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Synthesis and review: Tackling the nitrogen management
challenge: from global to local
scales
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homepage for more
2016 Environ. Res. Lett. 11 120205
(http://iopscience.iop.org/1748-9326/11/12/120205)
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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: [email protected]
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.
2
Environ. Res. Lett. 11 (2016) 120205 SReis et al
-
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
3
Environ. Res. Lett. 11 (2016) 120205 SReis et al
-
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
4
Environ. Res. Lett. 11 (2016) 120205 SReis et al
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
5
Environ. Res. Lett. 11 (2016) 120205 SReis et al
-
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