The global nitrogen cycle in the twenty-first centuryeebweb.arizona.edu/faculty/saleska/SWES.410.510/Readings/Fowler … · The nitrogen cycle in the oceans i ncluding BNF and denitrifica-tion

, 20130164, published 27 May 2013368 2013 Phil. Trans. R. Soc. B VossBouwman, Klaus Butterbach-Bahl, Frank Dentener, David Stevenson, Marcus Amann and MarenAlan Jenkins, Bruna Grizzetti, James N. Galloway, Peter Vitousek, Allison Leach, Alexander F. David Fowler, Mhairi Coyle, Ute Skiba, Mark A. Sutton, J. Neil Cape, Stefan Reis, Lucy J. Sheppard, The global nitrogen cycle in the twenty-first century

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ReviewCite this article: Fowler D et al. 2013 Theglobal nitrogen cycle in the twenty-first

century. Phil Trans R Soc B 368: 20130164.

http://dx.doi.org/10.1098/rstb.2013.0164

One contribution of 15 to a Discussion Meeting

Issue ‘The global nitrogen cycle in the

twenty-first century’.

Subject Areas:environmental science

Keywords:nitrogen fixation, denitrification, emissions,

deposition, global budgets

Author for correspondence:David Fowler

e-mail: [email protected]

& 2013 The Author(s) Published by the Royal Society. All rights reserved.

The global nitrogen cycle in the twenty-first century

David Fowler1, Mhairi Coyle1, Ute Skiba1, Mark A. Sutton1, J. Neil Cape1,Stefan Reis1, Lucy J. Sheppard1, Alan Jenkins1, Bruna Grizzetti2, JamesN. Galloway3, Peter Vitousek4, Allison Leach3, Alexander F. Bouwman5,Klaus Butterbach-Bahl6, Frank Dentener7, David Stevenson8, Marcus Amann9

and Maren Voss10

1NERC Centre for Ecology and Hydrology, Penicuik, UK2CNRS, University Pierre et Marie Curie (UPMC), Paris, France3Department of Environmental Sciences, University of Virginia, Charlottesville, VA, USA4Department of Biogeochemistry, Stanford University, Stanford, CA, USA5PBL Netherlands Environmental Assessment Agency, Utrecht University, Utrecht, The Netherlands6Institute for Meteorology and Climate Research (IMK-IFU), Garmisch-Partenkirchen, Germany7European Commission, Joint Research Centre, Ispra, Italy8School of Geosciences, University of Edinburgh, Edinburgh, UK9International Institute for Applied Systems Analysis (IIASA), Laxenburg, Austria10Leibniz Institute of Baltic Sea Research, Warnemünde, Rostock, Germany

Global nitrogen fixation contributes 413 Tg of reactive nitrogen (Nr) to terrestrialand marine ecosystems annually of which anthropogenic activities are respon-sible for half, 210 Tg N. The majority of the transformations of anthropogenicNr are on land (240 Tg N yr

21) within soils and vegetation where reduced Nrcontributes most of the input through the use of fertilizer nitrogen in agri-culture. Leakages from the use of fertilizer Nr contribute to nitrate (NO3

2) indrainage waters from agricultural land and emissions of trace Nr compoundsto the atmosphere. Emissions, mainly of ammonia (NH3) from land togetherwith combustion related emissions of nitrogen oxides (NOx), contribute100 Tg N yr21 to the atmosphere, which are transported between countriesand processed within the atmosphere, generating secondary pollutants,including ozone and other photochemical oxidants and aerosols, especiallyammonium nitrate (NH4NO3) and ammonium sulfate (NH4)2SO4. Leachingand riverine transport of NO3 contribute 40–70 Tg N yr

21 to coastal watersand the open ocean, which together with the 30 Tg input to oceans fromatmospheric deposition combine with marine biological nitrogen fixation(140 Tg N yr21) to double the ocean processing of Nr. Some of the marine Nris buried in sediments, the remainder being denitrified back to the atmosphereas N2 or N2O. The marine processing is of a similar magnitude to that in terres-trial soils and vegetation, but has a larger fraction of natural origin. The lifetimeof Nr in the atmosphere, with the exception of N2O, is only a few weeks, while interrestrial ecosystems, with the exception of peatlands (where it can be 102–103

years), the lifetime is a few decades. In the ocean, the lifetime of Nr is less wellknown but seems to be longer than in terrestrial ecosystems and may representan important long-term source of N2O that will respond very slowly to controlmeasures on the sources of Nr from which it is produced.

1. IntroductionThe global nitrogen cycle is central to the biogeochemistry of the Earth, withlarge natural flows of nitrogen from the atmosphere into terrestrial andmarine ecosystems through biological nitrogen fixation (BNF), in which the lar-gely un-reactive molecular nitrogen is reduced to ammonium compounds. Thefixed nitrogen is subsequently transformed into a wide range of amino acidsand oxidized compounds by micro-organisms, and finally returned to the

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atmosphere as molecular nitrogen through microbial denitrifi-cation in soils, fresh and marine waters and sediments [1]. Theinitial fixation steps generate compounds containing reactivenitrogen (Nr, which includes NH3, NH4, NO, NO2, HNO3,N2O, HONO, PAN and other organic N compounds) which,in addition to their role in biological and ecosystem function interrestrial and marine ecosystems, also become widely distribu-ted in the atmosphere and cryosphere as described in paperswithin this issue. The presence of Nr in these components ofthe Earth system provides a tracer of the biogeochemical cascadeof Nr through the environment as discussed by Galloway et al.[2]. In the atmosphere, NOx plays a key role in the photochemi-cal production of ozone and other key oxidants and radicalspecies [3] and is closely coupled to the oxidizing capacity ofthe atmosphere [4]. Similarly, the emission of N2O followingdenitrification plays a key role in the radiative balance of theEarth and in the chemistry of the ozone layer in the stratosphere,where N2O is destroyed by photolysis [3].

In the absence of human influences, BNF and the pro-duction of NOx by lightning would be the only sources ofnew Nr in the environment.

The supply of Nr is essential for all life forms, and increasesin nitrogen supply have been exploited in agriculture toincrease the yield of crops and provide food for the growingglobal human population. It has been estimated that almosthalf of the human population at the beginning of the twenty-first century depends on fertilizer N for their food [5]. Thenitrogen applied in agriculture is derived from atmosphericsources, but unlike the natural process of N fixation, most agri-cultural N is fixed industrially by the Haber–Bosch process [6],the remainder by nitrogen-fixing crops [7]. Nitrogen fixation bythe Haber–Bosch process also provides Nr for other industrialapplications, including explosives. Overall, the fixation ofnitrogen through Haber–Bosch (120 Tg N yr21) in 2010 wasdouble the natural terrestrial sources of Nr (63 Tg N yr

21).Atmospheric nitrogen is also fixed unintentionally throughhuman activities, especially during the combustion of fossilfuels by internal combustion engines, and industrial activity,including electricity production.

The overall magnitude of anthropogenic relative to naturalsources of fixed nitrogen (210 Tg N yr21 anthropogenic and203 Tg N yr21 natural) is so large it has doubled the globalcycling of nitrogen over the last century. As nitrogen is amajor nutrient, changes in its supply influence the productivityof ecosystems and change the competition between species andbiological diversity, [8]. Nitrogen compounds as precursors oftropospheric ozone [9] and atmospheric particulate material[10] also degrade air quality. Their effects include increases inhuman mortality [11], effects on terrestrial ecosystems[12,13] and contribute to the radiative forcing of global andregional climate [4].

There are therefore important consequences of the humanmodification of the global nitrogen cycle, with benefits infood production and costs due to impacts on human health,biodiversity loss and climate [8].

Knowledge of the global nitrogen cycle is incomplete, buthas developed rapidly over the last two decades, with manynew measurements and improved instrumentation, modelsand process understanding. Galloway et al. [14] documents achronology in the development of the science and showsmajor changes in understanding as knowledge has accumu-lated and the range of processes and compounds involvedhas expanded.

This paper describes the global nitrogen cycle at thebeginning of the twenty-first century, and quantifies each ofthe major terms in the global budget, separating where poss-ible the natural fluxes from those created by anthropogenicactivity. In this way, the contemporary magnitudes of naturaland anthropogenic contributions are identified and con-trasted. The very different sources and chemical propertiesof reduced and oxidized forms of nitrogen are also separated,to illustrate their relative magnitudes.

The overview presents the major fluxes between terres-trial and marine ecosystems and the atmosphere. Thedetailed descriptions of Nr processing within the atmosphereand terrestrial and marine ecosystems are provided bycompanion papers in this issue. The individual papers havebeen written independently and where possible cross refer-ences are made to the common issues, processes and fluxes.The fluxes used in this global summary are largely thosededuced within each of the sectors (terrestrial, marine, etc.)presented in the companion papers.

2. Sources of fixed nitrogen(a) Biological fixation(i) Terrestrial ecosystemsBNF provides an important reference when quantifying theimportance of human inputs to the global nitrogen cycle, asthis is the primary non-anthropogenic input of Nr [15]. Thequantity from lightning, discussed later, is over an order ofmagnitude smaller than any of the estimates of BNF, albeit oflarge importance for the formation of ozone in and the main-tenance of the oxidation capacity of the global atmosphere.The process of BNF was identified in the late nineteenth cen-tury and has since become a focus of ecological interest.There remain important limitations in understanding, includ-ing why, with such a widespread capability in ecosystems tofix atmospheric N2, organisms do not fix more N, when thebenefits would provide advantages over competitor organismsthat lack a nitrogen-fixing capability. For many ecosystems,the availability of Nr in soils clearly down-regulates BNF, soperhaps the widespread application of Nr on farmland anddeposition to semi-natural land has decreased non-agriculturalBNF (as assumed in [1]). Current knowledge of processes andcontrols has not provided unambiguous answers to thesequestions. The review in this issue by Vitousek et al. [16] pro-vides an estimate of annual pre-industrial BNF in terrestrialecosystems of 58 Tg N, within a range of 40–100 Tg, and adiscussion of current understanding and limitations. Theuncertainty range is large and reflects the difficulty inestimating the component terms. The value deduced by Vitou-sek et al. [16] is smaller than many published estimates,especially earlier values suggesting pre-industrial BNF in therange 100–290 Tg N yr21. However, this new calculation isbased on estimates of hydrological losses of nitrogen from ter-restrial systems and the fraction of nitrogen denitrified instreams and rivers may be overestimated.

(ii) Marine ecosystemsThe nitrogen cycle in the oceans including BNF and denitrifica-tion is reviewed by Voss et al. [17]. Estimates of both termssuggest either an excess of denitrification over BNF or anapproximate balance of the two [18]. However, uncertainties in

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Table 1. Global nitrogen fixation prior to human influence on agriculturalBNF and before the industrial revolution.

pre-industrial terrestrial BNF 58 Tg N yr21

marine BNF 140 Tg N yr21

lightning fixation of nitrogen 5 Tg N yr21

total global natural annual sources of Nr 203 Tg N yr21


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the individual terms preclude a clear consensus. The underpin-ning control mechanism over the balance between BNF anddenitrification at large scales has not been demonstrated, butphosphorus and iron availability may be important contributors.Covering three quarters of the Earth’s surface, oceans clearlydominate the surface area and even relatively small fluxes perunit area have the potential to make a substantial contributionto total N fluxes between the atmospheric N2 reservoir andmarine Nr. One of the key uncertainties in the rates of marineBNF is spatial variability, since these are coupled to the supplyof other nutrients required for the processes, especially phos-phorus and iron whose supply is spatially variable [19]. Largerrates of BNF have been suggested for the Atlantic than the Pacificoceans due to greater nutrient supply [17].

Global marine BNF has been estimated at 125 Tg N annually[20], with a suggested range of 60–200 Tg N [21]. Other recentestimates of marine BNF include values of 140 Tg N yr21 fromCanfield et al. [22] and 145 Tg N yr21 from Galloway et al. [1].It is unclear from the papers how independent the estimatesare and while there are substantial sets of measurements, thesedo not appear to be systematic in covering the spatial and tem-poral scales needed to provide rigorous estimates of variability.

Here, the value for marine BNF argued by Voss [17] of140 Tg N yr21 (+50) has been adopted in the global budget.

(b) LightningIn addition to BNF, nitrogen is also fixed naturally as NOx bylightning, which introduces reactive N to relatively remoteregions of the troposphere.

The process is has been investigated using direct measure-ments and supported by satellite remote sensing of lightningactivity. Global production has been estimated using avail-able data and models, but with substantial uncertainties inpart due to difficulties in up-scaling, by Brasseur et al. [23],who also consider possible effects of climate change onrates of NOx production from lightning. These authors calcu-late an increase in NOx production with increasing globaltemperature in the range 3–12% per 8K. Estimates of theoverall global source strength vary from 2 to 10 Tg N yr21

[24,25], with the more recent values closer to 5 Tg N annually.For this review a value of 5 Tg N yr21 has been adopted.

(c) Global natural sources of reactive nitrogenThe global natural sources of Nr total 203 Tg N (+50Tg N yr21), comprising approximately one-third from terres-trial ecosystems and two-thirds from marine ecosystems,with just 2.4 per cent from lightning (table 1). The uncertaintyin each of the estimated components is very large, reflecting thedifficulty in up-scaling from the available data and the lack ofglobal scale measurements to constrain the values. The marinefixation is the largest contributor to BNF but the factor of twodifference between marine and terrestrial is larger than manyearlier estimates due to the smaller estimate of terrestrial BNF.

(d) Anthropogenic nitrogen fixationAnthropogenic fixation of nitrogen compounds, while uncertain,is better known than natural fixation, in part because the sourcesectors have been subject to more extensive measurements andhave also been subject to greater scientific scrutiny, with regularmonitoring of some large industrial sources. The gases createdare the oxidized nitrogen compounds NO and NO2 from

transport and industry, biomass combustion and reducednitrogen as NH3 from the Haber–Bosch process (figure 1).

Organic nitrogen compounds, for example as amines, arewidely present in the environment and the quantities may besubstantial, as discussed by Cape et al. [26] and Jickells et al.[27]. However, there is no evidence that these compoundsrepresent additional Nr, which is therefore derived from thenatural or anthropogenic BNF or industrial sources of NH3or NOx. The compounds and processes involved in emissionof organic nitrogen and their fluxes into the atmosphere arenot known in sufficient detail to enable the up-scaling forregional or global estimates of their source strength. Thusan important contribution to anthropogenic emissions of Nrmay be missing from the global Nr budgets constructed todate, including the one presented here, but these compoundsare unlikely to represent additional primary sources of Nr.

(i) Biological nitrogen fixation in croplandNitrogen-fixing agricultural crops also contribute substantialquantities of Nr to soils. In a recent detailed review of agricul-tural BNF, Herridge et al. [28] compiled data from directmeasurements of BNF from a range of agricultural systemsglobally and up-scaled annual nitrogen fixation rates usingland-use and cropping data to calculate a global total. The cur-rent global BNF from agricultural crops and grazed savannahsestimated by Herridge is 50–70 Tg N yr21. For the purpose ofsummarizing the data, a central value of 60 Tg N yr21 as theglobal annual Nr flux for BNF in cropland has been used inthis review. The value of BNF for cropland is very close tothe pre-industrial BNF and is indistinguishable within the cur-rent range of uncertainty.

It is helpful to separate the oxidized and reduced sources ofNr, as these are produced by very different sources and haveeffects and pathways through the environment which also differ.

(ii) Oxidized nitrogenThe main process creating oxidized Nr compounds is com-bustion within internal combustion engines and industrialpower plants, especially for electricity supply. It is importantto distinguish between the creation of Nr and emission to theatmosphere. The focus in this section is on the creation of Nrbut the subject of most research in this field has been on emis-sions to the atmosphere, as this is the driver of many of theenvironmental issues involving NOx. The compounds gener-ated are mainly NO and NO2, which arise from oxidation ofatmospheric N2, and there is an additional contribution fromnitrogen compounds in the fuel, derived from sequestrationat the time the organic deposits were laid down [3]. Biomassburning represents an important global contribution of Nr tothe atmosphere, but this is primarily from nitrogen in the fueland does not represent new Nr fixation. Emissions of NOxhave been extensively measured both directly from sources


ocean

lightning

combustion

BNF

fertilizer production

BNF 30 ± 10%

60 ± 30%

140 ± 50%

annual fixation Nr 413 Tg N yr–1

anthropogenic 210 Tg N yr–1

agriculturalBNF

120 ± 10%

land

5 ± 50%

58 ± 50%

Figure 1. Global nitrogen fixation, natural and anthropogenic in both oxidized and reduced forms through combustion, biological fixation, lightning and fertilizerand industrial production through the Haber – Bosch process for 2010. The arrows indicate a transfer from the atmospheric N2 reservoir to terrestrial and marineecosystems, regardless of the subsequent fate of the Nr. Green arrows represent natural sources, purple arrows represent anthropogenic sources.


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and also derived from satellite remote sensing to estimateglobal biomass emissions [29].

Emissions of nitric oxide (NO) from soils also contribute sig-nificantly to atmospheric emissions, but this is not an additionalsource of Nr as it results from the microbial transformations ofexisting Nr in soil, through nitrification and denitrification[30,31]. The processes leading to soil emissions are discussedby Butterbach-Bahl et al. [32] and Pilegaard [33]; while emissionrates per unit land area are small (5–50 ng NO-N m22 s21) rela-tive to combustion sources, the emissions occur over large areasof the global agricultural landscapes.

Recent reviews of global emissions show a surprising agree-ment in the overall magnitude of NOx emissions but largerdifferences in specific source contributions, as discussed byGranier et al. [34] and Isaksen et al. [4]. Estimates of globalNOx production and emissions from van Vuuren et al. [35]show values for the year 2000 of approximately 40 Tg N yr21

of which 30 Tg N yr21 is new Nr, the remainder being Nr infuel and in biomass. The 40 Tg N total annual emission com-prises 30 Tg N from fossil fuel combustion, 5 Tg N frombiomass combustion and 5 Tg N from soil NO emissions.Control measures on emissions, despite industrial developmentin parts of Asia and Africa are assumed to reduce emissions bythe middle of the twenty-first century to approximately 30 TgN yr21, but with large uncertainty.

(iii) Reduced nitrogenAnthropogenic fixation of reduced nitrogen (NH3) is throughnitrogen-fixing crops and the main source through theHaber–Bosch process, where H2 and N2 are combined athigh temperatures and pressures in the presence of catalyst[5]. The process was developed during the early years of thetwentieth century and by the first decade of the twenty-firstcentury is producing 120 Tg N as NH3 annually, of which80 per cent is used as agricultural fertilizer and 20 per cent asfeedstock for industrial processes [36]. The fate of nitrogenused in crop production varies, with only 17 per cent consumedby humans in crops, dairy and meat products, the remainderbeing lost to the soils, freshwaters and the atmosphere [37].In the longer term (decades to centuries), most of the Nr isreturned to the atmosphere as N2 following denitrification,

but the lifetime in different reservoirs en route back to theatmosphere allows opportunities for transport into freshwatersor the atmosphere in reactive form. Some of the crop Nr appliedas fertilizer is emitted to the atmosphere as NH3 depending onthe relative balance between ambient NH3 concentrations andthe equilibrium concentration with the NH4

þ concentrationwithin intercellular fluids [38]. The annual total productionthrough the Haber–Bosch process of 120 Tg N as NH3 rep-resents the largest single contribution to Nr formationthrough anthropogenic activity. The use of nitrogen-fixingcrops in agriculture contributes an additional 60 Tg N annually[28], which enters the crop and soil cycling of Nr (figure 2).The total anthropogenic production of Nr in reduced form istherefore 180 (+20) Tg N annually.

The total fixation of atmospheric N2 by natural andanthropogenic activities at the beginning of the twentiethcentury is therefore 413 Tg N of which approximately halfresults directly from human activity. The relative proportionsof reduced and oxidized nitrogen within the anthropogeniccomponent is 85 per cent and 15 per cent, respectively, reveal-ing the dominant role of reduced Nr and the Haber–Boschprocess in the budget of emissions. The components ofglobal Nr production are summarized in figure 1.

3. Trends in Nr emissions during the twenty-firstcentury

Emissions of Nr to the atmosphere are a key driver of atmos-pheric chemistry and composition [10]. Estimates of emissionsof Nr compounds through the twenty-first century are providedby van Vuuren et al. [35] from a range of scenarios, includ-ing the IPCC-SRES and the RCP projections for the 4th IPCCassessments [39]. Emissions of approximately 40 Tg N annuallyof NOx continue through the period 2000–2040, and then declinethrough to 30 Tg N yr21 according to the RCP scenarios by theend of the century, with a gradual increase in uncertainty withtime such that the envelope containing the 25th and 75th percen-tiles stretches from 15 Tg N yr21 to 70 Tg N yr21 by 2100. Thefuture emissions of NOx strongly depend on the assumptionson how activities, especially energy and transport use will


N2O5.5

denitrificationN2 100

NO ¤ NO2 O3 …….

NH4NO3 aerosol

HNO3

atmosphericchemistry

atmospheric transport

burial20

230

100

70

dry and wetdeposition of

oxidized and reduced nitrogen

30

soil/plants crops; livestockforest GPP

biomass burning

leaching and transport to ocean

NH360

burial

t0.5 lifetimeNOyNHx

t0.5 lifetime

aerosols (in clouds and free air)e.g. NO2 + OH HNO3 + NH3 NH4NO3

biomassburning

soils andagriculture

land ocean

NO N2O NH3 N2O

NOxNH3

fossil fuelcombustion

NOx

30(30) 5(4) 60(40) 5(1) 13(7)

70 30

9(0) 5.5(3)

wet and drydeposition

(reduced and oxidized N)

photochemical O3 production and chemistry NO2

NO2

HO2

R–HORO2

NO

NO

OH

RO

O2

O2 O2

O2

RH

sunlight

sunlight

O3

O3

Figure 3. The global atmospheric processing of reactive nitrogen, illustrating the main sources, the main chemical pathways and products and the magnitudes ofthe fluxes (units Tg yr21). The emission flux values in black are the total fluxes while the red values indicate the anthropogenic contribution.

Table 2. A summary of global fluxes of Nr and literature sources.

global nitrogen fluxes Tg N yr21 references

industrial production (fertilizer

100, chemical industry 20)

120 [36,42]

N2 fixation natural ecosystems 58 [16]

N2 fixation by oceans 140 [17]

N2 fixation by agricultural crops 60 [28]

combustion NOx emissions 40 [35]

NO emissions from soils 5 [33,43]

N2O emissions from soils 13 [44]

lightning 5 [24,25]

NH3 emissions from terrestrial

ecosystems into the atmosphere

60 [41]

wet and dry deposition of oxidized

nitrogen to terrestrial surfaces

70 [45,21]

wet and dry deposition of oxidized

to oceans

30 [45,21]

NH3 emissions from oceans (and

volcanoes) to atmosphere

9 [42,39,21]

N2O emissions from the oceans to

atmosphere

5.5 [46]

denitrification to N2 in oceans 100 – 280 [17,47,21]

Nr burial in oceans 20 [17]


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of a freshly produced NH3 molecule to illustrate the point: con-sider a nitrogen atom converted to an NH3 molecule in theHaber–Bosch process, applied as fertilizer to soil and trans-formed many times before finally being returned to theatmosphere as N2. A possible sequence of transformations isillustrated in table 3, with an indication of the environmentaleffects at each stage.

The wide range of issues and processes in which nitrogenis involved are very seldom integrated at a global scale.Instead, the science is described within components such asthe oceans, atmosphere or terrestrial ecosystems, as in the com-panion papers. The issues within each and the approaches todescribe and investigate them are different. The followingthree sections outline approaches and issues for Nr in theatmosphere and terrestrial and marine ecosystems.

(b) Atmospheric processing of Nr(i) Application of chemistry transport modelsEmissions of NOx to the atmosphere from anthropogenicand natural processes have been a focus of interest as these com-pounds play a major role in atmospheric chemistry, especiallyof photochemical oxidants such as ozone (figure 1). The chemi-cal processing has been simulated within chemistry transportmodels (CTM) to quantify transport transformation anddeposition at regional and global scales. Early models of theglobal cycles of oxidized and reduced nitrogen (NOy andNHx) were treated separately [52]. Currently, while almost allglobal atmospheric chemistry models include a representationof NOy chemistry, few models include reduced nitrogen(NHx). In a recent model intercomparison [45], 23 globalmodels included NOy, while only seven included NHx. How-ever, increasingly, models now include combined aerosol andphotochemistry descriptions, as reviewed by Fiore et al. [53].

The first attempts to model the global NHx cycle werebased on a simplified, empirical approach that assumed alimited uptake of NH3 according to (NHx)1.5H0.5SO4.

More recent models describe aerosol equilibrium usingequilibrium modules.

The resolution of global models currently ranges from0.58 � 0.58 to 48 � 58 latitude–longitude and is expected toincrease to 0.258 � 0.258 in the coming years. Also the spatial


Table 3. Illustrating the nitrogen cascade: a possible life cycle of a nitrogen atom following fixation in the Haber – Bosch process to NH3 and its pathwaythrough terrestrial and marine ecosystems and the atmosphere before returning to the atmospheric N2 reservoir. The single N atom contributes en route toeutrophication and acidification of terrestrial and marine ecosystems, and to human health and climate effects.

transformation pathway environmental effect

N2 fixation: Haber – Bosch process

N2! NH3industry energy intensive process, production of CO2

plus all the consequences of the Nr as it

cascades through soils, the atmosphere and

aqueous phases

N fertilizer on crops agricultural lands provision of food for human consumption

NH4 nitrified to! NO3NO in soil! atmosphereoxidation of NO! NO2! HNO3

NO emission from soil to atmosphere and ozone

production during volatile organic compound

degradation

ozone effects on vegetation or human health

[48,49]

aerosol formation, HNO3! NO3 in atmosphere planetary albedo, human health [50]wet þ dry deposition NO3 to

soil! vegetation NO3! R-NH2removal from atmosphere and transfer to plant

biomass

eutrophication, acidification [51]

consumption by herbivores: excreted

as urea R-NH2! CO(NH2)2plant biomass! animal protein! excreted and

returned to soil

eutrophication [51]

urea converted to NH3 in soil and

released to atmosphere

soil to atmosphere flux of NH3 eutrophication

NH3/NH4 uptake by vegetation removal from atmosphere by dry deposition to

vegetation

eutrophication

decomposition R-NH3 ! NH4 vegetation to soil eutrophicationNH4 nitrified to NO3 transferred to

river/estuary/open ocean

soil to ground water! river! ocean eutrophication

ocean uptake in phyto/zooplankton shelf seas to open ocean eutrophication

denitrification in ocean sediments

NO3! N2returns to atmosphere as N2 and N2O climate change


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domain and resolution of regional models has been steadilyimproving typically from 36 km to 12 km grid sizes, andhigher resolutions for limited periods. As we argue belowhigh resolution is important to accurately describe deposition,especially over complex terrain.

(ii) Dry and wet removalRealistic descriptions of wet and dry deposition and thoroughevaluation with high-quality measurements remain a majorweakness of global modelling of the atmospheric Nr cycle.Rain formation, as a part of the hydrological cycle, is one ofthe more difficult parameters in global weather forecasting,and the removal of pollutants by rain formation in cloudsand scavenging below clouds is even more uncertain. Wetremoval is especially uncertain in tropical regions, where rain-fall often occurs on sub-grid model scales in convective stormsand in the mid-latitudes over mountains where orographic wetscavenging processes operate at sub-grid scales for thesemodels [54]. The description of dry deposition often followssimplistic deposition velocity schemes [55], coupled to aland-use database and model generated meteorology. Suchapproaches are some decades behind current understandingof processes for trace gases generally and nitrogen compoundsin particular [56]. In practice, some components of Nr are bothemitted and deposited onto terrestrial surfaces, a processreferred to as bidirectional exchange. The direction of the flux

is determined by the relative concentrations in the vegetationand above canopy air according to a compensation point [38].At present, global CTMs do not consider interactive exchangewith nitrogen pools in vegetation and soils. Moreover, thelack of routine flux measurements of reactive nitrogen com-pounds precludes validation of modelled dry depositionwith field data at any more than three or four locations.

(iii) Uncertainties and constraints on global atmospheric budgetsThe missing processes in the formulation of global atmospherictransport models include: sub-grid deposition; incompletemixing on sub-grid scales (consider, e.g., farm scale NH3 emis-sions and regional sulfate plumes), and emissions from canopyand oceans. To what extent, then, can we trust the outputs ofglobal models for global deposition? Some constraints areoffered by recent satellite observations. For example, NO2observations from Sciamachy instruments [57] provide con-straints on NOx emissions, and thus to some extent also ondeposition. Underestimates of NOx emissions over Chinawere reported by Van Noije et al. [58]. Very recent NH3 satelliteobservations indicate in some cases missing hot spots of NH3emissions [59] but have not so far been used to constrain theglobal NH3 cycle.

The global models cannot provide much of the regio-nal deposition detail; nevertheless, there was a recentcomparison by Dentener et al. [45] of 21 global models with



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wet deposition measurements in North America and Europe.They demonstrate reasonable performance in southeast Asia,but problems in Africa, South Asia and South America. Alack of high-quality data in the latter regions still precludesclear conclusions on model performance with regard to depo-sition. Mass conservation requires that global emissions equalglobal deposition; until higher accuracy measurements withsufficient spatial coverage become available, the global atmos-pheric nitrogen cycle will be associated with uncertainties inthe order of 30–50%.

The reactive gases are processed rapidly and lead tothe formation of O3 and other photochemical oxidants andsecondary inorganic and organic aerosols [9] during thephotochemical degradation of volatile organic compounds.The NH3 is either dry deposited back to the surface orincorporated in aerosol, either as NH4NO3 or, if SO2 is pre-sent in significant quantities, as (NH4)2SO4. The lifetimeof these short-lived compounds is typically a day or two,being longer as aerosol, which relies on wet scavenging forthe majority of the removal process. The models are able tocapture the global distribution of ozone in the troposphereat the surface quite well [9]. However, at regional scalesthere remain considerable problems reproducing thetrends in surface concentration changes through the last fewdecades [60].

The atmospheric processing of reduced nitrogen com-pounds has received much less attention than oxidizednitrogen, but is now incorporated in many regional [61,62]and global models [45]. Projected trends in emissions of NH3make this the dominant component of emissions through thiscentury, and one which is likely to increase with temperature,owing to the coupling between temperature and the gas andliquid phase partitioning [63].

Emissions of N2O from soil during denitrification [64,65]have a longer atmospheric lifetime at approximately 100 years,relying on photolysis in the stratosphere for its removal.

The net flow of Nr from the land into the oceans and theatmosphere is unsurprising given the mobility of Nr in soilwater and transfer to the oceans by rivers [66] and the advec-tion of the atmospheric Nr by wind over coastlines. There isalso transfer within the terrestrial landscape from the Nrhot spots to areas with small Nr inputs from farming andindustry. These include large areas of semi-natural land(e.g. heathlands, forest and mountains) but also includesmall areas embedded within intensively used parts of thelandscape such as nature reserves or unmanaged land sur-rounded by industrial areas or farmland. These are thecomponents of the landscape showing some of the largesteffects of Nr deposition, including widespread changes inflora or the emission of trace Nr species [67,68].

(c) Terrestrial processing of NrMost of the anthropogenic perturbation of the nitrogen cycleis driven by activity on land, both through the use of Nr inagriculture and through industry, electricity generation andtransport. Although the initial steps in much of the industrialand transport Nr production lead directly to emissions to theatmosphere, the relatively short residence times of oxidizedNr compounds lead to rapid return of NOy and NHx to theEarth’s surface as deposition. The geographical distributionof Nr source areas leads to two-thirds of global atmospheric

Nr inputs to terrestrial surfaces and one-third onto marinesurfaces [1] (figure 2).

To date, the most detailed assessment of terrestrial proces-sing and fluxes of Nr on a regional basis has been providedwithin the European Nitrogen Assessment (ENA) [69]. Assess-ments for other regions and the global scale have yet to becompleted. Earlier analyses by Galloway et al. [1] provide esti-mates of the global transformations and flow of Nr throughterrestrial ecosystems and into the atmosphere and oceans.These two syntheses are broadly consistent in showing thedominant role of terrestrial processing of Nr (figure 4).

The analysis within the ENA allows the relative scales ofthe different activities to be compared. The cycling of Nrwithin agriculture through fertilizer inputs to cropland andthe flow of Nr through livestock and back into soils revealsthe central role of processes, with soils as the principlelocation of Nr transformations and ultimately the main siteof denitrification back to N2. If we fully understood these pro-cesses globally and knew the magnitude of the fluxes andtheir spatial distribution globally, the uncertainties in globalbudgets would be greatly reduced. Simply ranking the mag-nitudes of the fluxes in the European N cycle by size showsthat of the 35 fluxes quantified in figure 4, fluxes from or tosoils comprise the top 15 and compromise most of the Nr pro-cessing within Europe. The processing and leaching of Nr incatchments and the export to coastal seas are described byHowarth et al. [70] and Billen et al. [66]. The long-termtrends in nitrate in the Thames in the UK (between 1868and 2008) reveal the magnitude of the change in countriesthat industrialized early [71].

(d) Processing Nr in the oceansThe cycling and processing of Nr within the oceans hasreceived much less attention, but recent reviews have identifiedthe major components and issues [17,21,72]. BNF in oceans is avery large component at 140 Tg N annually, among the largestin the global budget (figure 2), and is subject to more uncer-tainty than most of the terrestrial terms owing to the lack ofmeasurements. The net transfer of Nr to oceans from terrestrialsystems is processed (figure 5) and some is buried in organicsediments while the remainder is denitrified and returned tothe atmosphere as either N2 or N2O. The fraction of the Nrreturned to the atmosphere as N2O is spatially very variable,and quantifying the global N2O source from ocean sources,while subject to considerable uncertainty, is a substantialterm, estimated by Duce et al. [21] to be 5.5 Tg N yr21 asN2O, and represents approximately 30 per cent of the emissionflux of N2O, from the ocean [17]. A source strength of this mag-nitude may offset as much as two-thirds of the enhancement ofthe ocean sink for CO2 owing to nitrogen fertilization of theoceans [21].

The global flow of N in oceans is coupled to the wider cir-culation patterns, and especially the ocean conveyor systemtransporting solutes southwards at the ocean floor in the Atlan-tic ocean towards the Antarctic circumpolar current and fromthere northwards into the Indian and Pacific oceans. The time-scales of transport are long relative to other timescales of Nrprocessing, with Atlantic water residence times of approxi-mately 180 years, exceeding the time since industrialcontributions to the global nitrogen cycle began. Thus, theocean transport timescales are long relative to the processingtimes in the ocean and much longer than atmospheric transport


9.7

3.4 3.8

0.3

0.2

3.811.2

17.65.8

1.0

11.8

8

2.3

3.1

0.4

3.5

2.4

5

3.1

3.613.62.4

1.410.2

2.1 4.5 6.2

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0.1

4.62.7

0.6

1.8

4.5

humannutrit.

agricultsoils

livestockfarming

atmospheric N2 pool

cropproduction

Atmdepos

net import offood and feed

cropN2 fix

fertilizers

NH3,NOxand N2Oemission

denitrifi-cation

N2 fixindustry

andtraffic

export byrivers tothe sea

net atmosphericexport

semi-natsoils

natN2 fix

wood exp.

atmospheric NH3, NOx, N2O

wwt

leachgand

runoff

landfill

6

4

1

3

5

7

2

2

Figure 4. The nitrogen cycle within the EU-27 showing natural fluxes (Tg N) in green, (intentional) anthropogenic fluxes as blue and (unintentional) as orangeadapted from the ENA [69]. The terrestrial component of the cycle is delineated by the dotted ellipse.


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or land to ocean transport timescales, by several orders of mag-nitude. A consequence of these timescales is large regional andvertical variability in concentrations of Nr in oceans. Peakvalues occur in the coastal zones, which are strongly influencedby terrestrial outflow, and at the larger scale the peak valuesoccur in polar and bottom water and minimum values occurin tropical surface waters, where available Nr is quickly assimi-lated. A consequence of the large spatial variability, includingthe coastal zones, is that hot spots of accumulation and proces-sing are an important feature, resulting in substantial emissionsof N2O from relatively small areas of the ocean, which have notbeen measured.

(e) Fate and residence time of Nr in the atmosphere,and terrestrial and marine ecosystems

The ultimate fate of Nr fixed naturally and from humanactivity is as N2 returned to the atmosphere. However,during the pathway from production of Nr to its ultimatefate, it presents the potential for effects on terrestrial ecosys-tems, human health and climate [8], as illustrated in table 2.The effects occur in part through sequestration in biomass,the largest storage term in the global processing of Nr.There are also much smaller but potentially significantstores of Nr in inorganic form in aquifers, ice sheets and peat-land, all of which have residence times of century tomillennia. In this section, these residence times are briefly dis-cussed to indicate probable timescales for recovery fromeffects of human modification of the global nitrogen cycle.

(i) AtmosphereThe highly reactive compounds (NO, NO2, HNO3, NH3 andaerosol NH4 and NO3) have atmospheric lifetimes rangingfrom a few hours (NH3 and HNO3) to aerosols, which havelifetimes owing to removal by precipitation of a few days toa week. The greenhouse gas N2O has an atmospheric lifetimeof approximately 100 years and relies on photolysis in thestratosphere for oxidation to NO before it can be scavengedfrom the atmosphere by wet and dry deposition. Thus,except for effects of N2O, reduction in emissions of Nr tothe atmosphere would lead to a rapid reduction in most com-pounds in air and effects on climate and human health wouldcease after a period of a few weeks.

(ii) Terrestrial ecosystemsIn terrestrial ecosystems, the additional Nr leads to enhancedquantities of Nr cycling between vegetation and the soil, withthe main removal process being leaching as NO3 to groundwater and denitrification as N2 back to the atmosphere. Plantand soil communities have evolved to sequester and recycleNr as it is an essential and often limiting nutrient [73]. In tropi-cal ecosystems, Nr is rapidly cycled, maintaining small pools ofinorganic Nr in soil. Except for peatlands that store carbon andnitrogen for millennia, the majority of temperate and tropicalecosystems cycle the organic matter and nitrogen sufficientlyquickly and a pulse of additional Nr is lost through denitrifica-tion and fire over a few decades. Thus, it appears that terrestrialecosystems would recover from excess Nr inputs over a periodof less than a century, and probably a few decades, following areduction in Nr input. The species composition of the post-


riverine flux

groundwater

open ocean

deposition

230

30

20

BNF140

burial

4

40–70

N2O5.5

NH39

Figure 5. A simplified schematic of nitrogen cycling in the global oceans (adapted and simplified from [17]). The fluxes are as detailed in the text to be consistentwith figure 2.


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recovery ecosystems, however, may differ substantially fromthe composition prior to enhanced nitrogen deposition. Insome semi-natural ecosystems, active management has beenused to remove Nr from top soils, to restore low fertility plantcommunities and accelerate the recovery process [74].

Regional changes in biodiversity as a consequence of Nrdeposition have been observed across Europe [12,51], and itis likely that the other major regions of enhanced Nr depositionwill show similar trends. The primary productivity of theseecosystems may also be changing as many semi-natural ecosys-tems are nitrogen limited. The additional biomass sequesteredas a consequence of the Nr deposition has been estimated forforests [75,76]. These studies consistently show that forests inareas of enhanced Nr deposition have been growing morerapidly in recent decades, an effect that has been shown to bea consequence of Nr deposition rather than changes in climateor forestry practice [76]. To date, the data from long-term Nraddition field experiments show increases in productivity andnitrogen enrichment of vegetation and surface soils [73]. In con-trast to the networks of flux monitoring stations for terrestrialcarbon exchange, there are no systematic measurements ofnitrogen sequestration in terrestrial ecosystems, even thoughthe sequestration of Nr is one of the driving variables forcarbon sequestration [76]. Carbon sequestration in terrestrialecosystems is clearly coupled to nutrient supply, especially ofnitrogen and phosphorus [73,77].

(iii) Marine ecosystemsAs with terrestrial ecosystems, there are no systematic measure-ments of nitrogen sequestration in the oceans and, again, carbonsequestration is clearly coupled to nutrient supply. The time-scales of transport and Nr sequestration in the ocean aresubstantially longer than those in the atmosphere and in themajority of terrestrial ecosystems. Furthermore, the anoxicbottom waters are accumulating Nr, estimated by Gallowayet al. [1] to be approximately 4 Tg N yr21 and from whichN2O is generated, which may represent an important long-term global problem. Thus, marine Nr reservoirs may proveto be more important in the longer term, as terrestrial andatmospheric reservoirs appear to recover more rapidly.

( f ) Nitrogen sequestrationThe global sequestration of Nr has been quantified using eco-system models as described by Zaehle [78], who estimatedterrestrial Nr sequestion of 27 Tg N yr

21 between 2001 and2012. This may be compared with a rough estimate madeusing the annual terrestrial global C sequestration [79] andChurkina et al. [80], assuming a C/N ratio. Adopting thisvery simplistic approach for a C/N ratio of 30, terrestrial Nsequestration would be 75 Tg N yr21 and would vary between50 and 100 Tg N for C/N ratios between 25 and 50, effectivelyspanning the range of observed C/N values, and similar tothe value of 60 Tg N estimated by Galloway et al. [1] andsignificantly larger than the estimate by Zaehle [78].

The quantity of Nr sequestered in ice is discussed byWolff [81] and estimated at 260 Tg N. Although this quantitymay seem large, it represents accumulation over a very longtime and the annual inputs are small.

5. Closing remarksThe global nitrogen cycle has been greatly modified byhuman activity, and among the key biogeochemical cycleson which ecosystems depend for their sustainability the nitro-gen cycle is the most perturbed on the planet. Manycomponents of the global budget have been quantified overthe last 20 years, and the contrast between knowledge ofthe major fluxes in 1982 [82] and the descriptions of Nrcycling in ocean and terrestrial ecosystems and the atmos-phere presented in this issue are striking. However, manyfluxes are subject to large uncertainties and require extensivemeasurements to constrain the current range of values, a con-clusion similar to that reached by Stewart [83] following thediscussion meeting on the nitrogen cycle in 1981.

The consequences of human intervention in the nitrogencycle include the obvious benefits for food security withapproximately half of the global human population depen-dent on the increased yields of agricultural crops owing tofertilizer nitrogen usage, and substantially enhanced carbonsequestration resulting from Nr deposition to forests andother semi-natural terrestrial ecosystems [76]. The negative



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consequences of human fixation of nitrogen are also substan-tial and include the Nr contribution to effects of aerosols andozone on human health [84], terrestrial ecosystem losses inbiodiversity owing to Nr deposition at regional scales [85]and effects of Nr on climate described by Erisman et al. [8].The effects on terrestrial ecosystems and the atmospherehave been subject to much more control than effects inmarine ecosystems, which are the destination for a substantialfraction of Nr applied to terrestrial ecosystems. The transfer of80–100 Tg Nr from land to oceans annually representsapproximately half of anthropogenic emissions and com-prises 50–70 Tg N leached from land to the ocean infreshwaters and the deposition of an additional 30 Tg Nfrom the atmosphere on oceans. There are very few controlmeasures in place to reduce the transfer of Nr to oceansand no international measures to regulate the overall effectsof perturbation of the nitrogen cycle by human activity.

The Malthusian concept of food security being compro-mised by population growth has an interesting resonance inthe context of the human influence on the nitrogen cycle. Theproblem of growing sufficient food to date has been largelysolved by agricultural science, and the supply of nitrogen as

fertilizer from the Haber–Bosch process has been a substantialcontributor to increased productivity. However, the amountsof nitrogen applied have not been sufficiently constrained toprevent widespread leakage to freshwaters and the atmos-phere, with consequent effects on human health, biodiversityand climate. The Nr injected into the environment from indus-try and transport, largely combustion sources, further increasesthe scale and range of effects. The irony here is that the societalneeds for use of Nr for food have been satisfied by inefficientnitrogen use in agriculture, compromising other ecosystem ser-vices. To date, there has been much more effective regulation ofNr from combustion and transport sectors than Nr use in agri-culture. Many of the accumulated effects of Nr are notattributable to any specific country or region, and the oceansmay represent an important long-term problem as the marineNr store gradually releases N2O to the atmosphere.

The authors gratefully acknowledge support from the EU researchprojects ACCENTþ, PEGASOS and ECLAIRE for the preparationof this paper. The constructive comments of anonymous reviewersare also appreciated.

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The global nitrogen cycle in the twenty-first centuryIntroductionSources of fixed nitrogenBiological fixationTerrestrial ecosystemsMarine ecosystems

LightningGlobal natural sources of reactive nitrogenAnthropogenic nitrogen fixationBiological nitrogen fixation in croplandOxidized nitrogenReduced nitrogen

Trends in Nr emissions during the twenty-first centuryProcessing and distributing Nr through the Earth systemThe nitrogen cascadeAtmospheric processing of NrApplication of chemistry transport modelsDry and wet removalUncertainties and constraints on global atmospheric budgets

Terrestrial processing of NrProcessing Nr in the oceansFate and residence time of Nr in the atmosphere, and terrestrial and marine ecosystemsAtmosphereTerrestrial ecosystemsMarine ecosystems

Nitrogen sequestration

Closing remarksThe authors gratefully acknowledge support from the EU research projects ACCENT+, PEGASOS and ECLAIRE for the preparation of this paper. The constructive comments of anonymous reviewers are also appreciated.References

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The global nitrogen cycle in the twenty-first centuryeebweb.arizona.edu/faculty/saleska/SWES.410.510/Readings/Fowler … · The nitrogen cycle in the oceans i ncluding BNF and denitrifica-tion