour could be explained by a low drainage capacity and consequently high water filled pore space (Linn and Doran, 1984) associated with a very low N2 O reductase activity, i.e., a high N2 O:N2 ratio of the gas emitted during the denitrification process. We then developed a simple laboratory methodology to characterize soil N2 O reduction capacity. This approach, which can be used routinely, proved to be useful to discriminate soils with potentially high levels of N2 O emission at the field scale (H´enault et al., 2001; Hergoualc’h et al., 2009). A high temporal variability of soil N2 O fluxes is also observed at different scales (hours, days, seasons, years), which is expected since N2 O fluxes respond to climatic and agronomic events (Laville et al., 2011). Despite this temporal variability, measurements are most discontinuous in time (weekly to monthly measurements) and often realized over short periods. The discontinuous nature of the measurement strongly impacts the estimation of cumulative emissions (Smith and Dobbie, 2001; Parkin, 2008), and it was shown
430
that the uncertainty on cumulative emissions rose very quickly when the sampling interval changed from 4 to 10 days. With a sampling interval of 10 days, estimated cumulative emissions can fluctuate within a 50% interval around the expected value. Measurements restricted to periods extending over only a few months raise the problem of the representativity of the chosen period, given that the difference between N2 O emissions associated with different treatments such as tillage modalities can largely change during a crop rotation (unpublished results). Gregorich et al. (2005) also suggested that annual N2 O emissions based on growing-season measurements in Canada could be underestimated due to the concentrated N2 O emissions during freeze/thaw periods in winter and spring. Continuous measurement systems with automatic chambers can help to override these limitations, and have in addition some other positive consequences. For example, as chambers remain in place for long durations, it is possible to use chambers covering larger areas because they do not need to be moved frequently. So far, Bessou et al. (2010) proposed to use large chambers to integrate the heterogeneity of fluxes at a fine scale as they obtained systematically rather low coefficient of variation between replicate measurements (always less than 30%) with a sampling area of 0.5 m2 . Moreover, as concentration is measured frequently during chamber closure, the form of the N2 O accumulation kinetics is generally well apparent, and non-linear models can be used if necessary to better estimate the N2 O flux. Fig. 3 compares N2 O estimations obtained with respectively a linear and an exponential model. The inappropriate use of a linear model, i.e., when the
Fig. 3 Cumulative N2 O emissions estimated using either linear or exponential model during a whole sugarbeet growth cycle, in two years (2007 and 2008) and two soils (compacted and uncompacted). The data are from Bessou et al. (2010).
´ C. HENAULT et al.
the decrease in the concentration gradient between the soil and the atmosphere is progressive, results in a systematic underestimation of fluxes of about 35% with the linear model. Moreover, a generalization of continuous measurements allows detecting some quite unpredictable fluxes of N2 O. For example, Bessou et al. (2010) were able to measure significant N2 O fluxes during summer in sugarbeet fields in spite of dry conditions and low water contents in soil. However, economic or power supply constraints may prevent using continuous measurement systems. In these situations manual chambers remain the only accessible technique and the sampling frequency should be optimized. It has often been suggested that postfertilization periods, which generally exhibit high N2 O fluxes especially when they coincide with important rainfall, may require more frequent measurements (two per week during 3 weeks for example). However each situation is very specific, and numerical experiments have shown that increasing the sampling frequency during the post-fertilization period does not systematically improve N2 O emissions estimation. The use of N2 O emission models (Chen et al., 2008) may be a possible strategy for optimizing the sampling frequency and has to be tested. DEVELOPMENT OF MITIGATION STRATEGIES Oenema (1999) suggested that there are basically two strategies to decrease N2 O emissions from agriculture: 1) increasing the N use efficiency concomitantly to the lowering of the total N input, and 2) decreasing the release of N2 O per unit of nitrogen from nitrification and denitrification processes. Field tests have shown that nitrification inhibitors can limit N2 O from the application of ammonium-based fertilizers (Clough et al., 2007). Mosier et al. (1996) also proposed to adapt the nature of the fertilizer to the expected dominant process. For example, if nitrification is supposed to be the main contributor to N2 O fluxes, using a nitrate based fertilizer rather than an ammonium based one should limit N2 O production. Nevertheless, this methodology has not yet been tested in realistic conditions. The use of control traffic farming to mitigate N2 O emissions by minimizing the compacted soil area was also investigated in few studies. For example, Vermeulen and Mosquera (2009) obtained a 20% to 50% N2 O emission reduction with seasonally controlled traffic farming. This result is consistent with the known effect of compaction on the intensity of N2 O emissions: increasing by 20% to 50% on average (Hansen et al. 1993; Ruser et al. 1998; Ball et al., 1999; Sitaula et al., 2000; Yamulki and Jarvis, 2002;
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
Teepe et al., 2004). Temporal and spatial hotspots of N2 O fluxes represent a large part of the total emissions. Some targeted intervention on these hotspots could be of great interest for mitigating N2 O emissions, but this requires to identify the location in space and time of these hotspots as well as to understand their origin (soil conditions, agricultural practices). For example, important N2 O fluxes could be observed in specific situations, typically due to a poor capacity of soils to reduce N2 O into N2 . In these situations some innovating methodologies need to be proposed for increasing soils’ capacities to reduce N2 O. Sameshima-Saito et al. (2006) demonstrated that soybean roots nodulated with Bradyrhizobium japonicum USDA110, carrying the nosZ-gene, were able to reduce N2 O even at low concentration (Sameshima-Saito et al., 2006), suggesting that such soybean nodules could scavenge N2 O in soil and thereby lessen N2 O emission from soybean fields to the atmosphere. This could be a promising perspective for the mitigation of N2 O emission, especially in soils that are basically inefficient in reducing N2 O into N2 . CONCLUSIONS Large spatial and temporal variability of N2 O emissions by agricultural soils at different scales make it difficult to measure and predict the fluxes. Rough estimations can be obtained from total nitrogen inputs using the IPCC fertilizer-induced emission indicator but the development and evaluation of mitigation strategies imply a deeper understanding of the determinism of these emissions. Recent advances concerning the measurement of emissions and the development of indicators of soil N2 O emission potential will probably be of great help to improve and apply our knowledge. The development and generalization of continuous emission measurements will help to improve the estimation of fluxes and the integration over long periods such as a complete rotation. It will also allow to focus on processes often neglected because of their fleetingness, such as N2 O uptake by soils or N2 O peaks distant from fertilization events. Some analytical improvements for determining N2 O concentration in the atmosphere are also emerging. This will enable a best characterisation of the spatial variability of N2 O fluxes at different scales. Easily measurable indicators of soil N2 O emission potential will also help to detect situations that can potentially emit large level of N2 O. At the end, the spatial variability of N2 O emission, which makes it difficult to quantify the N2 O fluxes, may turn
431
to an opportunity for mitigation if we are able to understand it. REFERENCES Abbasi, M. K. and Adams, W. A. 2000. Gaseous N emissions during simultaneous nitrification-denitrification associated with mineral N fertilization to a grassland soil under field conditions. Soil Biol. Biochem. 32: 1251–1259. Alexander, M. 1977. Introduction to Soil Microbiology. 2nd Edition. John Wiley & Sons, New York. Ambus, P. and Christensen, S. 1994. Measurement of N2 O emission from a fertilized grassland: an analysis of spatial variability. J. Geophysic. Res. 99: 16549–16555. Arah, J. R. M. 1990. Diffusion-reaction models of denitrification in soil microsites. In Revsebech, N. P. and Sørensen, J. (eds.) Denitrification in Soil and Sediment. Plenum Press, New York. pp. 245–258. Ball, B. C., Horgan, G. W., Clayton, H. and Parker, J. P. 1997. Spatial variability of nitrous oxide fluxes and controlling soil and topographic factors. J. Environ. Qual. 26: 1399–1409. Ball, B. C., Parker, J. P. and Scott, A. 1999. Soil and residue management effects on cropping conditions and nitrous oxide fluxes under controlled traffic in Scotland. 2. Nitrous oxide, soil N status and weather. Soil Till. Res. 52: 191– 201. Bateman, E. J. and Baggs, E. M. 2005. Contributions of nitrification and denitrification to N2 O emissions from soils at different water-filled pore space. Biol. Fert. Soils. 41: 379–388. Bessou, C., Mary, B., L´ eonard, J., Roussel, M., Gr´ehan, E. and Gabrielle, B. 2010. Modelling soil compaction impacts on nitrous oxide emissions in arable fields. Eur. J. Soil Sci. 61: 348–363. Blackmer, A. M., Bremner, J. M. and Schmidt, E. L. 1980. Production of nitrous oxide by ammonia-oxidizing chemoautotrophic microorganisms in soil. Appl. Environ. Microb. 40: 1060–1066. Bouwman, A. F. 1996. Direct emission of nitrous oxide from agricultural soils. Nutr. Cycl. Agroecosys. 46: 53–70. Bremner, J. M. 1997. Sources of nitrous oxide in soils. Nutr. Cycl. Agroecosys. 49: 7–16. Chen, D., Li, Y., Grace, P. and Mosier, A. R. 2008. N2 O emissions from agricultural lands: a synthesis of simulation approaches. Plant Soil. 309: 169–189. Centre Interprofessionnel Technique d’Etude de la Pollution Atmosph´erique (CITEPA). 2011. Inventaire des ´emissions de polluants atmosph´eriques en France—s´eries sectorielles et analyses ´etendues (in French). Available online at http: //www.citepa.org/publications/Inventaires.htm#inv1 (verified on April 10, 2012). Clemens, J., Schillinger, M. P., Goldbach, H. and Huwe, B. 1999. Spatial variability of N2 O emissions and soil parameters of an arable silt loam—a field study. Biol. Fert. Soils. 28: 403–406. Clough, T. J., Di, H. J., Cameron, K. C., Sherlock, R. R., Metherell, A. K., Clark, H. and Rys, G. 2007. Accounting for the utilization of a N2 O mitigation tool in the IPCC inventory methodology for agricultural soils. Nutr. Cycl. Agroecosys. 78: 1–14. Conen, F., Dobbie, K. E. and Smith, K. A. 2000. Predicting N2 O emissions from agricultural land through related soil parameters. Glob. Change Biol. 6: 417–426.
432
Conrad, R. 1996. Soil microorganisms as controllers of atmospheric trace gases (H2 , CO, CH4 , OCS, N2 O, and NO). Microbiol. Rev. 60: 609–640. Eichner, M. J. 1990. Nitrous oxide emissions from fertilized soils: summary of available data. J. Environ. Qual. 19: 272–280. FAO. 2001. Global Estimates of Gaseous Emissions of NH3 , NO, N2 O from Agricultural Land. FAO and IFA. Farquharson, R. and Baldock, J. 2008. Concepts in modelling N2 O emissions from land use. Plant Soil. 309: 147–167. Garrido, F., H´ enault, C., Gaillard, H., P´erez, S. and Germon, J. C. 2002. N2 O and NO emissions by agricultural soils with low hydraulic potentials. Soil Biol. Biochem. 34: 559–575. Goossens, A., De Visscher, A., Boeckx, P. and Van Cleemput, O. 2001. Two-year field study on the emission of N2 O from coarse and middle-textured Belgian soils with different land use. Nutr. Cycl. Agroecosys. 60: 23–34. Gregorich, E. G., Rochette, P., VandenBygaart, A. J. and Angers, D. A. 2005. Greenhouse gas contributions of agricultural soils and potential mitigation practices in Eastern Canada. Soil Till. Res. 83: 53–72. Groffman, P. M. and Tiedje, J. M. 1989. Denitrification in north temperate forest soils: relationships between denitrification and environmental factors at the landscape scale. Soil Biol. Biochem. 21: 621–626. Guimbaud, C., Catoire, V., Gogo, S., Robert, C., Chartier, M., Laggoun-D´ efarge, F., Grossel, A., Alb´eric, P., Pomathiod, L., Nicoullaud, B. and Richard, G. 2011. A portable infrared laser spectrometer for flux measurements of trace gases at the geosphere-atmosphere interface. Meas. Sci. Technol. 22: 75601–75617. Hansen, S., Maehlum, J. E. and Bakken, L. R. 1993. N2 O and CH4 fluxes in soil influenced by fertilization and tractor traffic. Soil Biol. Biochem. 25(5): 621–630. H´ enault, C., Ch` neby, D., Heurlier, K., Garrido, F., Perez, S. and Germon, J.-C. 2001. Laboratory kinetics of soil denitrification are useful to discriminate soils with potentially high levels of N2 O emission on the field scale. Agronomie. 21: 713–723. H´ enault, C., Devis, X., Lucas, J. L. and Germon, J. C. 1998a. Influence of different agricultural practices (type of crop, form of N-fertilizer) on soil nitrous oxide emissions. Biol. Fert. Soils. 27: 299–306. H´ enault, C., Devis, X., Page, S., Justes, E., Reau, R. and Germon, J. C. 1998b. Nitrous oxide emission under different soil and land management conditions. Biol. Fert. Soils. 26: 199–207. H´ enault, C., Laville, P., Garrido, F. and Germon, J. C. 1999. Nitrous oxide emissions from cultivated soils in France. In Desjardins, R. L., Keng, J. C. and Haugen-Kozyra, K. (eds.) Reducing Nitrous Oxide Emissions from Agroecosystems. International N2 O Workshop, March 3–5, Banff, Alberta, Canada. pp. 44–50. H´ enault, C., Roger, P., Laville, P., Gabrielle, B. and Cellier, P. 2005. Les ´emissions par les sols des gaz ` a effet de serre CH4 et N2 O. In Girard, M. C. et al. (eds.) Sols et Environnement (in French). Dunod, Paris. pp. 326–344. Hensen, A., Groot, T. T., Van den Bulk, W. C. M., Vermeulen, A. T., Olesen, J. E. and Schelde, K. 2006. Dairy farm CH4 and N2 O emissions, from one square metre to the full farm scale. Agric. Ecosyst. Environ. 112: 146-152. Hergoualc’h, K., Harmand, J.-M., Cannavo, P., Skiba, U., Oliver, R. and H´ enault, C. 2009. The utility of process-based models for simulating N2 O from soils: a case study based on Costa Rican coffee plantations. Soil Biol. Biochem. 41: 2343–2355.
´ C. HENAULT et al.
International Panel on Climate Change (IPCC). 2007. Climate Change 2007—The Physical Science Basis: Working Group I Contribution to the Fourth Assessment Report of the IPCC. Cambridge University Press, Cambridge, UK. Knowles, R. 1982. Denitrification. Microbiol. Rev. 46: 43–70. Konda, R., Ohta, S., Ishizuka, S., Arai, S., Ansori, S., Tanaka, N. and Hardjono, A. 2008. Spatial structures of N2 O, CO2 , and CH4 fluxes from Acacia mangium plantation soils during a relatively dry season in Indonesia. Soil Biol. Biochem. 40: 3021–3030. Laville, P., Lehuger, S., Loubet, B., Chaumartin, F. and Cellier, P. 2011. Effect of management, climate and soil conditions on N2 O and NO emissions from an arable crop rotation using high temporal resolution measurements. Agr. Forest Meteorol. 151: 228–240. Leininger, S., Urich, T., Schloter, M., Schwark, L., Qi, J., Nicol, G. W., Prosser, J. I., Schuster, S. C. and Schleper, C. 2006. Archaea predominate among ammonia-oxidizing prokaryotes in soils. Nature. 442: 806–809 Linn, D. M. and Doran, J. W. 1984. Effect of water-filled pore space on carbon dioxide and nitrous oxide production in tilled and nontilled soils. Soil Sci. Soc. Am. J. 48: 1267– 1272. Martikainen, P. J. and De Boer, W. 1993. Nitrous oxide production and nitrification in acidic soil from a Dutch coniferous forest. Soil Biol. Biochem. 25: 343–347. Mathieu, O., L´ evˆ eque, J., H´ enault, C., Milloux, M. J., Bizouard, F. and Andreux, F. 2006. Emissions and spatial variability of N2 O, N2 and nitrous oxide mole fraction at the field scale, revealed with 15 N isotopic techniques. Soil Biol. Biochem. 38: 941–951. Mosier, A. R., Duxbury, J. M., Freney, J. R., Heinemeyer, O. and Minami, K. 1996. Nitrous oxide emissions from agricultural fields: assessment, measurement and mitigation. Plant Soil. 181: 95–108. Neftel, A., Ammann, C., Fischer, C., Spirig, C., Conen, F., Emmenegger, L., Tuzson, B. and Wahlen, S. 2010. N2 O exchange over managed grassland: Application of a quantum cascade laser spectrometer for micrometeorological flux measurements. Agr. Forest Meteorol. 150: 775–785. Oenema, O. 1999. Strategies for decreasing nitrous oxide emissions from agricultural sources. In Desjardins, R. L., Keng, J. C. and Haugen-Kozyra, K. (eds.) Reducing Nitrous Oxide Emissions from Agroecosystems. International N2 O Workshop, March 3–5, Banff, Alberta, Canada. pp. 175–191. Parkin, T. B. 1987. Soil microsites as a source of denitrification variability. Soil Sci. Soc. Am. J. 51: 1194–1199. Parkin, T. B. 2008. Effect of sampling frequency on estimates of cumulative nitrous oxide emissions. J. Environ. Qual. 37: 1390–1395. Parton, W. J., Mosier, A. R., Ojima, D. S., Valentine, D. W., Schimel, D. S., Weier, K. and Kulmala, A. E. 1996. Generalized model for N2 and N2 O production from nitrification and denitrification. Global Biogeochem. Cy. 10(3): 401– 412. Philippot, L. and Germon, J. C. 2005. Contribution of bacteria to initial input and cycling of nitrogen in soils. In Buscot, E. and Varma, A. (eds.) Microorganisms in Soils: Roles in Genesis and Functions. Springer-Verlag GmbH, Heidelberg, Germany. Ravishankara, A. R., Daniel, J. S. and Portmann, R. W. 2009. Nitrous oxide (N2 O): the dominant ozone-depleting substance emitted in the 21st century. Science. 326: 123–125. Ritchie, G. A. and Nicholas, D. J. D. 1972. Identification of the sources of nitrous oxide produced by oxidative and reduc-
NITROUS OXIDE EMISSION BY AGRICULTURAL SOILS
tive processes in Nitrosomonas europaea. Biochem. J. 126: 1181–1191. R¨ over, M., Heinemeyer, O., Munch, J. C. and Kaiser, E. A. 1999. Spatial heterogeneity within the plough layer: high variability of N2 O emissions rates. Soil Biol. Biochem. 31: 167–173. Ruser, R., Flessa, H., Schilling, R., Steindl, H. and Beese, F. 1998. Soil compaction and fertilization effects on nitrous oxide and methane fluxes in potato fields. Soil Sci. Soc. Am. J. 62: 1587–1595. Sameshima-Saito, R., Chiba, K., Hirayama, J., Itakura, M., Mitsui, H., Eda, S. and Minamisawa, K. 2006. Symbiotic Bradyrhizobium japonicum reduces N2 O surrounding the soybean root system via nitrous oxide reductase. Appl. Environ. Microb. 72: 2526–2532. Sitaula, B. K., Hansen, S., Sitaula, J. I. B. and Bakken, L. R. 2000. Effects of soil compaction on N2 O emission in agricultural soil. Chemosphere-Glob. Change Sci. 2: 367–371. Six, J., Ogle, S. M., Breidt, F. J., Conant, R. T., Mosier, A. R. and Paustian, K. 2004. The potential to mitigate global warming with no-tillage management is only realized when practised in the long term. Glob. Change Biol. 10: 155– 160. Smith, K. A. and Dobbie, K. E. 2001. The impact of sampling frequency and sampling times on chamber-based measurements of N2 O emissions from fertilized soils. Glob. Change. Biol. 7: 933–945. Stehfest, E. and Bouwman, A. F. 2006. N2 O and NO emission from agricultural fields and soils under natural vegetation: summarizing available measurement data and modelling of global annual emissions. Nutr. Cycl. Agroecosys. 74: 207– 288.
433
Syakila, A. and Kroeze, C. 2011. The global nitrous oxide budget revisited. Greenhouse Gas Meas. Manage. 1: 17–26. Teepe, R., Brumme, R., Beese, F. and Ludwig, B. 2004. Nitrous oxide emission and methane consumption following compaction of forest soils. Soil Sci. Soc. Am. J. 68: 605– 611. Tiedje, J. M. 1988. Ecology of denitrification and dissimilatory nitrate reduction to ammonium. In Zehnder, A. (ed) Biology on Anaerobic Microorganisms. John Wiley & Sons, New York. pp. 179–244. van den Heuvel, R. N., Hefting, M. M., Tan, N. C. G., Jetten, M. S. M. and Verhoeven, J. T. A., 2009. N2 O emission hotspots at different spatial scales and governing factors for small scale hotspots. Sci. Total Environ. 407: 2325–2332. Vermeulen, G. D. and Mosquera, J. 2009. Soil, crop and emission responses to seasonal-controlled traffic in organic vegetable farming on loam soil. Soil Till. Res. 102(1): 126–134. Vieten, B., Conen, F., Seth, B. and Alewell, C. 2008. The fate of N2 O consumed in soils. Biogeosciences. 5: 129–132. Yamulki, S. and Jarvis, S. C. 2002. Short-term effects of tillage and compaction on nitrous oxide, nitric oxide, nitrogen dioxide, methane and carbon dioxide fluxes from grassland. Biol. Fert. Soils. 36: 224–231. Yanai, J., Sawamoto, T., Oe, T., Kusa, K., Yamakawa, K., Sakamoto, K., Naganawa, T., Inubushi, K., Hatano, R. and Kosaki, T. 2003. Spatial variability of nitrous oxide emissions and their soil-related determining factors in an agricultural field. J. Environ. Qual. 32: 1965–1977. Yates, T. T., Si, B. C., Farrell, R. E. and Pennock, D. J. 2006. Probability distribution and spatial dependence of nitrous oxide emission: temporal change in hummocky terrain. Soil Sci. Soc. Am. J. 70: 753–762.