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Synthesis and review: Tackling the nitrogen management challenge: from global to local

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2016 Environ. Res. Lett. 11 120205

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Environ. Res. Lett. 11 (2016) 120205 doi:10.1088/1748-9326/11/12/120205

EDITORIAL

Synthesis and review: Tackling the nitrogenmanagement challenge:from global to local scales

StefanReis1,2,Mateete Bekunda3, ClareMHoward1,4, NancyKaranja5,WilfriedWiniwarter6, XiaoyuanYan7,Albert Bleeker8 andMarkASutton1

1 NERCCentre for Ecology&Hydrology, Bush Estate, Penicuik, EH26 0QB,UK2 University of ExeterMedical School, Knowledge Spa, Truro, TR1 3HD,UK3 International Institute of Tropical Agriculture (IITA-Tanzania), c/oAVRDC—TheWorldVegetable Center, POBox 10Duluti, Arusha,

Tanzania4 University of Edinburgh, School of Geosciences, Institute of Geography, Drummond Street, Edinburgh EH8 9XP,UK5 University ofNairobi, LandResourceManagement andAgricultural Technology, POBox 30197 -00100,Nairobi, Kenya6 International Institute for Applied SystemsAnalysis, Schlossplatz 1—A-2361 Laxenburg, Austria7 Institute of Soil Science, Chinese Academy of Sciences, No.71 East Beijing Road,Nanjing, People’s Republic of China8 Netherlands Environmental Assessment Agency (PBL), Antonie van Leeuwenhoeklaan 9, 3721MABilthoven, TheNetherlands

E-mail: srei@ceh.ac.uk

AbstractOne of the ‘grand challenges’ of this age is the anthropogenic impact exerted on the nitrogen cycle.Issues of concern range from an excess offixed nitrogen resulting in environmental pressures for someregions, while for other regions insufficientfixed nitrogen affects food security andmay lead to healthrisks. To address these issues, nitrogen needs to bemanaged in an integrated fashion, at a variety ofscales (fromglobal to local). Suchmanagement has to be based on a thorough understanding of thesources of reactive nitrogen released into the environment, its deposition and effects. This requires acomprehensive assessment of the key drivers of changes in the nitrogen cycle both spatially, at thefield, regional and global scale and over time. In this focus issue, we address the challenges ofmanagingreactive nitrogen in the context of food production and its impacts on human and ecosystemhealth.In addition, we discuss the scope for and design ofmanagement approaches in regionswith toomuchand too little nitrogen. This focus issue includes several contributions from authorswho participatedat theN2013 conference inKampala inNovember 2013, where delegates compiled and agreed uponthe ‘Kampala Statement-for-Action onReactiveNitrogen in Africa andGlobally’. These contributionsfurther underline scientifically the claims of the ‘Kampala Statement’, that simultaneously reducingpollution and increasing nitrogen available in the food system, by improved nitrogenmanagementoffers win-wins for environment, health and food security in both developing and developedeconomies. The specificmessages conveyed in theKampala Statement focus on improving nitrogenmanagement (I), including the reduction of nitrogen losses from agriculture, industry, transport andenergy sectors, as well as improvingwaste treatment and informing individuals and institutions (II).Highlighting the need for innovation and increased awareness among stakeholders (III) and theidentification of policy and technology solutions to tackle global nitrogenmanagement issues (IV),this will enable countries to fulfil their regional and global commitments.

1. Introduction

Nitrogen (N) is one of the five major chemicalelements that are necessary for life, but while nitrogenis the most abundant of these, more than 99.9% of itoccurs as molecular di-nitrogen (N2) and is notdirectly accessible to most organisms. In order to

break the triple bond connecting the two nitrogenatoms, and to ‘fix’ nitrogen into usable forms, asubstantial amount of energy is required, eitherthrough high-temperature processes (e.g., duringcombustion or in the Haber–Bosch process ) or bybiological nitrogen fixation (BNF), through the actionof certain specialized bacteria. By contrast, most living

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organisms are restricted to using the result of suchfixation processes: reactive nitrogen (Nr) compounds.These include inorganic forms of nitrogen such asammonia (NH3), ammonium ( )+NH ,4 nitric oxideand nitrogen dioxide (NO andNO2, collectively NOx),nitric acid (HNO3), nitrous oxide (N2O), and nitrate( )-NO ,3 as well as organic compounds like urea (CO(NH2)2), amines, proteins, and nucleic acids.

Releases of Nr into the environment are closelyrelated to agricultural activities and the combustion offossil fuels, or, in other terms, food production andenergy conversion. After they are emitted, Nr com-pounds are subject to chemical transformation andcan remain in the atmosphere, hydrosphere and bio-sphere for extended periods of time, circulatingbetween different environmental media in what hasbeen identified as the ‘nitrogen cascade’ (Gallowayet al 2003) until the energy contained in Nr is even-tually dissipated and it is denitrified back toN2.

While Nr contributes to a wide range of negativeeffects on human and ecosystem health, nitrogen usefor food production is essential to feed the growingworld population, its use thus requires a strategic,integrated management approach (Gallowayet al 2008, Sutton and Howard 2011, Sutton andReis 2011, Sutton et al 2012, 2013a, 2013b, Davidsonet al 2012, Austin et al 2013).

The overall goal of global activities such as theInternational Nitrogen Initiative (INI) is to optimizenitrogen’s beneficial role in sustainable food produc-tion, while aiming to minimize its negative effects onhuman and ecosystem health originating from foodand energy production. In order to achieve this, a bal-ance needs to be established between reducing exces-sive losses of Nr in regions of the world where toomuch nitrogen is used (thereby improving nitrogenuse efficiency, NUE), and increasing the availability

and sustainable use of nitrogen in regions where foodproduction is currently insufficient to sustain popula-tionswith a healthy diet.

These issues were addressed in preparing for theN2013 conference (Kampala, 18–22 November 2013).Four key areas were identified as a focus to achievethese objectives: the role of N in food production, Nmanagement, N impacts on human health, ecosystemsand in relation to climate change, and methods for theintegrated assessment of N management options.Figure 1 illustrates the key questions we have con-sidered in the following sections of this article in rela-tion to the contributions to this focus issue.

2.Nitrogen in food production

2.1.Nitrogen and food securityNatural BNF and lightning supply the biosphere withNr compounds. However, it was already recognizedover a century ago that this is not enough to produceenough food for an increasingly expanding andincreasingly urbanized population, demanding higherintake rates of food production and associated dietaryprotein (Crookes 1898). Chemical and biologicalanthropogenic processes have dominated the creationof extra Nr globally over the last century (Billenet al 2013, Fowler et al 2013, Sutton et al 2013a).Populations in parts of the world (usually industria-lized) where Nr is readily available have used it tointensify and increase agricultural production, providericher andmore diversified diets, all of which improvenutrition compared with the situation in the poorestcounties. For example, increased consumption oflivestock products not only provides high-value pro-tein, but is also an important source of a wide range ofessential micronutrients such as iron and zinc, and

Figure 1. Illustration of four key topic areas detailing the interactions between reactive nitrogen and the environment, and options forthe assessment andmanagement, as framed in preparation for theN2013 conference.

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vitamins such as vitamin A. In contrast, excessiveconsumption of these diets in some world regions hasled to excessive intakes of energy, fat and protein,leading to opportunities to optimize by reducingintake of meat and dairy products in these countries(e.g.Westhoek et al 2014, 2015).

In this focus issue, van Grinsven et al (2015) add tothe debate by examining the case to consider ‘sustain-able extensification’ as an alternative strategy to themore commonly discussed paradigm of ‘sustainableintensification’ (e.g., Garnett and Godfrey 2012). VanGrinsven et al (2015) conclude that, in Europe, exten-sification of agriculture can have positive environ-mental and biodiversity benefits, but at a cost ofreduced yields, if it were combined with adjusted dietswith reduced meat and dairy intake and the externali-zation of environmental costs to food prices. Changesin consumption patterns, for instance due to reducedanimal protein intakes as part of a demitarian diet,may amplify or weaken these effects. Building on thework of Westhoek et al (2014), these authors con-sidered a demitarian scenario, where European meatand dairy intake were halved, linking this also withpotential health benefits associated with avoidance ofexcessive intake.

In contrast, other parts of the world that have lim-ited access to sufficient Nr to replenish crop uptakefrom soils are faced with continuing food scarcity andnutritional insecurity. Per capita food consumption insub-Saharan Africa, for example, was 2238 kcal perday during 2005/2007, being 67% that of the indus-trialized countries (Alexandratos and Bruinsma 2012),while livestock products remain a desired food fortaste, nutritional value and social value. This high-lights the continued challenge to provide access to suf-ficient nitrogen in sub-Saharan African contexts toprevent mining of existing soil N stocks in agriculturalsoils (Vitousek et al 2009). For example, according tothe estimates of Zhou et al (2014) in this focus issue(see section 5.3), nitrogen export from the Lake Vic-toria catchment is substantially larger than imports orestimated N fixation, implying substantial soil Nmining.

In preparing for the N2013 Kampala Conference,it had been anticipated that a discussion on reducingmeat and dairy consumptionwould be highly sensitivein a continent where many citizens do not have accessto sufficient healthy diets. Nevertheless, it was agreedto implement the principles of the Barsac Declaration(Sutton et al 2009), where the catering for the con-ference would provide half the usual amount of meatintake per delegate for such an international con-ference in this region, accompanied by a larger frac-tion of vegetable products. The discussion waswelcomed by both the conference chef and the dele-gates, stimulating significant discussion on what con-stitutes a suitable balanced diet considering bothhealth and environment. The topic was incorporatedinto the ‘Nitrogen Neutrality’ analysis of Leip et al

(2014) (see section 5.1) and provided an importantcomparison with the experience of implementing theBarsac Declaration at the ‘Nitrogen and GlobalChange’ 2011 conference in Edinburgh (Sutton andHoward 2011).

Specifically, the baseline meat serving for a mainmeal (lunch or dinner) in other recent Edinburgh con-ferences had been 180 g per person, which wasreduced in the ‘Nitrogen and Global Change’ con-ference to 60 g per person. By comparison, in Kam-pala, the baseline serving for the venue was 270 g perperson, whichwas reduced in theN2013 conference to140 g per person (equivalent to 340 g per day, Leipet al 2014, Tumwesigye et al 2014). The fact that base-linemeat intake for international conferences in Kam-pala was 50% higher than for similar conferences inEdinburgh highlights the need not just to considernational or regional averages, but also the demo-graphic structure of meat and dairy intake betweendifferent sectors of society. It also recalls Article 6b ofthe Barsac Declaration: ‘In many developing countries,increased nutrient availability is needed to improve diets,while in other developing countries, per capita consump-tion of animal products is fast increasing to levels that areboth less healthy and environmentally unsustainable.’

In this focus issue, Billen et al (2015) examine thesechallenges, considering the implications for feeding agrowing world population. They estimate thatimproving the agronomical performance in the mostdeficient regions is a key requirement in order toachieve global food security without creating evengreater adverse effects of nitrogen pollution as theycurrently occur. They conclude that if an equitablehuman diet (in terms of protein consumption) is to beestablished globally (the same in all regions of theworld), then the fraction of animal protein should notexceed 40%of a total ingestion of 4 kg N capita−1 yr−1,or 25%of a total consumption of 5 kg N capita−1 yr−1.

These challenges for nitrogen and food securitywere brought together during the N2013 conference,as reflected in the agreed ‘Kampala Statement-for-Action on nitrogen in Africa and globally’ which sum-marized the conference conclusions and key messages(INI 2013). In particular, the Kampala Statementemphasized that Africa is entering a new Green Revo-lution where strengthened policies to supportimproved low-cost, reliable fertilizer delivery to small-holder farmers will be necessary to increase agri-cultural productivity. The messages specific to sub-Saharan Africa were complemented by global mes-sages including the need to reduce nitrogen lossesfrom agriculture and other sectors including industry,transport, energy andwaste.

2.2. Nr intensification in low input systems andintegrated soil fertilitymanagementThe growing demand for high-protein productsrecognized by the Kampala conference can have an

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undesirable impact on natural resources. A criticaleffect is the ongoing reduction in the soil’s Nr capital(soil ‘nitrogen mining’), where the labile pools of soilorganic N (SON) seem to be well correlated with Nrelease rates, such as particulate organicN andN in thelight fraction of soil organicmatter (SOM).While suchsoil Nr mining will maximize ‘service flows’ (usableoutputs) and the value of crop production for severalyears (Sanchez et al 1997), it is not sustainable in thelong term. In low-input smallholder systems, soilnitrogen stocks have reduced due to escapes into theenvironment as a result of over-farming, erosion andleaching (Stoorvogel and Smaling 1990) if the systemsare notmanaged for sustainability.

This is not to exclude the possibility of makingmaximum use of existing soil nitrogen stocks. How-ever, optimizing the contribution of existing N stockswill depend on determining and maintaining theminimal size of the Nr that allows themarginal costs ofnutrient replenishment to bemet by themarginal ben-efits. In addition to providing necessary inputs of Nfrom external sources, maintaining soil N stocks canalso be aided by more efficient Nr cycling, i.e. transferof nitrogen already in the field from one component toanother (Palm et al 1997).

In this focus issue, Powell (2014) demonstrateshow the efficiency of Nr cycling in crop-livestock sys-tems very much depends on optimizing approaches tofeed and manure management and targeting applica-tion, whether in low-N-input or high-N-input dairycattle systems as they impact manure N excretion,manure N capture and recycling, crop production andenvironmental N loss. They found that initial soil Nstock largely determined the degree of manure N useefficiency, with high rates of N input being associatedwith lowmanureNUE, while low rates ofN inputwereassociatedwith highmanureNUE. Similarly, the studyreported in this issue by Sanz-Cobena et al (2014), onyield-scaled mitigation of ammonia emission from Nfertilization, demonstrates how different rates, formsand methods of fertilizer N application can have sig-nificant implications for crop yield, N surplus andNUE. They show how these terms can be used as per-formance indicators that can help farmers’ acceptanceof technology and environmental protectionmeasures.

Recent developments also show that anthro-pogenic driven BNF can be successful for Nr intensifi-cation in low-N-input systems, provided thatappropriate legumes are inoculated with elite inocu-lants and ensuring that P is utilized as a key input. Overa period of 4 years, N2Africa’s BNF technology dis-semination project9 realized up to 15% increases infarm yields of grain legume and 17% in BNF (Woomeret al 2014).

2.3. ImprovingNmanagement in fertilizers andagriculturalmanuresIncreased attention internationally is now being givento defining metrics of NUE as a basis to assessimprovements in performance as a result of betternitrogen management (Norton et al 2015, Oenemaet al 2015). In this focus issue, Yan et al (2014)investigate this topic using data from cropping systemsacross China. In particular, they assess fertilizerrecovery efficiency for nitrogen (REN), which is basedon within year uptake of fertilizer nitrogen by crops,with a fuller view that accounts for all sources of cropN inputs and for crop recovery of nitrogen insubsequent years. Overall, they acknowledge that RENis low in China at less than 30%. By contrast, the long-term effective REN including uptake in subsequentyears is about 40%–68%. While they recognize thatthere are still substantial losses, including to denitrifi-cation, NH3 volatilization, surface runoff and leach-ing, the study shows the importance of accounting forthe residual effect of N when optimizing fertilizerinputs.

It is also critical that fertilization regimes be tai-lored to the biophysical environments and socio-eco-nomic status of farmers in order to optimize NUE.The response of agricultural soils to fertilizers applica-tion is, among other parameters, shown to be a func-tion of the state of soil fertility. This is especiallyillustrated by the contrasting situation of low fertilizerN inputs in sub-Saharan Africa. Here smallholderfarms that are cropped without any external nutrientinputs gradually become exhausted of nutrients andcarbon stocks. Such soils have been shown to respondpoorly to fertilizer application, while more efficientuse of nutrients can be kick-started with additions of acarbon source, such as livestock manure (Zingoreet al 2007). In the same way that sufficient availablephosphorus is needed to maximize NUE, it is evidentthat balanced availability of all required nutrients isnecessary if increased nitrogen fertilizer application isnot to be associated with reduced NUE and increasedair andwater pollution.

These examples illustrate the classic two-sidednitrogen problem of too little and too much, bothrequiring efficient fertilizer N management, as illu-strated for example by the 4R nutrient stewardshipconcept of the International Plant Nutrition Institute10:Right fertilizer, Right amount, Right time and Rightplacement, and in the ‘Five Element Strategy’ toimprove NUE described in ‘Our Nutrient World’:Nutrient stewardship, Crop stewardship, Appropriatepractices for irrigation, Integrated weed and pest man-agement, site-specific nutrient management, includ-ing formanures (Sutton et al 2013a).

9http://n2africa.org/

10http://ipni.net/4R

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http://n2africa.org/http://ipni.net/4R

3.Nitrogen impacts

3.1. Nitrogen effects on humanhealthNitrogen can affect human health through severaldifferent pathways. Examples include exposure toNOx, due to the emission of NO in combustionprocesses, and to fine particulate matter, formed fromsecondary inorganic aerosols by combination of nitro-gen oxide and ammonia emissions, which contributeto respiratory and cardio-vascular diseases (e.g. Mol-danova et al 2011). At the same time, release of excessN and P nutrients into freshwater and coastal ecosys-tems can cause toxic algae blooms causing healtheffects from the consumption of fish and otherseafood, as well as increased levels of nitrate indrinking water. Excess nutrient intake similarly leadsto obesity, resulting in adverse effects on the cardio-vascular system and causing a range of diseases, whilehigh levels of nitrate intake may have adverse effectsthrough the digestive tract, including increasing risk ofcolon cancer, as discussed by Brender (2016) as part ofan accompanying volume on the Kampala conference.Finally, the contribution of nitrogen to troposphericozone formation reduces crop yield and ecosystemhealth, as well as contributing to global warming withhealth effects due to temperature rise, extremeweatherevents or the increase of vector-borne diseases.

As a contribution to this focus issue, Schullehnerand Hansen (2014) illustrate these concerns for thepopulation of Denmark, showing that the trends innitrate exposure differ for users of public water supplycompared with those dependent on private wells.Overall, the fraction of the Danish population exposedto elevated nitrate concentrations has been decreasingsince the 1970s, as a result of lower nitrate levels in thepublic water supply. By contrast, nitrate levels havebeen increasing over this period amongst private wellusers. This leads Schullehner and Hansen to thehypothesis that the decrease in nitrate concentrationsin drinking water is mainly due to structural changesrather than improvement of the groundwater qualityofDenmark.

The risks of atmospheric emissions for humanhealth are highlighted by the contribution of SinghandKulshrestha (2014), who compare urban and ruralconcentrations of Nr in the air above the Indo-Gange-tic plains of India. Their findings highlight an abun-dance of reactive nitrogen (NH3 and NO2) withexceptionally high concentrations at both types of site,with both NH3 (6–150 μg m

−3; site means 41 and52 μg m−3) and NO2 concentrations (2.5–64 μg m

−3;sitemeans 19 and 24 μgm−3) showing substantial sea-sonal variability. These concentrations of the gaseousprecursors demonstrate the risk of extremely high sec-ondary particulate matter concentrations, with sub-stantial risks to human health. The concentrationsobserved in both sides are substantially higher than inpopulated areas in developed countries and demon-strate the need to focus observations and research into

air pollution control measures in densely populatedregions and cities of emerging and developingcountries.

3.2. Nitrogen effects on ecosystemhealthIncreased N deposition around the world affects keyenvironmental drivers such as biodiversity, health ofterrestrial ecosystems (Dise et al 2011, Goodaleet al 2011) the aquatic and marine environment(Borja 2014), with major interactions with health andwell-being through eutrophication, acidification, andnitrogen–carbon-climate interactions (Butterbach-Bahl et al 2011, Suddick et al 2012).

Europe, theUnited States of America, China, Indiaand others are the major hotspots for N emissions.Where stringent emission control policies have beenenacted and enforced, such as, for instance, the CleanAir Act in the USA since 1970, measures to controlNOx emissions have resulted in a 36% decrease overalland resulted in reduced NO3 deposition through pre-cipitation. However, in the same country, NH3 emis-sions have been mainly unregulated and this hasresulted in increased NH3 emissions with rising NH4in wet deposition in the same period (Bleekeret al 2009). A new comprehensive analysis in this focusissue by Du et al (2014) has assessed trends of wetdeposition of ammonium, nitrate and total dissolvedinorganic N (DIN, the sum of +NH4 and )-NO3 forthe period 1985–2012 over the USA. They applied sta-tistical tests to analyze data from the National Atmo-spheric Deposition Program (NADP; Helsel andFrans 2006). Du et al found that wet DIN did notchange significantly, but the mean annual NH4–N/NO3–N ratio increased from 0.72 to 1.49 over the per-iod, as the dominant N species in wet deposition toUSA ecosystems shifted from -NO3 to +NH .4 Theresult clearly reflects the effectiveness of NOx emissioncontrols and the lack of NH3 emissions controls. Dif-ferent N species (oxidized and reduced forms) alsoexert different effects on the environment (e.g., Shep-pard et al 2011 showed a proportionately larger effectof NH3 than +NH4 and -NO3 per unit N input) indi-cating the importance of taking into account all Nrspecies in the development of regulations for control-lingN emissions.

Another observation reported in this focus issue isthat demand for synthetically produced N fertilizersthrough the Haber Bosch process has increased muchfaster than for P fertilizer (Sutton et al 2013a), whichhas substantially increased the N:P ratio in environ-mental pools (Glibert et al 2014). In parallel with agrowing demand for N fertilizers and the extreme ‘lea-kiness’ of nitrogen use in agriculture, there has alreadybeen some levelling-off of global P losses to theenvironment as industrialized nations reduced P usein detergents and upgraded sewage treatment pro-cesses in the mid-1980s and 1990s. Glibert et al (2014)relate this increase in N:P ratio to the occurrence and

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proliferation of harmful algal blooms (HABs) in waterbodies including lakes, rivers and coastal waters bring-ing about large negative economic and ecologicalimpacts.

For example, Glibert et al (2014) show how fertili-zer use in China, which has risen from 0.5 Mt in the1960s to 42Mt in 2010 with urea increasing fivefold inthe last two decades (IFA 2014), has led to nitrogenexport during the same period increasing from 500 to1200 kg N km−2 in the Yangtze River catchment, withan increase from 400 to>1200 kg N km−2 in the Zhu-jiang (Pearl) River catchment (Ti and Yan 2013).Recognizing these changes, Wang et al (2014) in thisfocus issue, apply a mass balance model based onHowarth et al (1996) to estimate that N input to thewhole Yangtze River basin was 16.4 Tg N in 2010,representing a twofold increase over a period of 20years. Other major sources of inorganic N in theregion include atmospheric +NH4 resulting fromNH3 emission, with livestock excretion, fertilizer N,crop residue and burning, human waste contributing(Luo et al 2014). The result, as Luo et al show in thisissue, is extremely high rates of atmospheric nitrogendeposition to coastal seas. Improving NUE, with asso-ciated reduction in the Nr inputs and the consequentNr pollution losses, would result in far reaching bene-fits to ecosystems. In contrast, van Meter et al (2016)analyzed long-term soil data (1957–2010) from 2069sites throughout the Mississippi River Basin (MRB) toreveal N accumulation in cropland of 25–70 kg ha−1

yr−1, a total of 3.8±1.8 Mt yr−1 at the watershedscale. Based on a simple modeling framework to cap-ture N depletion and accumulation dynamics underintensive agriculture, they show that the observedaccumulation of SON in the MRB over a 30 year per-iod (142 Tg N) would lead to a biogeochemical lagtime of 35 years for 99% of legacy SON, even withcomplete cessation of fertilizer application. Thesefindings make a critical contribution towards closingwatershed N budgets by demonstrating that agri-cultural soils can act as a netN sink.

3.3. Nitrogen and climate changeNitrogen climate interactions are recognized to oper-ate in twoways. First, human alteration of the nitrogencycle can alter N flows in the environment withpotential impacts on climate by altering global warm-ing potential. Secondly, ongoing climate change maylead to feedbacks with other consequences for thenitrogen cycle and its impacts. Both issues are highlycomplex, as increased N use and losses have bothwarming effects (increasedN2O emission, suppressionof C sequestration due to tropospheric ozone) andcooling effects (increased C sequestration due to theforest fertilizing effect of atmospheric deposition),light scattering due to higher loading of nitrogencontaining aerosol (Butterbach-Bahl et al 2011). Interms of the feedbacks of climate change on the

nitrogen cycle, this can include alteration of carboncycling, potentially threatening the stability of storedcarbon pools (Suddick et al 2012) as well as lead toincreased rates ofN volatilization (Sutton et al 2013b).

The contributions addressing the nitrogen climateinteraction in this focus issue all concentrate on thefirst part of this challenge, and specifically on under-standing how to quantify and reduce emissions of thegreenhouse gas N2O. While methods to upscale N2Oemissions use a wide range of inventory approaches,Fitton et al (2014) highlight the importance of apply-ing process-based models that can incorporate theeffects of improved management actions. Theyapplied the Daily DayCent (DDC) model to UK con-texts assessing its performance to simulate measuredN2O emissions as compared with use of the IPCC Tier1methodology. They found theDDCmodel to be par-ticularly sensitive to soil pH and clay content and wereable to provide a more accurate representation ofannual emissions than the Tier 1 approach.

One of the most widely discussed methods toreduce N2O emissions in fertilized agricultural sys-tems is the use of nitrification inhibitors, which slowthe conversion of +NH4 to -NO ,3 thereby limitingbuild-up of soil -NO ,3 which is a key substrate forN2O emission. Misselbrook et al (2014) assess theireffectiveness for a range of UK field conditions, givingparticular emphasis to the performance of dicyandia-mide (DCD) additions to fertilizer, cattle urine andcattle slurry application to land. They found it toreduce N2O emissions for ammonium nitrate, ureaand cattle urine by 39%, 69% and 70%, while similarreductions for cattle slurry (56%) were more scatteredand therefore not statistically significant. Overall, theyestimated that the approach could reduce nationalagricultural N2O emissions by 20% (without increas-ing NH3 emission or NO3 leaching), though morecost-effective delivery mechanisms are needed tomake the approach more attractive to farmers. It isworth noting that the mitigation efficiencies of Mis-selbrook et al are higher than most previous studies(e.g., a meta-analysis of Akiyama et al 2010 found anaverage N2O mitigation efficiency of 30%). This islikely because DCD applied in this study was sprayedacross the whole soil surface, while in most other stu-dies, DCDwas combined with fertilizers and thus mayhave affected only fertilizer-induced emission.

Davidson and Kanter (2014) extend the theme ofN2O to the global scale, reporting results of an assess-ment initiated by UNEP (Alcamo et al 2013) on theactions that would be needed to reduce global N2Oemissions. Davidson and Kanter first compare andupdate recent estimates of global N2O emissions andthen consider possible emission scenarios up to 2050.They then show how several business-as-usual scenar-ios are expected to double N2O emissions by 2050. Bycontrast, they estimate that a 22% reduction in emis-sions (compared with 2005)would be needed to stabi-lize N2O concentrations by 2050 (at around 350 ppb).

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According to their comparisons, this will only be pos-sible with aggressive mitigation in all sectors (agri-culture, industry, biomass burning, aqua-culture) andsubstantially reduced per capita meat consumption inthe developedworld.

4.Other options for nitrogenmanagement

4.1.Managing nitrogen inwasteThe management of nitrogen in waste has not been acore focus of the papers within this focus issue,however its importance as part of the anthropogenicnitrogen cycle is clear. Nitrogen in waste (from bothhousehold and industrial sources) includes both ‘solidwaste’ (i.e. discarded food, products and packaging) or‘wastewater and sewage’ (including industrial waste-water). The items with the highest nitrogen fraction inthis system are sewage andwastewater, alongwith foodwaste—due to the nitrogen levels within protein(around 16%).

Due to the high quantity of nitrogen found withinwastewater and sewage, its management is crucial forminimizing the impact of nitrogen on the environ-ment. This has been highlighted in the Kampala State-ment, which stated one of its Global Messages as‘Improving Treatment of Waste: Sewage treatment andsolid municipal waste (household wastes) are sources ofnitrogen losses that could be reduced by treatment and/orrecycling.’ The need for this also stems from the largevariation in management of wastewater and sewageglobally. Hutchings et al (2014, this issue) can showongoing improvements in wastewater treatment andincreases in N2 emission in the Danish national Nbudget. However, in Africa, in this issue, Zhou et al(2014) discuss the difficulties of estimating fluxes ofwastewater to rivers in the Lake Victoria Basin due tothe lack of wastewater treatment plants and waste-water collection facilities. Bustamente et al (2015, thisissue) highlight that wastewater represents the largestsource of total dissolved nitrogen (TDN) to coastalecosystems in South America and whilst in Brazilaccess to cleanwater has improved, access to improvedsanitation is still not available to 125 million residents.Singh and Kulshrestha (2014, this issue) also provideimportant comparative insights into both ammoniaand NOx emission profiles from rural and urban areasin India—where human waste (and municipal waste)led to high levels of ammonia concentrations. Waste-water and sewage also contribute to 3% of the globalbudget of N2O—either directly fromwastewater efflu-ent or from bioreactors removing N in biologicalnutrient removal plants (Davidson and Kanter 2014,this issue). Finally whilst improved wastewater treat-ment avoids runoff into rivers, ultimately it also repre-sents the loss of N from the system, which couldotherwise be recycled.

Food waste is also a key battleground for nitrogen,once produced and collected, it can be incinerated or

added to landfill, however anaerobic digestion of wastefood (and separated sewage) to generate methane andcarbon dioxide biogas is gaining in importance andyields are comparable to several energy crops whichcan be grown for the same purpose (Weiland 2009).Hutchings et al (2014, this issue) indicate that theDan-ish government has established targets for sub-stantially increasing the recycling of organic waste.However, unlike sewage and wastewater, a large pro-portion of food waste is avoidable and therefore thepotential benefits of decreasing food waste streams hasalso been discussed in this issue. Bodirsky and Müller(2014, this issue) highlighted the importance thatdecreasing foodwaste could have in increasingNUE intwo of their three scenarios, Also in this issue, Leip et al(2015) stated that reducing over-consumption of foodand food waste was central to achieve ‘Nitrogen Neu-trality’ and againHutchings et al (2014) discussed foodwaste in the context of a Danish nitrogen budget, andthe potential gains that could be made in reducing thefood waste from retailers, from restaurants and ininstitutional food preparation.

It is clear from this focus issue, that consideringwaste is important for nitrogen and more work is nee-ded in terms of both minimizing waste streams,improving sanitation and waste collection and wherepossible increasing recycling and re-use. However,such solutions will need to be underpinned byimprovements in data availability on N flows in wastestreams.

4.2. Reducing nitrogen emissions from combustionand industryAs Galloway et al (2014) show in this issue, substantialreductions of Nr emissions from fossil fuel combus-tion sources have been achieved in most developedcountries since the 1990s. For Europe, Vestreng et al(2009) report consistent downward trends in part-icular for emissions from road transport and largecombustion sources. Due to the implementation ofincreasingly stringent air pollution control policies inEurope and the US, most large power plants todayutilize both primary and secondary control measures,reducing the formation and emission of nitrogenoxides with varying efficiency. Primary emissioncontrolmeasures typically applied comprisemodifica-tions of the combustion process such as:

• burner optimization (e.g. excess air control orburner fine tuning)

• air staging (over fire air or two-stage combustion)

• flue gas recirculation

• low-NOx burners.

While primary measures address the formation of Nrin the combustion chamber, secondary measuresconvert the formed oxides of nitrogen by treating the

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flue gas, for instance by selective catalytic and non-catalytic reduction through the injection of sal ammo-niac, ammonia or urea. State-of-the-art secondarycontrol measures can achieve reduction efficiencies of80%–90% for NOx, however, a small amount ofammonia may be released into the environment, theso-called ‘ammonia slip’, which reduces the overallefficiency for Nr control. (see e.g. Javed et al 2007,Johnson et al 2009).

Road vehicles have been subject to several stages ofregulation with nominal reductions of NOx emissionsranging from approx. 90% for diesel and 94% forgasoline engines, when considering the type approvallimit values for a EURO 6 compliant passenger carrelative to a EURO 1 compliant vehicle. By analogy forheavy duty vehicles (HDV), a EURO V compliantHDV emits less than 13% of NOx emissions comparedto a pre-EURO standard vehicle (European Commis-sion 2008, Carslaw et al 2016).

Emission reductions of NOx for road vehicles havebeen mainly achieved through the application of cata-lytic converters (e.g. the three-way catalyst), as well asthe use of enginemanagement systems. The latter haverecently been the topic of public debate, as softwaremanipulations as well as the exploitation of legal loop-holes by vehicle manufacturers have resulted in lesseffective emission control for NOx in real-world driv-ing conditions than test cycles suggested (Burki 2015,Oldenkamp et al 2016). The real emission reductionsachieved for road transport sources over the past dec-ades is thus difficult to quantify until more advancedand wide-spread emission measurements are under-taken. In addition, a trade-off between state-of-the-artparticle traps has been observed, which results inincreased emissions of primary NO2 from diesel vehi-cles (Chen andBorken-Kleefeld 2014).

As a result of these emission control efforts, a peakof NOx emissions from fossil fuel combustion sourceshas happened in the late 1990s or early 2000s, depen-dent on the region, for industrialized countries. Incontrast, emerging economies (e.g. Brazil, Russia,India and China—BRIC countries) still show rapidlyincreasing emissions of Nr from combustion sources,as efforts to control emissions are outpaced by rapideconomic growth, leading to fast increasing vehiclefleets and fossil fuel power plants to satisfy growingenergy demand, as recently shownby Liu et al (2013).

4.3. Progress in implementing nitrogenmanagement actionsPrevious successful examples of improving N useefficiency and reducing Nr loss by agricultural man-agement, have been documented, for instance in thecase of maize production at national scale in theUnited States (Cassman et al 2002), or rice productionat farm scale in Asia (Dobermann et al 2002). In thisfocus issue, Dalgaard et al (2014) describe a case studydemonstrating how, on a country scale, substantial

reductions of N input have been achieved, whilemaintaining and even increasing agricultural produceoutput at the same time. The average N-surplus inDanish agriculture has been reduced from approxi-mately 170 kg N ha−1 yr−1 to below 100 kg N ha−1

yr−1 during the past 30 years, while the overall NUEfor the agricultural sector (crop+livestock farming)has increased from around 20%–30% to 40%–45%.As a result, N-leaching from the field root zone hasbeen halved and N losses to the aquatic and atmo-spheric environment have been significantly reduced.This was achieved through the implementation of aseries of policy action plans to mitigate losses of N andother nutrients since mid-1980s. However, the reduc-tion in total N loadings to the environment did notresponse linearly to the reduction in surplus N,showing the need to gain a better understanding of therelationships between the different N pools and flows,including the denitrification of N, and the buffers of Nin bioticNpools.

For the Taihu Lake region of China, a well-knownhigh N load region, Xue et al (2014) document in thisfocus issue how reduced fertilizer input to rice–wheatrotation systems from farmer’s conventional rates of510 kg N ha−1 yr−1 to 390 kg N ha−1 yr−1 byimproved management practices such as the com-bined use of organic and inorganic fertilizer, use ofcontrolled release fertilizer, respectively to 333 kg Nha−1 yr−1 by adopting site-specific management,resulted in reduced environmental impacts of fertili-zerN.

For livestock systems, Bealey et al (2014) describehow landscape structure can be used to limit netammonia emission. They show in this issue the effectof tree canopy structure on recapturing ammoniafrom livestock production, using a coupled turbulenceand deposition turbulence model. They found thatusing agro-forestry systems of different tree structuresnear ‘hot spots’ of ammonia in the landscape couldprovide an effective abatement option for the livestockindustry in livestock operations in the UK. This exam-ple may be contrasted with rather different livestocksystems in low-N input Africa, where Rufino et al(2014) report how only few data are available to date tounderstand the livestock-related N flows. They there-fore propose joint efforts for data collection and thedevelopment of a nested systems definition of live-stock systems to link local, regional and continentallevel and to increase the usefulness of point measure-ments ofN losses.

5. Integrated assessment of nitrogenmanagement strategies

5.1.Harmonizing indicators on effects, losses andnitrogen use efficiencyWithNr freelymoving between different environmen-tal pools (Galloway et al 2003), management strategies

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aiming to reduce emissions to the environmentrequire integrated perspectives in order to avoid‘pollution swapping’, i.e. exchanging improvementtowards one pool by deterioration for another pool,while at the same time maximizing the beneficialsynergies. Such an integrated assessment cannot bebased on observing individual effects, but needs to takeadvantage of indicators, such as already discussed inthe increasing adoption of NUE indicators (Nortonet al 2015, Oenema et al 2015).

The concept of ‘nitrogen neutrality’, introducedby Leip et al (2014) in this focus issue, goes the nextstep to relate human actions to indicate environmentalperformance. Offsetting the release of Nr by way ofcompensating at a distinctively different entity will notremove local or regional effects, unless the spatial reso-lution of compensation matches the respective envir-onmental effect. The major merit of compensation,however, consists of awareness raising to demonstratehowmuch effort is needed to compensate for a specificadverse human action.

Nitrogen neutrality as a concept addresses theeffects of a certain activity over a whole life cycle,including preceding process stages. Such ‘nitrogenfootprint’ analyses have been developed on severallevels, for whichGalloway et al (2014) provide an over-view. These indicators include an ‘N-calculator’ to beused by individuals in selected countries to assess theirprivate impacts (potentially also guided by an N-labelattached to products), an institution-oriented foot-print that can be used by organizations or companies,and an N-loss indicator to quickly evaluate N impactsof world regions or countries. Developing and harmo-nizing indicators allows easy benchmarking betweenentities and thus provides guidance towards possibleimprovements.

5.2. Interaction of the nitrogen cycle with othernutrients and thewater cycleAn overarching perspective not only integrates overenvironmental pools, but also considers interactionsbetween relevant effective constituents. With Nr beinga potent plant nutrient, its relationship to othernutrients requires attention. In this focus issue,Bouraoui et al (2014) investigate the different andcombined effects of Nr and phosphorous (P) inEuropean inland waters. They employ a modelingapproach to investigate the most effective means toabate pollution. Regarding P, they conclude that theban of P in laundry detergents, together with the fullimplementation of European water protection legisla-tion, would maximize effects. In addition, optim-ization of practices for organic manure applicationprovides the ideal strategy to mitigate Nr-related waterpollution. Retention of nitrogen as a part of nutrientmanagement strategies has similarly been discussed byGrizzetti et al (2015), who here compare differentmodeling approaches. They conclude that the

integration of all processes in the river basin, thepossible lag time between nitrogen sources andimpacts, and the difficulty in separating temporaryand permanent nitrogen removal, and the associatedN2O emissions to the atmosphere, remain criticalaspects and a source of uncertainty in integratednitrogen assessments. As already noted, the impacts ofnitrogen leaching to the long-term trends of drinkingwater have also been studied for the Danish situationby Schullehner andHansen (2014).

5.3. Regional and global nitrogen assessmentThe application of indicators mentioned in section 5.1with consideration of the interconnections betweenNr flows provide useful hooks to guide studies aregional level. In this focus issue, especially the over-views developed on situations of sub-Saharan Africa,allow insight in topics for which information islimited. In this way, Zhou et al (2014) apply net-anthropogenic nitrogen input (NANI) as an indicatorto assess human impacts on the Lake Victoriawatershed. On average, NANI was assessed to be in theorder of 20 kg N ha−1 yr−1, which was associated withsoil mining due to lack of mineral fertilizer or food/feed N imports. Riverine Nr flows into Lake Victoriawere thus relatively low, with human and animalwastes considered to be the major contributors to lakepollution.

Atmospheric nitrogen fluxes were evaluated byGaly-Lacaux and Delon (2014) from measurementsalong an ecosystem transect across Western and Cen-tral Africa, considering dry and wet savannah and for-est. They find emissions and deposition of Nr roughlyin balance at around 10 kg N ha−1 and year, with aclear discrepancy in forests (higher deposition), whilein both savannah types the difference between esti-mated emission and deposition is insignificant.

Extending from Africa, a regional footprint of Nrdue to anthropogenic activities is reported in the focusissue by Shibata et al (2014). These authors demon-strate that food imports are beneficial for Japan’s Nfootprint as the specific impacts of local productionare much higher. Footprints can be differentiated bypopulation group, with younger people in Japan con-suming less fish and more meat and thus impactingmore strongly on the N cycle. Total footprints in Japanare comparable to Europe, but lower than those oftheUS.

In their analysis for the Netherlands and the Eur-opean Union, van Grinsven et al (2015) demonstratethat economic outputs and food security not alwaysbenefit from more intensive agricultural production,especially when considering the external costs of pol-lution. Using specific scenarios, they argue that byhalving meat consumption, pollution related costscould be decreased more strongly than the produc-tion-related GDP, resulting in a net economic gain. Ina region rich in nitrogen, adjusted human diets and

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externalization of environmental costs of excess Nrcould drive a sustainable extensification of agriculturalproduction. In their assessment for the USA, Sobotaet al (2015) estimated the health and environmentaldamages of anthropogenic N in the early 2000s toamount to $210 billion yr−1 USD (range: $81–$441billion yr−1). Despite recognizing gaps and uncertain-ties that remain in these estimates, the overall work byvan Grinsven et al (2015) and Sobota et al (2015) pre-sents a starting point to inform decisions and engagestakeholders on the economic costs ofNpollution.

Using analyses of selected watersheds in SouthAmerica, Bustamante et al (2015) show median con-centrations of TDN at 325 μg l−1 and 275 μg l−1 in theAmazon and Orinoco basins, respectively, increasingto nearly 850 μg l−1 in La Plata Basin rivers and2000 μg l−1 in small northern Venezuelan watersheds.The median TDN yield of Amazon Basin rivers(approximately 4 kg ha−1 yr−1) was larger than TDNyields of undisturbed rivers of the La Plata and Ori-noco basins; however, TDN yields of polluted riverswere much higher than those of the Amazon and Ori-noco rivers. They conclude that organic matter loadsfrom natural and anthropogenic sources in rivers ofSouth America strongly influence the N dynamics ofthis region.

Lassaletta et al (2014) have applied the NUEapproach to investigate the global trajectories of Nrflows on a global scale over the last 50 years. Using databy the Food and Agriculture Organization of the UnitedNations (FAO), their study allows a comparison of thedevelopment in total Nr inputs and agricultural yieldsin 124 countries. The dataset compiled shows whichcountries of the world were affected by soil mining,where Nr has been applied excessively, and when thesecountries have managed to improve their NUE, oftenby a significantmargin.While available data would notallow for the compilation of full nitrogen budgets andan evaluation of individual country’s Nr relateddamage, the study clearly exemplifies to which extentindicators can be used to establish the potential of suchdamage and to develop (sub-)national benchmarks.Results for Europe presented by Leip et al (2015) showthat the livestock sector contributes significantly toagricultural environmental impacts, with contribu-tions of 78% (terrestrial biodiversity loss), 80% (soilacidification and air pollution due to ammonia andnitrogen oxides emissions), 81% (global warming),and 73% (water pollution, both N and P) respectively.Agriculture as a whole is one of themajor contributorsto these environmental impacts, ranging between 12%(global warming) and 59% (N water quality) impacts.Leip et al (2015) conclude that in order to make sig-nificant progress in mitigating these environmentalimpacts in Europe, a combination of technologicalmeasures reducing livestock emissions, improvedfood choices and reduced food waste of European citi-zens is required.

Based on a detailed analysis of nutrient dischargesfrom aquaculture operations in China, Zhang et al(2015a) conclude that improvement of feed efficiencyin cage systems and retention of nutrients in closedsystems is necessary. Furthermore, strategies toincrease nutrient recycling (e.g. applying integratedmulti-trophic aquaculture), as well as socio-economicmeasures (e.g. subsidies), should be increased in thefuture. Zhang et al (2015a) recommend the use ofhybrid agricultural-aquacultural systems and theadoption of NUE as an indicator at farm or regionallevel for the sustainable development of aquaculture,among other measures, to improve the sustainabilityof Chinese aquaculture. Liang et al (2015) propose theuse of a regionally optimal N rate (RONR) determinedfrom the experiments (on average 167 kg ha−1 andvaried from 114 to 224 kg Nha−1) for different regionsin China. If these RONR were widely adopted inChina, they estimate that∼56%of farmswould reduceN fertilizer use, while ∼33% would increase their useofN fertilizer. As a result, grain yield would increase by7.4% and the estimated GHG emissions would declineby 11.1%, suggesting that to achieve improved regio-nal yields and sustainable environmental develop-ment, NUE should be optimized both among N-poorandN-rich farms and regions inChina.

6.Nitrogen challenges projected into thefuture

Observations of past developments may serve to guidean understanding of a possible future—a future forwhich all the N-related interactions described in thisissue remain to be considered. Specifically two paperscover such future global scenarios. Billen et al (2014)report on a wide range of available options to satisfyglobal food demand—options that impact the N cyclein very different ways. Remarkably, the authors pointto solutions where international trade is kept at a lowlevel as those that produce less N losses to theenvironment. As with the scenarios of Davidson andKanter (2014) for N2O, already described, these resultsdemonstrate, likemany of the other examples reflectedon here, that substantially improved nitrogenmanage-ment is indeed possible if there is the requiredwillingness. It is therefore in the hands of humansociety to decide on the future implementation of suchnitrogen options, which will determine the extent ofthe future nitrogen benefits and the adverse environ-mental impacts.

Future challenges have remained in the center ofattention in the time since the Kampala conference,which initiated this special issue. The planetaryboundaries of nitrogen express the amounts ofanthropogenic nitrogen fixation this world can handlesustainably. Steffen et al (2015) have established thisboundary at a level of 62 Tg N yr−1, while the currentlevel is about two and a half times this value. Work is

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ongoing to break down the boundary to regional andto sectoral targets that are compatible with other sus-tainability goals. A key parameter to be considered inthis respect is theNUE—and its different fate in differ-ent countries over time. Zhang et al (2015b) discussedthe global and country trends, which follow the Envir-onmental Kuznets Curve (EKC; improved situation associeties becomemore effluent) at least for some of thehistoric examples presented, and possibly could beextrapolated to other regions via sustainable intensifi-cation. NUE thus also provides the key theme for thenext conference held in the same series in Melbourne,December 2016.

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1. Introduction2. Nitrogen in food production2.1. Nitrogen and food security2.2. Nr intensification in low input systems and integrated soil fertility management2.3. Improving N management in fertilizers and agricultural manures

3. Nitrogen impacts3.1. Nitrogen effects on human health3.2. Nitrogen effects on ecosystem health3.3. Nitrogen and climate change

4. Other options for nitrogen management4.1. Managing nitrogen in waste4.2. Reducing nitrogen emissions from combustion and industry4.3. Progress in implementing nitrogen management actions

5. Integrated assessment of nitrogen management strategies5.1. Harmonizing indicators on effects, losses and nitrogen use efficiency5.2. Interaction of the nitrogen cycle with other nutrients and the water cycle5.3. Regional and global nitrogen assessment

6. Nitrogen challenges projected into the futureReferences