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Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate
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Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate Klaus Butterbach-Bahl1 and Michael Dannenmann2 Human activities have accelerated global nitrogen cycling by approx. a factor of two. Also under future environmental conditions, agricultural nitrogen use is expected to remain the leading cause of reactive nitrogen (Nr) release to the environment. The main process to remove Nr from the environment is microbial denitrification. Here we summarize potential mechanisms that may affect denitrification and associated nitrous oxide (N2O) emissions in/from agricultural systems under future environmental conditions. Though changes in climate, specifically in temperature and precipitation, are likely to directly affect denitrification rates and N2O emissions, we identified several indirect mechanisms of global change that may potentially override direct effects. Among these are a) landscape scale changes of hotspots of denitrification: while the importance of non-hydromorphic upland soils for denitrification may decrease owing to limitations in soil moisture the importance of riparian areas as denitrification hotspots may further increase owing to the increased likeliness of flooding events leading to more frequent occurrences of aerobic– anaerobic cycles in riparian areas and, thus, increased denitrification, b) increased provision of labile carbon substrates via plant root exudation in the rhizosphere under elevated atmospheric carbon dioxide (CO2) concentrations, leading to increased microbial activity and higher denitrification rates in agricultural subsoils, thereby potentially reducing rates of nitrate leaching from agricultural soils and c) increased ammonia (NH3) volatilization from agricultural systems leading to increased denitrification rates and N2O emissions downwind from NH3 emission sources. Obviously, under future environmental conditions the mentioned mechanisms would further strengthen the regional disjunction of areas of Nr application from those of Nr removal by denitrification, thereby calling for a reappraisal of the importance of indirect emissions of N2O from agricultural Nr use. It remains unclear, to which extent climate change mitigation options such as the introduction of no-till systems or the increasing use of slow release fertilizers in conjunction with nitrification inhibitors or the adaptations of agricultural management practices to climate change such as altered timing of cultivation, choice of crop varieties and adaptation of water saving production systems may finally override direct and indirect climate change effects on denitrification and N2O emissions from agricultural systems. Addresses 1 Karlsruhe Institute of Technology, Institute for Meteorology and Climate Research, Atmospheric Environmental Research (IMK-IFU), Kreuzeckbahnstr. 19, 82467 Garmisch-Partenkirchen, Germany 2 Institute of Forest Botany and Tree Physiology, Chair of Tree Physiology, University of Freiburg; Georges-Koehler-Allee 53/54, 79110 Freiburg, Germany Corresponding author: Butterbach-Bahl, Klaus ([email protected]) www.sciencedirect.com
Current Opinion in Environmental Sustainability 2011, 3:389–395 This review comes from a themed issue on Carbon and nitrogen cycles Edited by Carolien Kroeze and Lex Bouwman Received 2 May 2011; Accepted 4 August 2011 Available online 26th August 2011 1877-3435/$ – see front matter # 2011 Elsevier B.V. All rights reserved. DOI 10.1016/j.cosust.2011.08.004
Introduction The human perturbation of the nitrogen (N) cycle due to a) the increased production of nitrogen fertilizer to fuel the increasing demand of mankind for food and feed and b) the incidental production of oxidized reactive N compounds in the frame of combustion processes has led to an unprecedented accumulation of reactive nitrogen (Nr) in the biosphere [1]. The resulting environmental consequences are numerous and serious, including eutrophication, loss of biodiversity, health problems and effects on the climate system [2]. Microbial denitrification is the dominating process removing Nr from the terrestrial biosphere by converting oxidized nitrogen compounds such as nitrate (NO3) via nitrous oxide (N2O) back into inert dinitrogen (N2). It has been estimated that soils of terrestrial ecosystems denitrify approx. 124 Tg N yr1 or 35– 40% of total N from land-based Nr sources [3]. Agricultural fields with high nitrogen application rates and poor soil drainage are supposedly hot spots for denitrification [4]. Other major sinks for land-based Nr are freshwater systems or the ocean. Denitrification rates in agricultural soils are supposed to be approximately one order of magnitude larger than in natural soils [15] and total denitrification N losses from arable soils are estimated to be in a range of 22–87 Tg N yr1 [4]. Arable soils are also the dominating anthropogenic source for atmospheric N2O contributing approximately 5.3 Tg N2O-N yr1 or 30–40% to the total global atmospheric N2O source strength [16]. Denitrification is of outstanding importance for closing the nitrogen cycle, and arable as well as managed grassland soils are hotspots for denitrification, a key source process for atmospheric N2O. This manuscript reviews existing literature and aims to provide a summary of current understanding of feedbacks of climate change on denitrification and direct (at the site of fertilizer N application to cultivated Current Opinion in Environmental Sustainability 2011, 3:389–395
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soils or grasslands) and indirect (N2O production following the dislocation of nitrogen downstream [leaching, surface run-off] and downwind [NH3 volatilization] of the application site) N2O emissions owing to agricultural activities. The potential feedback of expected climate change on denitrification and soil N2O losses is also separated into ‘direct effects’ such as temperature and moisture impacts on microbial processes and ‘indirect effects’ such as impacts of elevated CO2 on denitrification via the plant–soil link. Thereby we are tackling the problem if emissions of N2O may further increase or decrease with changes in climate. The focus of this review is on soils and soil–plant processes, thereby only partly considering possible adaptations of management and cropping systems under future climatic conditions.
Climate (global) change and denitrification Microbial denitrification is a sequential enzymatic process predominantly occurring under oxygen (O2) limiting or anaerobic conditions and is concomitant with energy conservation [5]. The capability for denitrification is widespread and can be found among proteobacteria, archaea and fungi. Besides oxidized N substrates all non-chemo-litho-authotrophic microorganisms capable to denitrify require easy degradable carbon (C) sources, which are oxidized while the N-oxides are reduced. However, the respiratory reduction chain of denitrification – typically NO3 ! nitrite (NO2) ! nitric oxide (NO) ! N2O ! N2 – does not necessarily operate to N2, but may stop already at the stage of NO or N2O depending on environmental conditions or genetic configuration. Some denitrifiers are even lacking the enzyme for reducing N2O to N2, so that denitrification stops at the stage of N2O [6]. Consequently, denitrification is on the one hand the key process for the removal of Nr from the terrestrial biosphere, but on the other hand – besides nitrification – also one of the dominating sources for the atmospheric greenhouse gas N2O. These closely linked two faces of denitrification attracted interest of biogeochemists and microbiologists since many decades [7]. However, they had to realize, that, owing to extreme methodological difficulties in the quantification of its gaseous end product N2 [8] and its extremely high spatial and temporal variability [9], denitrification is a miserable process to investigate [8]. In the past years, molecular methods have increasingly contributed to our understanding of denitrification. However, parameters such as denitrifier community composition, gene expression and enzyme activities of denitrification could only rarely be related with simultaneously determined production and emission of denitrification products such as N2O and N2 [10,11]. Overall, surprisingly little progress has been made in denitrification research since the 1960s [12]. Then, as now, similar methodological problems hamper our understanding of denitrification at site, landscape (>5 km 5 km) to continental scales as well as the controls and magnitude of net N2O loss [8,13,14]. Current Opinion in Environmental Sustainability 2011, 3:389–395
Denitrification as a microbial process in soils is depending on a multitude of environmental factors finally driving its magnitude, temporal dynamics and end product preference (Figure 1). Namely substrate availability, here oxidized nitrogen compounds and easy degradable carbon, temperature redox potential or oxygen availability and soil pH are the major factors affecting denitrification [5,8,10,11]. Moreover, food web interactions and the diversity of the denitrifier community and its response to environmental disturbances such as drying re-wetting or freeze-thaw events may affect denitrification [6,10,11]. Climate change will directly affect denitrification via changes in soil moisture and temperature regimes [10], but indirect effects may be as important as direct ones. Indirect effects include rising atmospheric carbon dioxide (CO2) concentrations and associated changes in plant water use efficiency, plant biomass production and rhizo-deposition of C substrates (Figure 2). The latter processes will increase water as well as substrate availability in soils. If one continues this line of argumentation, it gets obvious that, as a net result, increased levels of atmospheric CO2 may lead to increased soil microbial activity going along with higher rates of oxygen consumption in the rhizosphere [17], which finally may stimulate denitrification and N2O formation (Figure 2). On the contrary, increased plant C assimilation may lead to a widening of litter C:N ratios that may slow down decomposition, thereby also limiting substrate availability for denitrification and N2O production [18]. It should be noted that this article is primarily dealing with effects of climate change on denitrification and soil N2O emissions inagricultural systems, which are normally not N limited owing to sufficient N fertilization. Hence, the potential impact of N limitations on denitrification will be neglected, though the latter mechanism may constrain denitrification in natural, N-limited systems but not in agricultural systems where farmers may increase N fertilization to achieve optimal crop yields. Furthermore, it needs to be acknowledged that differentiating climate change effects on denitrification from effects in changes in agricultural management is potentially misleading, too (Figure 1). The widespread introduction of no-till systems in agriculture as a measure to recarbonize agricultural soils and thus to mitigate increases in atmospheric CO2 concentrations [19] has significant implications on soil moisture, soil aeration, denitrification substrate availability and soil N2O emissions [20]. Also the increasing use of nitrification inhibitors to increase N fertilizer use efficiencies and to simultaneously reduce N trace gas emissions from soils [21] may by far be more important for denitrification dynamics in agriculture systems as compared to changes in climate. Finally, it can be expected that farmers will increase irrigation of crops, which unavoidably would stimulate denitrification and associated N2O emissions. www.sciencedirect.com
Denitrification and associated soil N2O emissions Butterbach-Bahl and Dannenmann 391
Land use
Figure 1
Change Nitrification Climate Management
Atmospheric composition
Precipitation
CO2
Physico - chemical environment
Climate change
Temperature
NH3 (R-NH2)NH2OHNO2- NO3-
Radiation Temperature
Adaptation (e.g. fertilizer use, irrigation, crops & crop rotations
Soil C and N mineralisation
Moisture
N2O NO
DOC
NO3NO2-
Soil microbial community
Water table
Denitrification Soil physics Texture Compaction
NO3-
Plant litter & Exudation
NO2-
Aeration
Soil chemistry C/N availability Soil redox
NO
Plant species composition
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N-Deposition (+O3, …)
Plant Physiology
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(WUE, Photosynthesis)
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Pathways, mechanisms and processes involved in climate change effects on denitrification and N2O emissions. Denitrification will not only be affected by direct climate change effects such as changes in temperature and precipitation, but also by indirect effects, for example, changes in atmospheric composition and land use and land management. Land management also comprises measures to adopting to climate change such as changes in fertilizer use, additional irrigation or changes of crops or crop rotations. These indirect effects could override direct climate change effects on denitrification. DOC: dissolved organic carbon, here used as synonym for easily degradable carbon substrates. WUE: water use efficiency.
Denitrification and future soil moisture and temperature changes To analyze how climate change may affect denitrification we reviewed climate scenarios for Europe. Based on SRES B2 emission scenario average temperature in Europe may increase by 1–4 8C for the period 2070–2090 as compared to the climate normal period (1960–1990), with warming being greater in winter in the North and in summer in southern and central Europe [22]. Predictions of changes in precipitation are remaining uncertain, but in general all simulations agree that mean annual precipitation may increase in northern Europe while decrease further south. It is noteworthy that projected seasonal precipitation will vary substantially from season to season and across regions in response to changes in large-scale circulation and water vapor loading [22]. Consequently, the likeliness of extreme events such as prolonged and intensive drought periods and heat waves as well as flooding events is increasing too [22]. Agriculture has already started to adapt, for example, by expanding growing of silage and grain maize northwards or by changing timing of cultivation, choice of crop varieties and adapting water saving www.sciencedirect.com
production systems [23]. How these changes in land management will finally feedback on denitrification in agricultural systems remains uncertain. If climate change adaptations also include measures to increase nitrogen use efficiencies, this would result in a reduction of the Nr-surplus and, thus, in the long run decrease denitrification and N2O emissions from the agricultural sector. Major uncertainties are also remaining with regard to the response of denitrification to the climate signal, that is, how soil denitrification activity and N2O emissions will change if average temperatures are increasing or if precipitation – and thus soil moisture – get more variable. Also the effect of extreme events on denitrification needs to be considered here. Generally, denitrification in agricultural systems will respond positively to changes in temperature if denitrification substrates – that is, easy decomposable carbon substances and nitrate – are available, which depends among others on fertilizer application schemes and crop N uptake. The potential enhancement of denitrification activity can be explained on the one hand by larger Current Opinion in Environmental Sustainability 2011, 3:389–395
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Figure 2
+ extreme events
+
+ temperature
Indirect N2 O emissions
+ CO2 concentration
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Overall balance: + (?)
+ + photosynthesis
Direct N 2 O emissions
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Overall balance: +/- (?)
+ plant N uptake + nutrient surface flow
+ C rhizodeposition
+ NH3 volatilization
SOM + DOC
+ soil respiration + plant WUE + anaerobic volume + N 2 :N2 O ratio
NH 4+
NO 3-
+ Denitrification + microbial Immobilization
- NO3- leaching Current Opinion in Environmental Sustainability
Feedback mechanisms of extreme events, increased temperature and elevated atmospheric CO2 concentrations on denitrification and associated direct and indirect N2O emissions. DOC: dissolved organic carbon; NH3/NH4: ammonia/ammonium; NO3: nitrate; C: labile organic carbon compounds such as sugars, amino acids; N: nitrogen; WUE: water use efficiency, SOM: soil organic matter. Dashed coloured arrows represent feedback mechanisms of climate change factors, white arrows represent soil processes. Note that only selected processes of the nitrogen cycle are included in this graph.
microbial turnover rate coefficients with increasing temperatures. On the other hand soil anaerobiosis will expand owing to temperature related increases in soil respiration. Reported Q10 values for denitrification are in the range of approx. 2–10, with values being in the range of 6–8 for non-limiting conditions with regard to soil moisture and nitrate supply [24]. Values higher than approx. 2 indicate that the temperature response is not purely enzymatic, but that increased anaerobiosis in the soil – owing to the increasing respiratory demand for O2 of the microorganism community and limited O2 diffusion into the soil – has fueled denitrification. This strong response of denitrification to temperature does not necessarily allow to concluding that N2O emissions may also exponentially increase Current Opinion in Environmental Sustainability 2011, 3:389–395
with increasing temperatures, since the few studies available indicate that the N2O:N2 ratio may decrease with increasing temperature, though the increase in total denitrification could partly outweigh this effect [26]. This view is supported by a modeling study where the response of forest soil N2O and N2 emissions under future climate conditions was investigated. Driving the biogeochemical model PnET-N-DNDC with climate scenarios for the period 2031–2039 as compared to present day climate (1991–2000) resulted in an overall lowering of N2O emissions from European forest soils by 6%. This simulated decrease in N2O emissions was mainly due to a shift in the N2O:N2 ratio driven by enhanced denitrification [27]. The favoring of N2 as endproduct of denitrification at elevated temperatures www.sciencedirect.com
Denitrification and associated soil N2O emissions Butterbach-Bahl and Dannenmann 393
can be explained by the decreasing availability of electron acceptors with increasing anaerobiosis forcing denitrifiers to be as resource efficient as possible and, thus, to express the full chain of denitrification enzymes. By contrast, studies evaluating warming effects on denitrifying enzyme activities (DEA) are contradictory: out of six investigated studies, only one reported a significant effect (+44%), while the other five studies could not demonstrate a significant positive response (+<20%) [25]. However, since it can be questioned if DEA assays are related to actual rates of denitrification, the importance of such findings for understanding responses of denitrification to a warming environment remains unsafe. The effect of increased occurrence of prolonged drought and subsequent re-wetting periods under future climate conditions on denitrification and associated N2O emissions is uncertain, since the sensitivity of microorganisms and processes involved in the N cycle (ammonification, nitrification, denitrification, immobilization) to drought stress is largely unknown [28]. On the one hand it is well documented that soil re-wetting events may result in pulse emissions of NO and N2O. If this also applies for N2 is unsure owing to missing experimental evidence. However, even in view that pulse emissions may be several fold larger than ‘normal’ background emissions, the reduction in cumulative N2O emissions over a drought period is usually not compensated by the following rewetting-induced emission pulse [28]. Therefore, it is unlikely that future increases in the length and intensity of drought periods will result in increased denitrification and N2O emissions from typical upland soils such as cambisols. The contrary may be true for hydromorphic soils such as gley soils often found in riparian areas, which are hotspots of terrestrial denitrification [3,9]. Here, larger variability of rainfall will increase the frequency of aerobic–anaerobic cycles and therefore increase denitrification activity [29]. Also the likeliness of periods of high N2O emissions from hydromorphic soils may increase since maximum N2O fluxes are observed when soil moisture is switching over from dry conditions to soil water matrix potentials in the range of 1.9 to 4.7 kPa (equaling pF 1.3–1.7), that is, if soils are approaching waterlogging [30]. Consequently, the importance of riparian areas and hydromorphic soils as hotspots for denitrification (and N2O emissions) may further increase under predicted climate change. A better quantification and prediction of the importance of hydromorphic soils as potentially dominating N2O sources under future climate conditions will require a better understanding of sources and sinks of nitrogen at landscape scales – including lateral transport of nitrate with soil water – and a reappraisal of indirect N2O emissions at regional scales owing to fertilizer use in adjacent and/or upstream agricultural systems. The latter point is also important with regard to indirect N2O emissions resulting from ammonia (NH3) volatilization following synthetic or organic fertilizer www.sciencedirect.com
applications to agricultural soils. Under future climate conditions – assuming that fertilizer, manure and slurry spreading techniques are not changing – NH3 volatilization may increase while soil N2O emissions may stay stable or even decrease owing to higher temperatures and lower soil moisture conditions during spring-time, the main period for fertilizer applications and associated NH3 emissions. Re-deposition of NH3 to downwind ecosystems may again fuel denitrification and N2O emissions (see Figure 2). A further point to acknowledge is the effect of increased soil erosion of agricultural fields following extreme rain events in future climate scenarios. Here sediment transport is accompanied with nutrient losses, also potentially stimulating denitrification as well as N2O emissions downstream the Nr source (Figure 2).
Denitrification and changes in atmospheric composition (CO2, Nr deposition, O3) – the plant–soil link In view of the direct positive link between Nr availability, microbial N turnover processes and denitrification in soils and N2O emissions, changes in future rates of atmospheric Nr deposition are a key factor for predicting how denitrification may change under future climate conditions. Surely, this applies at first for non-agricultural systems and not for fertilized soils, where direct Nr application rates may by far exceed rates of atmospheric Nr deposition. Nevertheless, most of the atmospheric Nr deposition originates from agricultural sources. Furthermore, it has to be acknowledged that all scenarios agree in projecting a decrease in NOx emissions owing to energy production, while agricultural nitrogen use is expected to remain the leading cause of Nr release to the environment [2]. Thus, Nr cascading starting with the use of Nr in agricultural systems will continue at high levels [2,13] and overall reductions in N2O emissions are unlikely to be expected. A more indirect mechanism how altered atmospheric composition may affect denitrification and associated N2O emissions is induced by elevated atmospheric CO2 concentrations. Increased atmospheric CO2 levels are likely to act on two ways on soil denitrification activity and N2O emissions (Figure 2): a) The water use efficiency of plant photosynthesis is positively correlated with levels of atmospheric CO2. Consequently, under elevated atmospheric CO2 concentrations plant transpiration is reduced, which leads to higher soil water contents [31]. These higher soil water contents decrease soil gas diffusion, stimulating anaerobiosis and thus increase the likeliness of denitrification in soils. b) For conditions of elevated atmospheric CO2 rhizodeposition of labile C compounds such as amino acids and amino sugars from agricultural plants is likely to increase. As a result the availability of labile carbon Current Opinion in Environmental Sustainability 2011, 3:389–395
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substrates in the soil is increased that may result in a stimulation of soil microbial turnover processes and an improvement of environmental conditions for denitrification via increased soil anaerobiosis and C substrate provision [17,18].
However, results from CO2 enrichment experiments are highly controversial [18]: an earlier meta-analysis on CO2-effects on denitrification enzyme activity (DEA), predominantly conducted with herbaceous systems, reported a decrease at increasing CO2 levels. However, as already pointed out earlier, one may on the one hand question the DEA approach and on the other hand needs to discuss if the proposed mechanism that finally leads to reduced denitrification rates – that is, increased immobilization of Nr in the plant biomass and thus a decrease in mineral N and NO3 in the soil – may also be valid for highly fertilized agricultural systems. Recent reports on changes in soil N2O emissions from fertilized soils under elevated atmospheric CO2 concentrations strongly indicate that N2O emissions are likely to increase, thereby partly off-setting the greenhouse gas benefits from increased plant CO2 fixation [32,33,34]. A so far rarely considered side effect of increased C substrate availability under elevated CO2 is its potential consequence for subsoil denitrification. A major fraction of agricultural surplus Nr is leached to the groundwater. Nitrate can pass the subsoil without being further reduced by denitrification since the existing denitrifier community is strongly C substrate limited. If under future climate conditions and elevated atmospheric CO2 concentrations easily degradable C substrates are increasingly leached to the subsoil [35], more NO3 may get denitrified, thereby decreasing the NO3 load of the groundwater and increasing subsoil N2O and N2 production. Finally, also changes in atmospheric O3 concentration may indirectly affect soil denitrification. Again it is the plant–soil link being of importance here and specifically the effect of tropospheric O3 on plant health, biomass growth and litter quality. Based on a modeling study it has been estimated that owing to plant ozone damage the global gross primary production in 2100 is decreased by 8–23% as compared to 1901 [36]. Associated changes in rhizodeposition of C substrates and litter quality may also affect denitrification in soils and associated N2O emissions, even though this mechanism may be of little importance as compared to other climate change effects.
nonlinear interrelated and rarely investigated in multifactorial field and laboratory experiments. However, it is obvious that the plant–soil link and its importance as controller of soil N and C substrate availability needs to be further stressed and that single site observations need to be supplemented by a more holistic view on denitrification and N2O emissions at landscape scales. This will require a stronger linkage of modeling and measuring activities, specifically since measurements of denitrification and N2 production by denitrification are still scarce but needed for a thorough understanding of the variability of the denitrification process as affected by environmental constrains and, thus, for an improved numerical description of denitrification in process models. It still remains an open question if climate change effects – that is, changes in precipitation, temperature and atmospheric CO2 concentrations – on denitrification and soil N2O emissions may not be overridden by changes in agricultural management practices, for example, in the frame of adaptation measures to climate change.
Acknowledgements We thank the German Science Foundation (Deutsche Forschungsgemeinschaft) for generously funding the work of Michael Dannenmann through contract number DA 1217/2-1. Part of this work is a contribution to the EU funded integrated project NitroEurope.
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Conclusions It is apparent that the existing knowledge how denitrification and associated N2O emissions from agricultural sources may change in a changing climate is limited. The reason for this is that mechanisms leading to changes in denitrification under future environmental conditions are Current Opinion in Environmental Sustainability 2011, 3:389–395
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Climate Change 2007: Impacts, Adaptation and Vulnerability. Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. Edited by Parry ML, Canziani OF, Palutikof JP, Van der Linden PJ, Hanson CE. Cambridge, UK: Cambridge University Press; 2007:541-580. 23. Olesen JE, Trnka M, Kersebaum KC, Skjelvagd AO, Seguin B, Peltonen-Sainio P, Rossi F, Kozyra J, Micale F: Impacts and adaptation of European crop production systems to climate change. European Journal of Agronomy 2011, 34:96-112. 24. Abdalla M, Jones M, Smith P, Williams M: Nitrous oxide and denitrification sensitivity to temperature in Irish pasture soils. Soil Use and Management 2009, 25:376-388. 25. Barnard RP, Leadley W, Hungate BA: Global change, nitrification, and denitrification: a review. Global Biogeochemical Cycles 2005, 19:GB1007 doi: 10.1029/ 2004GB2282. Summarizing current understanding how global changes may feedback on the microbial processes of nitrification and denitrification. 26. Smith KA: The potential for feedback effects induced by global warming on emissions of nitrous oxide by soils. Global Change Biology 1997, 3:327-338. 27. Kesik M, Bru¨ggemann N, Forkel R, Knoche R, Li C, Seufert G, Simpson D, Butterbach-Bahl K: Future scenarios of N2O and NO emissions from European forest soils. Journal of Geophysical Research 2006, 111:G02018. 28. Borken W, Matzner E: Reappraisal of drying and wetting effects on C and N mineralization and fluxes in soils. Global Change Biology 2008, 14:1-17. 29. Pinay G, Gumiero B, Tabacchi E, Gimenez O, Tabacchi-Planty AM, Hefting MM, Burt TP, Black VA, Nilsson C, Iordache V et al.: Patterns of denitrification rates in European alluvial soils under various hydrological regimes. Freshwater Biology 2007, 52:252-266. 30. Castellano MJ, Schmidt JP, Kaye JP, Walker C, Graham CB, Lin H, Dell CJ: Hydrological and biogeochemical controls on the timing and magnitude of nitrous oxide flux across an agricultural landscape. Global Change Biology 2010, 16:2711-2720. 31. Long SP, Ainsworth EA, Rogers A, Ort DR: Rising atmospheric carbon dioxide: plants face the future. Annual Reviews Plant Biology 2004, 55:591-628. 32. Baggs EM, Richter M, Cadisch G, Hartwig UA: Denitrification in grass swards is increased under elevated atmospheric CO2. Soil Biology and Biochemistry 2003, 35:729-732. 33. Kammann C, Mu¨ller C, Gru¨nhage L, Ja¨ger HJ: Elevated CO2 stimulates N2O emissions in permanent grassland. Soil Biology and Biochemistry 2008, 40:2194-2205. Provides insights from a field (FACE) study in a temperate grassland ecosystem how elevated CO2 may change soil microbial N turnover processes and associated N2O production and emission. 34. Lam SK, Lin E, Norton R, Chen D: The effect of increased atmospheric carbon dioxide concentration on emissions of nitrous oxide, carbon dioxide and methane from a wheat field in a semi-arid environment in northern China. Soil Biology and Biochemistry 2011, 43:458-461. 35. Harrison AF, Taylor K, Scott A, Poskitt J, Benhan D, Grace J, Chaplow J, Rowland P: Potential effects of climate change on DOC release from three different soil types on the Northern Pennines UK: examination using field manipulation experiments. Global Change Biology 2008, 14:687-702. 36. Sitch S, Cox PM, Collins WJ, Huntingford C: Indirect radiative forcing of climate change through ozone effects on the land carbon sink. Nature 2007, 448:791-794.
Current Opinion in Environmental Sustainability 2011, 3:389–395
Denitrification and associated soil N2O emissions due to agricultural activities in a changing climate Klaus Butterbach-Bahl1 and Michael Dannenmann2 Human activities have accelerated global nitrogen cycling by approx. a factor of two. Also under future environmental conditions, agricultural nitrogen use is expected to remain the leading cause of reactive nitrogen (Nr) release to the environment. The main process to remove Nr from the environment is microbial denitrification. Here we summarize potential mechanisms that may affect denitrification and associated nitrous oxide (N2O) emissions in/from agricultural systems under future environmental conditions. Though changes in climate, specifically in temperature and precipitation, are likely to directly affect denitrification rates and N2O emissions, we identified several indirect mechanisms of global change that may potentially override direct effects. Among these are a) landscape scale changes of hotspots of denitrification: while the importance of non-hydromorphic upland soils for denitrification may decrease owing to limitations in soil moisture the importance of riparian areas as denitrification hotspots may further increase owing to the increased likeliness of flooding events leading to more frequent occurrences of aerobic– anaerobic cycles in riparian areas and, thus, increased denitrification, b) increased provision of labile carbon substrates via plant root exudation in the rhizosphere under elevated atmospheric carbon dioxide (CO2) concentrations, leading to increased microbial activity and higher denitrification rates in agricultural subsoils, thereby potentially reducing rates of nitrate leaching from agricultural soils and c) increased ammonia (NH3) volatilization from agricultural systems leading to increased denitrification rates and N2O emissions downwind from NH3 emission sources. Obviously, under future environmental conditions the mentioned mechanisms would further strengthen the regional disjunction of areas of Nr application from those of Nr removal by denitrification, thereby calling for a reappraisal of the importance of indirect emissions of N2O from agricultural Nr use. It remains unclear, to which extent climate change mitigation options such as the introduction of no-till systems or the increasing use of slow release fertilizers in conjunction with nitrification inhibitors or the adaptations of agricultural management practices to climate change such as altered timing of cultivation, choice of crop varieties and adaptation of water saving production systems may finally override direct and indirect climate change effects on denitrification and N2O emissions from agricultural systems. Addresses 1 Karlsruhe Institute of Technology, Institute for Meteorology and Climate Research, Atmospheric Environmental Research (IMK-IFU), Kreuzeckbahnstr. 19, 82467 Garmisch-Partenkirchen, Germany 2 Institute of Forest Botany and Tree Physiology, Chair of Tree Physiology, University of Freiburg; Georges-Koehler-Allee 53/54, 79110 Freiburg, Germany Corresponding author: Butterbach-Bahl, Klaus ([email protected]) www.sciencedirect.com
Current Opinion in Environmental Sustainability 2011, 3:389–395 This review comes from a themed issue on Carbon and nitrogen cycles Edited by Carolien Kroeze and Lex Bouwman Received 2 May 2011; Accepted 4 August 2011 Available online 26th August 2011 1877-3435/$ – see front matter # 2011 Elsevier B.V. All rights reserved. DOI 10.1016/j.cosust.2011.08.004
Introduction The human perturbation of the nitrogen (N) cycle due to a) the increased production of nitrogen fertilizer to fuel the increasing demand of mankind for food and feed and b) the incidental production of oxidized reactive N compounds in the frame of combustion processes has led to an unprecedented accumulation of reactive nitrogen (Nr) in the biosphere [1]. The resulting environmental consequences are numerous and serious, including eutrophication, loss of biodiversity, health problems and effects on the climate system [2]. Microbial denitrification is the dominating process removing Nr from the terrestrial biosphere by converting oxidized nitrogen compounds such as nitrate (NO3) via nitrous oxide (N2O) back into inert dinitrogen (N2). It has been estimated that soils of terrestrial ecosystems denitrify approx. 124 Tg N yr1 or 35– 40% of total N from land-based Nr sources [3]. Agricultural fields with high nitrogen application rates and poor soil drainage are supposedly hot spots for denitrification [4]. Other major sinks for land-based Nr are freshwater systems or the ocean. Denitrification rates in agricultural soils are supposed to be approximately one order of magnitude larger than in natural soils [15] and total denitrification N losses from arable soils are estimated to be in a range of 22–87 Tg N yr1 [4]. Arable soils are also the dominating anthropogenic source for atmospheric N2O contributing approximately 5.3 Tg N2O-N yr1 or 30–40% to the total global atmospheric N2O source strength [16]. Denitrification is of outstanding importance for closing the nitrogen cycle, and arable as well as managed grassland soils are hotspots for denitrification, a key source process for atmospheric N2O. This manuscript reviews existing literature and aims to provide a summary of current understanding of feedbacks of climate change on denitrification and direct (at the site of fertilizer N application to cultivated Current Opinion in Environmental Sustainability 2011, 3:389–395
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soils or grasslands) and indirect (N2O production following the dislocation of nitrogen downstream [leaching, surface run-off] and downwind [NH3 volatilization] of the application site) N2O emissions owing to agricultural activities. The potential feedback of expected climate change on denitrification and soil N2O losses is also separated into ‘direct effects’ such as temperature and moisture impacts on microbial processes and ‘indirect effects’ such as impacts of elevated CO2 on denitrification via the plant–soil link. Thereby we are tackling the problem if emissions of N2O may further increase or decrease with changes in climate. The focus of this review is on soils and soil–plant processes, thereby only partly considering possible adaptations of management and cropping systems under future climatic conditions.
Climate (global) change and denitrification Microbial denitrification is a sequential enzymatic process predominantly occurring under oxygen (O2) limiting or anaerobic conditions and is concomitant with energy conservation [5]. The capability for denitrification is widespread and can be found among proteobacteria, archaea and fungi. Besides oxidized N substrates all non-chemo-litho-authotrophic microorganisms capable to denitrify require easy degradable carbon (C) sources, which are oxidized while the N-oxides are reduced. However, the respiratory reduction chain of denitrification – typically NO3 ! nitrite (NO2) ! nitric oxide (NO) ! N2O ! N2 – does not necessarily operate to N2, but may stop already at the stage of NO or N2O depending on environmental conditions or genetic configuration. Some denitrifiers are even lacking the enzyme for reducing N2O to N2, so that denitrification stops at the stage of N2O [6]. Consequently, denitrification is on the one hand the key process for the removal of Nr from the terrestrial biosphere, but on the other hand – besides nitrification – also one of the dominating sources for the atmospheric greenhouse gas N2O. These closely linked two faces of denitrification attracted interest of biogeochemists and microbiologists since many decades [7]. However, they had to realize, that, owing to extreme methodological difficulties in the quantification of its gaseous end product N2 [8] and its extremely high spatial and temporal variability [9], denitrification is a miserable process to investigate [8]. In the past years, molecular methods have increasingly contributed to our understanding of denitrification. However, parameters such as denitrifier community composition, gene expression and enzyme activities of denitrification could only rarely be related with simultaneously determined production and emission of denitrification products such as N2O and N2 [10,11]. Overall, surprisingly little progress has been made in denitrification research since the 1960s [12]. Then, as now, similar methodological problems hamper our understanding of denitrification at site, landscape (>5 km 5 km) to continental scales as well as the controls and magnitude of net N2O loss [8,13,14]. Current Opinion in Environmental Sustainability 2011, 3:389–395
Denitrification as a microbial process in soils is depending on a multitude of environmental factors finally driving its magnitude, temporal dynamics and end product preference (Figure 1). Namely substrate availability, here oxidized nitrogen compounds and easy degradable carbon, temperature redox potential or oxygen availability and soil pH are the major factors affecting denitrification [5,8,10,11]. Moreover, food web interactions and the diversity of the denitrifier community and its response to environmental disturbances such as drying re-wetting or freeze-thaw events may affect denitrification [6,10,11]. Climate change will directly affect denitrification via changes in soil moisture and temperature regimes [10], but indirect effects may be as important as direct ones. Indirect effects include rising atmospheric carbon dioxide (CO2) concentrations and associated changes in plant water use efficiency, plant biomass production and rhizo-deposition of C substrates (Figure 2). The latter processes will increase water as well as substrate availability in soils. If one continues this line of argumentation, it gets obvious that, as a net result, increased levels of atmospheric CO2 may lead to increased soil microbial activity going along with higher rates of oxygen consumption in the rhizosphere [17], which finally may stimulate denitrification and N2O formation (Figure 2). On the contrary, increased plant C assimilation may lead to a widening of litter C:N ratios that may slow down decomposition, thereby also limiting substrate availability for denitrification and N2O production [18]. It should be noted that this article is primarily dealing with effects of climate change on denitrification and soil N2O emissions inagricultural systems, which are normally not N limited owing to sufficient N fertilization. Hence, the potential impact of N limitations on denitrification will be neglected, though the latter mechanism may constrain denitrification in natural, N-limited systems but not in agricultural systems where farmers may increase N fertilization to achieve optimal crop yields. Furthermore, it needs to be acknowledged that differentiating climate change effects on denitrification from effects in changes in agricultural management is potentially misleading, too (Figure 1). The widespread introduction of no-till systems in agriculture as a measure to recarbonize agricultural soils and thus to mitigate increases in atmospheric CO2 concentrations [19] has significant implications on soil moisture, soil aeration, denitrification substrate availability and soil N2O emissions [20]. Also the increasing use of nitrification inhibitors to increase N fertilizer use efficiencies and to simultaneously reduce N trace gas emissions from soils [21] may by far be more important for denitrification dynamics in agriculture systems as compared to changes in climate. Finally, it can be expected that farmers will increase irrigation of crops, which unavoidably would stimulate denitrification and associated N2O emissions. www.sciencedirect.com
Denitrification and associated soil N2O emissions Butterbach-Bahl and Dannenmann 391
Land use
Figure 1
Change Nitrification Climate Management
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Pathways, mechanisms and processes involved in climate change effects on denitrification and N2O emissions. Denitrification will not only be affected by direct climate change effects such as changes in temperature and precipitation, but also by indirect effects, for example, changes in atmospheric composition and land use and land management. Land management also comprises measures to adopting to climate change such as changes in fertilizer use, additional irrigation or changes of crops or crop rotations. These indirect effects could override direct climate change effects on denitrification. DOC: dissolved organic carbon, here used as synonym for easily degradable carbon substrates. WUE: water use efficiency.
Denitrification and future soil moisture and temperature changes To analyze how climate change may affect denitrification we reviewed climate scenarios for Europe. Based on SRES B2 emission scenario average temperature in Europe may increase by 1–4 8C for the period 2070–2090 as compared to the climate normal period (1960–1990), with warming being greater in winter in the North and in summer in southern and central Europe [22]. Predictions of changes in precipitation are remaining uncertain, but in general all simulations agree that mean annual precipitation may increase in northern Europe while decrease further south. It is noteworthy that projected seasonal precipitation will vary substantially from season to season and across regions in response to changes in large-scale circulation and water vapor loading [22]. Consequently, the likeliness of extreme events such as prolonged and intensive drought periods and heat waves as well as flooding events is increasing too [22]. Agriculture has already started to adapt, for example, by expanding growing of silage and grain maize northwards or by changing timing of cultivation, choice of crop varieties and adapting water saving www.sciencedirect.com
production systems [23]. How these changes in land management will finally feedback on denitrification in agricultural systems remains uncertain. If climate change adaptations also include measures to increase nitrogen use efficiencies, this would result in a reduction of the Nr-surplus and, thus, in the long run decrease denitrification and N2O emissions from the agricultural sector. Major uncertainties are also remaining with regard to the response of denitrification to the climate signal, that is, how soil denitrification activity and N2O emissions will change if average temperatures are increasing or if precipitation – and thus soil moisture – get more variable. Also the effect of extreme events on denitrification needs to be considered here. Generally, denitrification in agricultural systems will respond positively to changes in temperature if denitrification substrates – that is, easy decomposable carbon substances and nitrate – are available, which depends among others on fertilizer application schemes and crop N uptake. The potential enhancement of denitrification activity can be explained on the one hand by larger Current Opinion in Environmental Sustainability 2011, 3:389–395
392 Carbon and nitrogen cycles
Figure 2
+ extreme events
+
+ temperature
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+ CO2 concentration
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+ + photosynthesis
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+ plant N uptake + nutrient surface flow
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+ NH3 volatilization
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+ soil respiration + plant WUE + anaerobic volume + N 2 :N2 O ratio
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NO 3-
+ Denitrification + microbial Immobilization
- NO3- leaching Current Opinion in Environmental Sustainability
Feedback mechanisms of extreme events, increased temperature and elevated atmospheric CO2 concentrations on denitrification and associated direct and indirect N2O emissions. DOC: dissolved organic carbon; NH3/NH4: ammonia/ammonium; NO3: nitrate; C: labile organic carbon compounds such as sugars, amino acids; N: nitrogen; WUE: water use efficiency, SOM: soil organic matter. Dashed coloured arrows represent feedback mechanisms of climate change factors, white arrows represent soil processes. Note that only selected processes of the nitrogen cycle are included in this graph.
microbial turnover rate coefficients with increasing temperatures. On the other hand soil anaerobiosis will expand owing to temperature related increases in soil respiration. Reported Q10 values for denitrification are in the range of approx. 2–10, with values being in the range of 6–8 for non-limiting conditions with regard to soil moisture and nitrate supply [24]. Values higher than approx. 2 indicate that the temperature response is not purely enzymatic, but that increased anaerobiosis in the soil – owing to the increasing respiratory demand for O2 of the microorganism community and limited O2 diffusion into the soil – has fueled denitrification. This strong response of denitrification to temperature does not necessarily allow to concluding that N2O emissions may also exponentially increase Current Opinion in Environmental Sustainability 2011, 3:389–395
with increasing temperatures, since the few studies available indicate that the N2O:N2 ratio may decrease with increasing temperature, though the increase in total denitrification could partly outweigh this effect [26]. This view is supported by a modeling study where the response of forest soil N2O and N2 emissions under future climate conditions was investigated. Driving the biogeochemical model PnET-N-DNDC with climate scenarios for the period 2031–2039 as compared to present day climate (1991–2000) resulted in an overall lowering of N2O emissions from European forest soils by 6%. This simulated decrease in N2O emissions was mainly due to a shift in the N2O:N2 ratio driven by enhanced denitrification [27]. The favoring of N2 as endproduct of denitrification at elevated temperatures www.sciencedirect.com
Denitrification and associated soil N2O emissions Butterbach-Bahl and Dannenmann 393
can be explained by the decreasing availability of electron acceptors with increasing anaerobiosis forcing denitrifiers to be as resource efficient as possible and, thus, to express the full chain of denitrification enzymes. By contrast, studies evaluating warming effects on denitrifying enzyme activities (DEA) are contradictory: out of six investigated studies, only one reported a significant effect (+44%), while the other five studies could not demonstrate a significant positive response (+<20%) [25]. However, since it can be questioned if DEA assays are related to actual rates of denitrification, the importance of such findings for understanding responses of denitrification to a warming environment remains unsafe. The effect of increased occurrence of prolonged drought and subsequent re-wetting periods under future climate conditions on denitrification and associated N2O emissions is uncertain, since the sensitivity of microorganisms and processes involved in the N cycle (ammonification, nitrification, denitrification, immobilization) to drought stress is largely unknown [28]. On the one hand it is well documented that soil re-wetting events may result in pulse emissions of NO and N2O. If this also applies for N2 is unsure owing to missing experimental evidence. However, even in view that pulse emissions may be several fold larger than ‘normal’ background emissions, the reduction in cumulative N2O emissions over a drought period is usually not compensated by the following rewetting-induced emission pulse [28]. Therefore, it is unlikely that future increases in the length and intensity of drought periods will result in increased denitrification and N2O emissions from typical upland soils such as cambisols. The contrary may be true for hydromorphic soils such as gley soils often found in riparian areas, which are hotspots of terrestrial denitrification [3,9]. Here, larger variability of rainfall will increase the frequency of aerobic–anaerobic cycles and therefore increase denitrification activity [29]. Also the likeliness of periods of high N2O emissions from hydromorphic soils may increase since maximum N2O fluxes are observed when soil moisture is switching over from dry conditions to soil water matrix potentials in the range of 1.9 to 4.7 kPa (equaling pF 1.3–1.7), that is, if soils are approaching waterlogging [30]. Consequently, the importance of riparian areas and hydromorphic soils as hotspots for denitrification (and N2O emissions) may further increase under predicted climate change. A better quantification and prediction of the importance of hydromorphic soils as potentially dominating N2O sources under future climate conditions will require a better understanding of sources and sinks of nitrogen at landscape scales – including lateral transport of nitrate with soil water – and a reappraisal of indirect N2O emissions at regional scales owing to fertilizer use in adjacent and/or upstream agricultural systems. The latter point is also important with regard to indirect N2O emissions resulting from ammonia (NH3) volatilization following synthetic or organic fertilizer www.sciencedirect.com
applications to agricultural soils. Under future climate conditions – assuming that fertilizer, manure and slurry spreading techniques are not changing – NH3 volatilization may increase while soil N2O emissions may stay stable or even decrease owing to higher temperatures and lower soil moisture conditions during spring-time, the main period for fertilizer applications and associated NH3 emissions. Re-deposition of NH3 to downwind ecosystems may again fuel denitrification and N2O emissions (see Figure 2). A further point to acknowledge is the effect of increased soil erosion of agricultural fields following extreme rain events in future climate scenarios. Here sediment transport is accompanied with nutrient losses, also potentially stimulating denitrification as well as N2O emissions downstream the Nr source (Figure 2).
Denitrification and changes in atmospheric composition (CO2, Nr deposition, O3) – the plant–soil link In view of the direct positive link between Nr availability, microbial N turnover processes and denitrification in soils and N2O emissions, changes in future rates of atmospheric Nr deposition are a key factor for predicting how denitrification may change under future climate conditions. Surely, this applies at first for non-agricultural systems and not for fertilized soils, where direct Nr application rates may by far exceed rates of atmospheric Nr deposition. Nevertheless, most of the atmospheric Nr deposition originates from agricultural sources. Furthermore, it has to be acknowledged that all scenarios agree in projecting a decrease in NOx emissions owing to energy production, while agricultural nitrogen use is expected to remain the leading cause of Nr release to the environment [2]. Thus, Nr cascading starting with the use of Nr in agricultural systems will continue at high levels [2,13] and overall reductions in N2O emissions are unlikely to be expected. A more indirect mechanism how altered atmospheric composition may affect denitrification and associated N2O emissions is induced by elevated atmospheric CO2 concentrations. Increased atmospheric CO2 levels are likely to act on two ways on soil denitrification activity and N2O emissions (Figure 2): a) The water use efficiency of plant photosynthesis is positively correlated with levels of atmospheric CO2. Consequently, under elevated atmospheric CO2 concentrations plant transpiration is reduced, which leads to higher soil water contents [31]. These higher soil water contents decrease soil gas diffusion, stimulating anaerobiosis and thus increase the likeliness of denitrification in soils. b) For conditions of elevated atmospheric CO2 rhizodeposition of labile C compounds such as amino acids and amino sugars from agricultural plants is likely to increase. As a result the availability of labile carbon Current Opinion in Environmental Sustainability 2011, 3:389–395
394 Carbon and nitrogen cycles
substrates in the soil is increased that may result in a stimulation of soil microbial turnover processes and an improvement of environmental conditions for denitrification via increased soil anaerobiosis and C substrate provision [17,18].
However, results from CO2 enrichment experiments are highly controversial [18]: an earlier meta-analysis on CO2-effects on denitrification enzyme activity (DEA), predominantly conducted with herbaceous systems, reported a decrease at increasing CO2 levels. However, as already pointed out earlier, one may on the one hand question the DEA approach and on the other hand needs to discuss if the proposed mechanism that finally leads to reduced denitrification rates – that is, increased immobilization of Nr in the plant biomass and thus a decrease in mineral N and NO3 in the soil – may also be valid for highly fertilized agricultural systems. Recent reports on changes in soil N2O emissions from fertilized soils under elevated atmospheric CO2 concentrations strongly indicate that N2O emissions are likely to increase, thereby partly off-setting the greenhouse gas benefits from increased plant CO2 fixation [32,33,34]. A so far rarely considered side effect of increased C substrate availability under elevated CO2 is its potential consequence for subsoil denitrification. A major fraction of agricultural surplus Nr is leached to the groundwater. Nitrate can pass the subsoil without being further reduced by denitrification since the existing denitrifier community is strongly C substrate limited. If under future climate conditions and elevated atmospheric CO2 concentrations easily degradable C substrates are increasingly leached to the subsoil [35], more NO3 may get denitrified, thereby decreasing the NO3 load of the groundwater and increasing subsoil N2O and N2 production. Finally, also changes in atmospheric O3 concentration may indirectly affect soil denitrification. Again it is the plant–soil link being of importance here and specifically the effect of tropospheric O3 on plant health, biomass growth and litter quality. Based on a modeling study it has been estimated that owing to plant ozone damage the global gross primary production in 2100 is decreased by 8–23% as compared to 1901 [36]. Associated changes in rhizodeposition of C substrates and litter quality may also affect denitrification in soils and associated N2O emissions, even though this mechanism may be of little importance as compared to other climate change effects.
nonlinear interrelated and rarely investigated in multifactorial field and laboratory experiments. However, it is obvious that the plant–soil link and its importance as controller of soil N and C substrate availability needs to be further stressed and that single site observations need to be supplemented by a more holistic view on denitrification and N2O emissions at landscape scales. This will require a stronger linkage of modeling and measuring activities, specifically since measurements of denitrification and N2 production by denitrification are still scarce but needed for a thorough understanding of the variability of the denitrification process as affected by environmental constrains and, thus, for an improved numerical description of denitrification in process models. It still remains an open question if climate change effects – that is, changes in precipitation, temperature and atmospheric CO2 concentrations – on denitrification and soil N2O emissions may not be overridden by changes in agricultural management practices, for example, in the frame of adaptation measures to climate change.
Acknowledgements We thank the German Science Foundation (Deutsche Forschungsgemeinschaft) for generously funding the work of Michael Dannenmann through contract number DA 1217/2-1. Part of this work is a contribution to the EU funded integrated project NitroEurope.
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Conclusions It is apparent that the existing knowledge how denitrification and associated N2O emissions from agricultural sources may change in a changing climate is limited. The reason for this is that mechanisms leading to changes in denitrification under future environmental conditions are Current Opinion in Environmental Sustainability 2011, 3:389–395
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Current Opinion in Environmental Sustainability 2011, 3:389–395