The Nitrogen Cascade
Author(s): James N. Galloway, John D. Aber, Jan Willem Erisman, Sybil P. Seitzinger, Robert
W. Howarth, Ellis B. Cowling, B. Jack Cosby
Source: BioScience, Vol. 53, No. 4 (Apr., 2003), pp. 341-356
Published by: American Institute of Biological Sciences
Stable URL: http://www.jstor.org/stable/1314367
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oArticles
The
Nitrogen Cascade
JAMESN. GALLOWAY,
JOHND. ABER,JAN WILLEMERISMAN,SYBILP SEITZINGER,
ROBERTW. HOWARTH,
ELLISB. COWLING,
AND B. JACKCOSBY
Humanproductionoffood and energyis the dominantcontinentalprocessthat breaksthe triplebondin molecularnitrogen(N2) and createsreac-
Nr in Earth's
andbiosphere
hasa widevarietyofconsequences,
tivenitrogen
(Nr)species.Circulation
ofanthropogenic
atmosphere,
hydrosphere,
Nr
can
cause
whicharemagnified
withtimeasNr movesalongitsbiogeochemical
The
same
atom
multipleeffectsin theatmosphere,
pathway.
of
Asthecascascade.
in terrestrial
infreshwater
andmarinesystems,
andonhumanhealth.Wecallthissequence
ecosystems,
ofeffectsthenitrogen
the
rate
all
environmental
not
at
same
cadeprogresses,
theoriginofNr becomes
Reactive
does
cascade
systems;
through
unimportant.
nitrogen
andresult
Theselagsslowthecascade
somesystemshavetheabilitytoaccumulate
Nr,whichleadstolagtimesin thecontinuation
of thecascade.
NraccumuTheonlywaytoeliminate
whichin turncanenhancetheeffectsofNr on thatenvironment.
inNr accumulation
in certainreservoirs,
Nr backto nonreactive
lationandstopthecascadeis toconvert
N2.
ozone,denitrification
cascade,
Keywords:
fertilizer,
forestdieback,
eutrophication,
nitrogen
T
he chemicalelementsnitrogen(N), carbon(C),
phosphorus(P), oxygen (0), and sulfur(S) areall necessaryforlife.Withone exception,theyaregenerallyavailable
in globalreservoirsto sustainlife formsrangingfromsinglecell organismsto vertebrates.Of these elements,N has the
greatesttotalabundancein Earth'satmosphere,hydrosphere,
and biosphere;it is ironic that N is the elementleast readily
availableto sustain life. The total amount of N in the at4 x 1021
mosphere,soils,andwatersof Earthis approximately
of
these
other
elof
all
four
than
the
mass
grams(g)-more
than
more
ements combined (Mackenzie1998). However,
99%of this N is not availableto more than 99%of livingorganisms.The reason for this seeming contradictionis that
while thereis an abundanceof N in nature,it is almost entirelyin the formof molecularnitrogen,a chemicalformthat
is not usableby most organisms.Breakingthe triple bond
holding the two N atoms together requires a significant
amount of energy-energy that can be mustered only in
high-temperatureprocessesor by a small number of specializedN-fixing microbes.
We divide the N compounds in natureinto two groups:
nonreactiveand reactive.NonreactiveN is N2; reactiveN
(Nr) includes all biologically,photochemically,and radiatively activeN compounds in Earth'satmosphereand biosphere. Thus, Nr includes inorganic reduced forms of N
(e.g., ammonia [NH3] and ammonium [NH4+]), inorganic
oxidizedforms(e.g.,nitrogenoxide[NOx],nitricacid[HNO3],
nitrousoxide [N20 ], and nitrate[NO3-]), and organiccompounds (e.g., urea,amines,proteins,and nucleicacids).
In the prehumanworld,creationof Nr from N2 occurred
primarilythrough two processes,lightning and biological
nitrogenfixation(BNF).ReactiveN did not accumulatein environmental reservoirsbecause microbial N fixation and
denitrificationprocesseswere approximatelyequal (Ayres
et al. 1994).
This is no longer the case.ReactiveN is now accumulating in the environmenton all spatialscales-local, regional,
andglobal(Gallowayet al. 1995).Duringthe lastfewdecades,
productionof Nr by humanshas been greaterthan production from all naturalterrestrialsystems.The globalincrease
in Nr productionhas threemain causes:(1) widespreadcultivationof legumes,rice,and other cropsthat promoteconversionof N2 to organicN throughBNF;(2) combustionof
fossilfuels,which convertsboth atmosphericN2 and fossilN
to reactiveNOx; and (3) the Haber-Boschprocess,which
convertsnonreactiveN2 to reactiveNH3to sustainfood production and some industrialactivities.
The globalrateof increasein Nr creationby humanswas
relativelyslowfrom1860to 1960.Since1960,however,the rate
of increasehas acceleratedsharply(figure la). CultivationinducedNr creationincreasedfrom approximately15 teragrams(Tg) N peryearin 1860to approximately33 Tg N per
year in 2000. ReactiveN creationthrough fossil fuel combustion increasedfrom less than 1 Tg N per yearin 1860to
approximately25 Tg N per yearin 2000.ReactiveN creation
from the Haber-Boschprocesswent from 0 before 1910 to
andB.JackCosbyareprofessors
JamesN. Galloway(e-mail:[email protected])
in the Departmentof EnvironmentalSciencesat the Universityof Virginia,
VA22904.JohnD. Aberis a professorat the Institutefor the
Charlottesville,
StudyofEarth,Oceans,and Space,UniversityofNew Hampshire,Durham,
NH 03824. Jan WillemErismanis head of the Departmentof Integrated
Assessmentat the EnergyResearchCenterof the Netherlands,PO Box 1,
1755ZGPetten,TheNetherlands.SybilP Seitzingeris a professorat theInstituteof Marineand CoastalSciences,RutgersUniversity,71 DudleyRoad,
New Brunswick,NJ 08901.Robert Howarthis a professorin theDepartW.
ment of Ecologyand EvolutionaryBiology,CornellUniversity,Ithaca,NY
North
14853.EllisB. Cowlingis a professorin theCollegeofNaturalResources,
CarolinaState University,1509 VarsityDrive,Raleigh,NC 27606. @2003
AmericanInstituteofBiologicalSciences.
April2003 / Vol.53 No. 4 * BioScience 341
Articles 4
200
6
a
4
100
2/
.150
0.. - .. ...
1910
'
0
1850
1870
-
Population
1890
.
Haber-Bosch
....
; .
1930
1950
1990
1970
- Fossil fuel
C-BNF
i 0
2010
Total Nr
40
0.3
b
30
20
0.1
10
0.0
1850
1870
-
Population
1890
1910
- Fertilizer
1930
C-BNF
1950
-
1990
1970
Fossilfuel
-
Total Nr
0
2010
morethan 100TgN peryearin 2000,
with about85%used in the production of fertilizers.
Thus,between1860
and 2000,the anthropogenicNr creation rate increasedfrom approximately 15 Tg N per yearto approximately165Tg N peryear,with about
fivetimesmoreNr comingfromfood
production than from energy production (Gallowayet al. 2002).
As in the global system, the Nr
creationratein the UnitedStateshas
increasedoverthelastfewdecades.In
1961, the United States createdNr
at a rateof approximately8 Tg N per
year(figure1ib).By 1997,the Nr creationratewasapproximately
25 Tg N
per year.Companionpapersin this
issue (Aberet al. 2003, Driscollet al.
2003, Fenn et al. 2003a, 2003b) discuss Nr biogeochemistry in the
United States,with a focus on the
Northeastand the West.
The remarkablechangesin the N
cycle haveresultedin a wide variety
of changes,both beneficialanddetrimental,to the healthand welfareof
people and ecosystems.A largeportion of the humanpopulationof the
worldis sustainedtodaybecauseNr
is providedas syntheticfertilizersand
cultivation-induced BNF (Smil
2000). But there are also some significant worrisome consequences.
First,Nr is widely dispersedby hydrologicand atmospherictransport
processes.Second,Nr is accumulating in the environmentbecauseNr
creationratesaregreaterthanratesof
Figure1. (a) Globalpopulation trendsfrom 1860 to 2000 (billions, left axis) and reactivenitrogen (Nr) creation (teragrams
nitrogen[Tg N] per year, right axis). "Haber-Bosch"
representsNr creation throughthe Haber-Boschprocess,including
ammonia
For
1920, 1930, and 1940, we assumedthat global total Nr production
productionof
for nonfertilizerpurposes.
the
Haber-Bosch
was
to
through
process
equivalent global anthropogenicfertilizerproduction (Smil2001). For 1950 onward,
data on Nr creation throughthe Haber-Boschprocesswere obtainedfrom USGSMinerals (Kramer1999). "C-BNF"
(cultivation-inducedbiologicalnitrogenfixation) representsNr creationfrom cultivation of legumes,rice,and sugarcane.
The C-BNFratefor 1900 is estimated to be approximately15 TgN per year (VaclavSmil, Universityof Manitoba, Winnipeg,
Canada,personal communication,January2002). The C-BNFratesfor 1860, 1870, 1880, and 1890 were estimatedfrom population, using the 1900 data on population and Nr creation.For 1961-1999, Nr creation rateswere calculatedfrom crop-spe2000) and fixation rates (Smil 1999). Decadal datafrom 1910 to 1950 were interpocific data on harvestedareas (FAOSTAT
lated between 1900 and 1961. "Fossilfuel" representsNr createdfrom fossilfuel combustion.The data from 1860 to 1990 are
from a compilationfrom ElisabethHolland, basedon Miiler (1992), Keeling(1993), and Holland and Lamarque(1997).
Thesedata agree well with those recentlypublishedby van Aardenneand colleagues(2001)for decadal time stepsfrom 1890
to 1990. The data for 1991 to 2000 were estimatedby scaling emissionsof nitrogenoxides to increasesin fossilfuel combustion over the same period. "TotalNr" representsthe sum createdby these threeprocesses.(b) USpopulation trendsfrom 1961
to 1997 (billions,left axis; FAO2000) and Nr creation (Tg N per year, right axis; Howarth et al. 2002a).
342 BioScience * April2003 / Vol.53 No. 4
Articles
Nrremovalthroughdenitrification
to nonreactive
N2.Third,
Nrcreationandaccumulation
is projected
to continueto increasein thefutureashumanpopulations
andpercapitaresourceuseincrease.
contributes
to
Fourth,Nraccumulation
environmental
For
manycontemporary
problems. example:
* Increases
in Nrleadto production
of tropospheric
ozoneandaerosols
thatinduceseriousrespiratory
andcardiac
diseasein humans(Popeet
illness,cancer,
al.1995,FollettandFollett2001,WolfeandPatz2002).
* Forestandgrassland
increase
andthen
productivity
decrease
wherever
Nrdeposition
increases
atmospheric
andcriticalthresholds
areexceeded;
Nr
significantly
additions
also
decrease
in
probably
biodiversity many
natural
habitats
(Aberet al.1995).
* Reactive
N is responsible
withS)foracidifi(together
cationandlossof biodiversity
in lakesandstreams
in
et al.1997).
manyregionsof theworld(Vitousek
* Reactive
N is responsible
foreutrophication,
hypoxia,
lossof biodiversity,
andhabitatdegradation
in coastal
Itis nowconsidered
thebiggestpollution
ecosystems.
in
coastal
waters
Howarth
et al.2000,
problem
(e.g.,
NRC2000,Rabalais
2002).
* Reactive
N contributes
to globalclimatechangeand
ozonedepletion,
bothof whichhave
stratospheric
health(e.g.,Cowling
impactson humanandecosystem
etal. 1998).
Thisarticlefocuseson the multiple linkagesamong the ecological and human health effectsof
Nr moleculesas they move from
(oS
.
I
oneenvironmental
systemto another.Thisphenomenonis called
the N cascade (Galloway1998),
which we define as the sequential transferof Nr through environmental systems and which
resultsin environmentalchanges
as Nr movesthroughor is temporarilystoredwithineachsystem.
We use figure2 as a frame of
referencefor two illustrativescenarios of the Nr cascade.In the
firstexample,energyproduction
by fossilfuelcombustionresultsin
the conversionof atmosphericN2
(or fossil Nr) into NOx. In sequence,an atom of N mobilized
as NOx in the atmosphere can
first increase ozone concentrations,then decreaseatmospheric
visibilityand increaseconcentrations of small particles, and
finallyincreaseprecipitationacidity. Following deposition to the
terrestrialecosystem,the sameN atom can increasesoil acidity (if a base cation is lost from the system),decreasebiodiversity,and eitherincreaseor decreaseecosystemproductivity. If dischargedto the aquaticecosystem,the N atom can
increasesurfacewateracidityand lead to coastaleutrophication. If the N atom is convertedto N20 and emitted back
into the atmosphere,it can firstincreasegreenhousewarming potentialand then decreasestratosphericozone.
The second exampleillustratesa similarcascadeof effects
of Nr from food production.In this case,atmosphericN2 is
convertedto NH3 in the Haber-Boschprocess.The NH3 is
used primarilyto producefertilizer.Abouthalf the Nr fertilizerappliedto globalagroecosystems
is incorporated
into crops
that areharvestedfrom fieldsand used for human food and
livestockfeed (Smil 1999,2001). The otherhalf is transferred
to the atmosphere as NH3, NO, N20, or N2 or is lost to
aquaticecosystems,primarilyas NO3-.Once transferredto
these downstreamor downwindsystems,the N atom is part
of the cascade.Dependingon its chemicalform,Nr will enter the cascadeat differentplaces.An importantcharacteristic of the cascadeis thatonceit starts,thesourceof theNr (e.g.,
fossil fuel combustionor fertilizerproduction)becomes irrelevant.Nr speciescan be rapidlyinterconvertedfrom one
Nr formto another.Thus,the criticalstep is the formationof
Nr in the firstplace.
The simplifiedconceptualoverviewin figure2 does not
cover some importantaspectsof the N cascade.It ignores
the internal cycling of Nr within each component of the
tratospheric
Effects
I
I
NOF(1
Ene
Visibility
Effects
Ec
!"
sts
nFc
rgyA
Production
I
I
N2AT
N
iFood
Production
NH3
Effects
Agroecosystem
NH
Forests
.&
.
Grassland
Animal
Crop
-
Peoplesoi
(Food; Fiber)
-N--1
G
Groundwater
Human Activities
Effects
Efects
water Ioe..
TheNitrogen
Surfiace
ETects Efects
Cascade
1
Ecosyste
Aquatic
s
Figure2. Illustrationof the nitrogen (N) cascadeshowing the sequential effectsthat a single atom of N can have in various reservoirsafter it has been convertedfrom a nonreactive
to a reactiveform. Abbreviations:GH,greenhouseeffect;NHY ammonia;NO,, nitrate;
NO., nitrogenoxide;N20, nitrous oxide;PM, particulate matter.
April2003 / Vol.53 No. 4 * BioScience 343
Articles 4
ecosystem;it does not accountfor long-termNr storage;and
it does not accountfor all the pathwaysthat Nr followsas it
flowsfrom one "box"or effectto another.The followingsections describethese characteristicsin greaterdetail,first for
the atmosphere(troposphereand stratosphere),next forterrestrialecosystems(agroecosystems,forests,andgrasslands),
and finallyfor aquaticecosystems(groundwater,wetlands,
streams,lakes,rivers,and marinecoastalregions).The coverage for these systems is not meant to be exhaustivebut
ratherto give an overviewof how each systembehavesand
interactswithothersystemswithinthe cascade.Wedo not considerthe N cycleof the open ocean,becauselittle of the Nr
createdby human activitieson land reachesthe open ocean
(Nixon et al. 1996, Seitzingerand Giblin 1996, Chen and
Wang 1999).
The cascadeof Nr fromone systemto anotheris enhanced
if thereis limitedpotentialforNr accumulationor loss of N2
through denitrificationwithin a given system and thus increasedpotentialfortransferto the next system.Thereis a lag
in the cascadeif there is a largepotentialfor accumulation
within a system.The cascadedecreasesif thereis a largepotential for denitrificationto N2 within a system (table 1).
Thus,at each stageof the N cascade,we evaluatethe potential for
* accumulationand cyclingof Nr withinthe system;
* loss of Nr throughconversionto N2 by denitrification;
* transferof Nr to othersystems;and
* effectsof Nr withinthe system.
Atmosphere
The atmospherereceivesNr mainlyas airemissionsof NOx,
NH3,and N20 from aquaticand terrestrialecosystemsand
and
fromcombustionof biomassor fossilfuels.
of
NOx
NOx
NHx (NH3 andNH4+) canaccumulatein the troposphereon
a regionalscale.ButbecauseNOxand NHxhavea shortresidencetime in the atmosphereand lackpotentialto form N2
by denitrification,almost all Nr emitted as NOxand NHx is
transferredback to Earth'ssurface within hours to days.
Thereis some internalcyclingof Nr within the atmosphere.
Togetherwith volatileorganicC compounds,increasedconcentrationsof
can lead to increasedconcentrationsof
NOx
ozone and other
photochemicaloxidantsin the atmosphere.
of the NOxis convertedto HNO3,which is
much
Ultimately
eitherconvertedto an aerosol(e.g.,ammoniumnitrate)or deposited on land,surfacewaters,or othersurfaces.NH3 emitted to the atmosphereis either deposited or transformed
into an ammonium aerosol (e.g., ammonium bisulfateor
ammoniumsulfate).Beforedeposition,ammoniumaerosols
contributeto fine particulatematterand regionalhaze concentrationsin the atmosphere.
Sixmajoratmosphericeffectsareassociatedwith increased
NOx and NH3 emissions: (1) Fine particulatematter decreasesatmosphericvisibility;(2) elevatedozone concentrationsenhancethe greenhousepotentialof the atmosphere;(3)
ozone and fine particulatematterhave serious impacts on
human health (Pope et al. 1995);(4) ammoniaplaysan importantrole in the directand indirecteffectsof aerosolson
radiativeforcingand thus on globalclimatechange(Seinfeld
and Pandis1998,Penneret al. 2001;RussellDickerson,Universityof Maryland,CollegePark,MD 20742,personalcommunication,March2003);(5) ozone depositioncan decrease
productivityof crops,forests,andnaturalecosystems;and (6)
atmospheric deposition of NH , NO (all oxidized forms
of nitrogenother than N20), and organicforms of Nr can
contribute to ecosystem acidification, fertilization, and
eutrophication.
N20 and NOxareproducedduringboth nitrificationand
denitrification.Addition of Nr to agroecosystemsleads to
increased N20 and NOx emissions. Nitrous oxide has a
Table1. Characteristicsof differentsystemsrelevantfor the nitrogen cascade.
System
Accumulation
potential
Transfer
potential
N2production
potential
Linksto
systems down
the cascade
Atmosphere
Low
Veryhigh
None
Allbut groundwater
Humanand ecosystem health,
climate change
Agroecosystems
Lowto
moderate
Veryhigh
Lowto
moderate
All
Humanand ecosystem health,
climate change
Forests
High
Moderate,
high in places
Low
All
Biodiversity,net primary
mortality,groundwater
productivity,
Grasslands
High
Moderate,
high in places
Low
All
Biodiversity,net primary
productivity,
groundwater
Groundwater
Moderate
Moderate
Moderate
Surface water,
atmosphere
Humanand ecosystem health,
climate change
Wetlands,streams,
lakes, rivers
Low
Veryhigh
Moderateto
high
Atmosphere,marine
coastal systems
Biodiversity,ecological
structure,fish
Marinecoastal regions
Lowto
moderate
Moderate
High
Atmosphere
Biodiversity,ecological structure,fish,
harmfulalgal blooms
344 BioScience o April2003 / Vol.53 No. 4
Effects
potential
Articles
troposphericresidencetime of approximately100yearsand
is increasingin the troposphereat a rate of approximately
0.25%peryear(Pratheret al.2001).Nitrousoxideis a greenhouse gas in the troposphereand, when transferredto the
stratosphere,decreasesthe concentrationof stratospheric
ozone.As discussedabove,NOxcan contributeto increased
troposphericozone and decreasedatmosphericvisibility.
In summary,the residencetime for most Nr speciesin the
atmosphereis short.Thereis an internalcascadeof effects:
NOx increases the potential first for ozone and then for
aerosolformation.Exceptfor N20, thereis verylimitedpotential for long-term storage of Nr (and thus limited lag
time),buttherearesignificanteffectsfromNr whileit remains
in the atmosphere.Thereis no potentialfor denitrification
andthereis a largepotential
backto N2 withinthetroposphere,
for Nr transferto the next receptor-terrestrialand aquatic
ecosystems(table 1).
Terrestrial
ecosystems
This section discusses the nitrogen cascade in three types
of terrestrial ecosystems-agroecosystems, forests, and
grasslands.
Agroecosystems.Intensivelymanagedagroecosystemsand,
evenmore,concentratedanimalfeedingoperations(CAFOs,
alsocalled"factoryfarms")areonlythe latesttechnicalmeans
by whichhumanneedsand dietarypreferencesaremajordrivers of changein the N cycle.About 75%of the Nr created
to sustainfood
globallyby humansis addedto agroecosystems
production.About 70%of thatNr is from the Haber-Bosch
processandabout30%fromculBNF(figurela).
tivation-induced
Smil(2001)estimatesthatabout
40%of thepeoplealivetodayowe
theirlife to the productionand
wideuseof fertilizers
produced
by
theHaber-Bosch
process.
The agroecosystemsof the
world consist of two general
types: (1) crop production
systems,composedof primary
and (2) animalproproducers;
ductionsystems,composedof
producers.
Cropagrosecondary
producecerealgrains,
ecosystems
and commerfruits,vegetables,
cial fibersthroughthe uptake
of mostlyinorganic
Nr,othernutrients,andwater,usingsunlight
as the energy source. Crop
productionis sustainedby indigenoussourcesof Nr in the
soil;by wet and dry deposition
of Nr fromthe atmosphere;
by
biologicalN fixation;by recycling of crop residues,animal
manure,and human waste;and by applicationof synthetic
Nr fertilizers.The residencetime of Nr within crop agroecosystemscan be yearsto decadesbecauseof the largepool
of organicmatterin the soil.Cassmanand colleagues(2002)
reportsubstantialindigenoussoil Nr reserves;for example,
a typicalirrigatedrice soil in Asiacontainsabout 2800 kilograms (kg) N per hectare(ha) in the upper 20 centimeters
(cm). Fertileprairiesoil in the CornBeltof the UnitedStates
often containsabout4000 kg N per ha in the upper20 cm of
the soil profile.However,usuallyless than 5%of this indigenous supply is availablefor crop uptakein a given season.
Thus, the annualcrop yield is determinedprimarilyby the
amountof Nr added.Nearlyall of this addedNr is lost from
most agroecosystemsover the courseof a year.On a global
basis,about 120Tg N fromnew Nr (fertilizerand cultivationinducedBNF)and about50 Tg N frompreviouslycreatedNr
(e.g., crop residue,animalmanure,and atmosphericdeposition) is addedannuallyto cropagroecosystems(Smil2001,
2002). Of this amount,about 33 Tg N per yearis consumed
by animalsand about 16 Tg N per yearis consumedby humans (figure3). The remainder(about 121Tg N peryear)is
lost to the atmosphere(as NOx,NH3, N20, and N2) or to waters (as dissolvedand particulateNr) or is partof the material reintroducedto crop systemsduringthe next cropping
cycle.Smil (1999) estimatesthatonly a smallamount (about
4 Tg N per year) of the 170 Tg N per yearintroducedaccumulatesin cropagroecosystems.Generally,the moreNr that
is addedto cropagroecosystems,the more is lost throughair
and waterpathways.Once lost, the releasedNr can cascade
throughnaturalecosystems,whereit alterstheirdynamicsand
THE
AGROECOSYSTEM
Nr
inputs
50
" Cropland 49
S'Io121
, AFO
1
Humans 4
Fromfish.
Sgrazrs
,8r an w25
Lossesto soil, airandwater
Figure3. Majorreactivenitrogen (Nr)flows in cropproductionand animal production
componentsof the global agroecosystem.Croplandscreatevegetableprotein through
primaryproduction;animal productionutilizes secondaryproductionto createanimal
protein. Reactivenitrogeninputs representnew Nr, createdthroughthe Haber-Bosch
processand throughcultivation-inducedbiologicalnitrogenfixation, and existingNr that
is reintroducedin theform of crop residues,manure,atmosphericdeposition,irrigation
water,and seeds.Portionsof the Nr lossesto soil, air, and water are reintroducedinto
the croplandcomponentof the agroecosystem(Smil2001, 2002). Numbersrepresent
teragramsof nitrogenper year;AFO,animal feeding operations.
April2003/ Vol.53 No.4 * BioScience345
Articles
in manycasesdecreasestheirabilityto provideecosystemservices (table 1).
Animal agroecosystemsproduce dietary protein (milk,
eggs, and edible meat) from the consumption of proteins
produced by crop agroecosystems.Just as in crop agroecosystems, most of the Nr that enters the animal agroecosystemis lost to the environmentoverthe courseof a year.
AnimalsreceiveNr primarilythrough the consumption of
aminoacidsin grainsandothervegetation.Theefficiencywith
which food animals use N from forage and grain varies
greatly.Typicalrates of N-use efficiencyfor production of
human-digestibleprotein from feed grains and forageson
farmsareabout 50%to 60%for fish, about40%to 50%for
poultry,about35%to 40%for dairy,and about 15%to 30%
forbeef.On a globalbasis,33 Tg N peryearof grainproduced
by the cropagroecosystemis fed to animals(figure3). Of this
amount,about 15%is consumedby humans.The remaining
Nr is lost as manure and waste (Smil 2001, 2002). The
manure can be reused as fertilizer,but the Nr is often lost
through air emissions (e.g., NH3, N20, NO, and N2) and
throughleachingof NO3-to groundor surfacewaters.
Humansconsumeabout25 TgN peryear,mostlyas dietary
protein.Of this amount,64%comes from grain,20%from
CAFOs,andabout16%fromfishandpasturegrazinganimals
(figure3).
A portionof the Nr addedto agroecosystemsis denitrified
back to nonreactiveN2 in systemsthat have high NO3- or
NH4+concentrations,high organicmatter,and low 02 concentrations,such as agriculturalfieldswith high watercontent (e.g., wetlandrice), those that receivelargeamounts of
precipitationovera shorttime period(e.g.,springrains),and
anaerobicmanurestoragesystems.Unfortunately,
the amount
in
denitrification
agroecosystemsis poorly
ofN2 lost through
known. Oenemaand colleagues(2001) reviewedNOx,N20,
andN2 emissionsfrompastures;fromanimalhousingsystems;
frommanureslurryin tanks,silos,andlagoons;frommanure
heaps;and fromslurryand manureappliedto the soil. They
concludedthatour knowledgeof gaseouslossesfrom animal
manure is greatestfor NH3 and successivelyless for N20,
NO, and N2.Smil (1999) estimatesthat on a globalbasis6%
is denitrifiedto N2.
to 12%of the Nr addedto agroecosystems
In an analysisof agroecosystemsin the GreatPlainsregionof
the United States,Del Grosso and colleagues (2001) used
modelto showthatN2 fluxesweresmallcomthe DAYCENT
pared with NO and N20 fluxes, primarilybecause of the
of the region.Theyestimatethatless
semiaridcharacteristics
than 5%of the appliedNr is lost as N2. Forlargewatersheds
of the easternUnited States,van Breemenand colleagues
(2002) estimateby differencethat up to 49%of the Nr input
to agroecosystemsis denitrified.In the Netherlands,with
high levelsof Nr production,30%to 40%of the Nr applied
is eitherstoredor denitrified(Erismanet al.2001).Theselarge
differencesreflectin partregionalvariabilityin the conditions
that promote denitrification (e.g., soil moisture) and the
generaluncertaintyof the magnitudeof denitrification.
346 BioScience s April2003 / Vol.53 No. 4
In summary,global crop agroecosystemsreceive about
75% of the Nr createdby human activity (Gallowayand
to othersystems
Cowling2002).Mostof thisNr is transferred
the
N
a
much
smaller
cascade;
along
portion globally is
denitrifiedto N2 (table1). Improvingthe efficiencyof N use
in majorgrainandanimalproductionsystemswillrequirecollaboration among ecologists, agronomists, soil scientists,
agriculturaleconomists,and politicians.A greatneed exists
for accuratemeasurementsof actual fertilizerN-use efficiency,N losses,andloss pathwaysin majorcropand animal
systems.Onlyin thiswaycanwe (a) identifyopportunitiesfor
increasedefficiencyof N use through improved crop and
soil management;(b) quantify N-loss pathwaysin major
food crops,includingCAFOs;and (c) improvehuman understandingof local, regional,and globalN balancesand N
losses from majorcrop and animalsystems.
Forests. Forestscan be a major reservoirand a short- to
long-termsinkwithin the N cascade.TotalNr stocksin soils
and biomass can rangeas high as 500 g N per squaremeter
(m2). Inputsof Nr in unpollutedregionsare0.1 to 0.2 g N per
m2per yearbut can reach5 or,very rarely,10 g N per m2per
year(Dise andWright1995).Outputsas dissolvedorganicN
in steamwaterare low and relativelyconstant across sites
(e.g.,Goodaleet al.2000),whiledissolvedinorganicN (DIN)
loss is quite variableand can be as low as zero or equal to
deposition,dependingon foresthistoryand condition (Dise
et al. 1998,Gundersenet al. 1998,Fennet al. 2003a).In general,this meansthatNr residencetime withina forestis measuredin hundredsto thousandsof years,and thus thereis a
substantialopportunityfor lags in the N cascade.However,
human activitycan shortenthis residencetime eitherby increasinginputsor by removingNr throughharvests,fires,or
conversionto agriculture.Largereservoirsize and relatively
low turnoverrates mean that human-induced changes in
the Nr statusof forestscan havelong-termeffects,and previouslandusehistorycanplaya largerolein conditioningforest responseto Nr additions(Goodaleet al. 2000,Aberet al.
2003).
Our understandingof the responsesof historicallyNrlimited foreststo increasesin Nr depositionhavebeen presentedin summarydiagramsof the processknown as N saturation(figure4;Aberet al. 1998). Fourgeneralstagesalong
this continuum have been discussed.In highly Nr-limited
(stage0) systems,low Nr availabilityis reflectedin low foliar
N contentand low net primaryproductivity.Plantsand root
and
symbionts compete effectivelyfor mineralized
while N20
net nitrificationand NO3-leachingareminimal,NH4,
effluxis low to undetectable.In stage 1, increasedNr depositiongraduallyrelievesNr limitationson biologicalfunctions.
Eitherthrough plant uptake or through direct incorporation into soil organic matter,added Nr enters into the N
cycle of the forest and increasesmineralizationand cycling
rates.FoliarNr increases,as does productivity.
Therearetwo criticalthresholdsin the N saturationprocess.
The firstis induction of net nitrification(stage2). Thus,the
Articles
presenceof net nitrificationand extractablesoil NO3- arekey
indicatorsof ecosystemNr status. Field experimentshave
shown that there can be a significant delay between the
initiationof Nr additionsandthe inductionof detectablerates
of net nitrification(Magillet al. 2000). Both NO3- leaching
and N20 effluxesarelow but detectableduringthis period.
The second criticalthresholdoccurswhen Nr becomes a
nonlimitingelementfor plantgrowth(stage3). At thispoint,
biologicalretentionprocessesbecomelesseffective,andNO3leaching losses increasesubstantially.Effluxesof NO and
N20 also may increasebecauseof nitrificationor denitrificationprocesses(Davidsonet al. 2000), which may become
significantif soilsareimperfectlyor variablydrainedsoils.In
stage 3, experimental additions of Nr may decrease tree
growth(e.g.,Magillet al. 2000), while decreasesin Nr depositionmayincreasetreegrowth(Beieret al. 1998,Boxmanet
al. 1998).ExcessNr may damageforestsby causingnutrient
imbalancesandby increasingsensitivityto factorssuchasfrost
and attacksby fungi (Erismanand de Vries2000).
Thereis substantialfielddocumentationthatN saturation
does occur and that it is relatedto increasesin atmospheric
Aber
inputs. In a companionarticlein thisissueof BioScience,
and colleagues(2003) analyzefoliar,soil, and surfacewater
chemistryfroma largenumberof sitesto testforpatternsthat
coincide with strong Nr deposition gradients across the
northeasternUnited States.Surfacewatersyield the clearest
patternsbecausethey integrateover largeareas;the surface
water data show increasingNr leachingin responseto increasingNr deposition (Aberet al. 2003). These resultsare
verysimilarto patternsobservedin Europeanforests.In an
analysis of 139 forests,Dise and colleagues (1998) found
that inorganicNr leachingincreasedwith Nr depositionas
well as with changesin humus compositionand soil acidity
(figure5).
How quickly Nr status or degree of N saturation can
changeis poorly known.VeryNr-poor sites receivingconcentrateddosesof DIN can retainover 100g N perm2 before
nitrificationand NO3- leaching are induced (Magill et al.
2000). Richersitesreceivingmore dilutesolutionscan show
an increasein NO3- loss immediately(Kahlet al. 1993).Less
N appearsto be requiredto move needle-leavedevergreens
from stage 1 to stage3 than is requiredfor broad-leaveddeciduousforests(Aberet al. 1995, 1998).Nitrogensaturation
may occur quicklynear largepoint sourcesof Nr (Erisman
and de Vries2000).
It is clearthat most Nr retainedin forestsis held in soils
(Nadelhofferet al. 1999, Magill et al. 2000). Recent work
suggeststhateitherabioticreactionsbetweenDIN andsoil organicmatteror assimilationand conversionby mycorrhizae
maybe important(Aberet al. 1998,Johnsonet al.2000,Dail
et al.2001).Understandingthe kineticsand capacityof these
or other retentionmechanismsis key to predictingNr retention ratesand the role of forestsin the N cascade.
To summarizethe roleof forestsin the N cascade:(a) The
residencetimes and lag times of Nr in forestscan be yearsto
centuriesdependingon foresthistory,type,andNr inputs;(b)
the effects of Nr accumulation in forests are numerous,
mostlyrelatingto changesin forestandmicrobialproductivity
and function; (c) there is significantpotentialfor Nr to be
transferredto the atmosphereas NO andN20, and especially
to surfacewatersas NO3-, once Nr additionsor availand (d) relativeto inabilityexceedbioticrequirements;
with
Nr
in
areas
puts
high deposition,thereis a limited
to
be removed from the cascadeby
for
Nr
potential
meansofN2 formation.
Succession, N Deposition
Harvest,Fire,Agriculture
FoliarN
200
N
Mineralization
NPP)
S100
Soil C:NRatio
Methane
Consumption
>
Nitrification
Leaching,
N20 Efflux
0
0
2
1
3
Stage
Figure4. Changesin severalecosystemfunctions with increasingNr
availability or degreeofN saturation (modifiedfrom Aberet al.
1998).Abbreviations:C, carbon;N, nitrogen;N20, nitrous oxide;
NPP, net primaryproductivity.
Grasslands.Unmanaged grasslandsreceive most of
their Nr from BNF and atmosphericdeposition;the
lattersource is much more importantwhere deposition ratesare large.As with forests,temperategrasslands have the potential to be a major storagereservoir and a short- to long-term sink within the N
cascade.At the Konza Prairie(tallgrass)site, for example,Nr stocksin soils and in biomassareon the order of 625 g per m2 and 6 to 25 g per m2, respectively
(Blairet al. 1998). Inputsof Nr in unpollutedregions
are less than 1 g N per m2 per yearbut can reach 5 g
N per m2 per year (Gallowayand Cowling2002). The
residencetimes of Nr in grasslandscan be decadesto
centuries, because most biomass is subsurfaceand
decompositionratesareslow (Blairet al. 1998,Epstein
et al. 2001). Giventhe N-limitednatureof most grasslandsand the long residencetimes,thereis a largepotential for significantinternal cycling (including redistribution by grazing animals) and for Nr
accumulation.
o
April2003 / Vol.53 No. 4 BioScience 347
Articles 4
Aquaticecosystems
60
a
m 50 -
Nin< 65% NH4+-N
Nin> 65% NH4 -N
This section discussesthe N cascadein threetypes of
aquatic ecosystems:(1) groundwater;(2) wetlands,
streams,lakes,and rivers;and (3) coastalsystems.
TheprimaryanthropogenicNr sourcefor
Groundwater.
groundwateron a globalbasis is leachingfrom agroS
*
ecosystems,althoughin some regionshumanwastedisposal can also be important(Puckettet al. 1999,Refsgaardet al. 1999,Hudak2000,Nolan and Stoner2000,
Nolan2001,vanEgmondet al.2002).Nitrateis themost
e 20
common Nr species(Burkartand Stoner2001). As in
othersystemsconsideredin this article,therearethree
AAOA
fatesof Nr in groundwater:accumulation,conversion
10
20
30
40
50
60
70
80 to N2, and distributionto other systemsthroughhyS
or atmosphericpathdrologicpathways(e.g.,as
NO3-)
as
or
ways (e.g., N20 NO). Althoughpollutioncan reDINflux(kg N perha peryear)
sult in high levels of NO3- in some groundwater
Throughfall
aquifers,the accumulationof N in groundwateris not
a
majorsink for the N mobilizedby human activityat
Figure5. Dissolved inorganicnitrogen(DIN, in kilogramsper hectare
either
globalor regionalscales.In regionsof intenseagriper year) lost in runoffand seepage.Siteswith throughfallDIN domicultural
activityin Europeandthe UnitedStates,the avnated by nitrogenfrom ammonium (NH4+-N)are shown in open trirate
of accumulationof NO3- in groundwater
erage
angles (Dise et al. 1998). Ni, representsN throughfallinputs.
amountsto at most a few percentof the N inputsfrom
fertilizerand other sources(Howarthet al. 1996).
Nr losses from grasslandscan occur through hydrologic
Nitrogen is lost from groundwater both through denitrification to N2 and through losses of Nr to surface
losses and atmospheric emission. Because precipitation
watersandthe atmosphere,but the relativemix of thesefates
ratesandthus runoffratesin grasslandsarelow,atmospheric
is site dependent,as is the residencetime of Nr in groundemissions are important, especiallyif fire is frequent;firearea
waterreservoirs.Forexample,in an intensiveagricultural
induced Nr losses can be approximatelyequal to input by
in west-centralMinnesota,about40%of the Nr thatentered
atmosphericdeposition.Forexample,in ungrazedregionsof
the groundwaterwas denitrified,and the rest accumulated
the KonzaPrairie,Nr lossesfromfirecan approximateor exin the aquiferwith little dischargeto surfacewaters(Puckceed atmosphericNr deposition inputs (Blairet al. 1998).
ett et al. 1999, Puckett and Cowdery2002). In the southHowever,some of theselossesarein the form of N2 (Crutzen
eastern United States, some systems have high losses of
and Andreae 1990). For biomass burning in general,
Kuhlbuschand colleagues (1991) estimate that N2 constiNO3- and concomitant low NO3- concentrations, while
other systemshavelow losses of NO3- and high NO3- contutes the largest flux of N gases emitted. Thus, if fire is
centrations (Nolan 1999). A review of several studies of
Nr
from
some
atmospheric deposition resulting
frequent,
denitrificationin groundwaterby Groffmanand colleagues
human action maybe returnedto the atmosphere,partlyas
Nr and partlyas N2.
(1998) found similardegreesof variability.
In additionto denitrificationthroughfire,Nr can alsobe
Althoughthe accumulationof Nr in groundwateris not a
convertedto N2 and lost from the grasslandthroughmicroregionallyor globallyimportantsink relativeto the amount
do pose
of Nr created,theeffectsof elevatedNr in groundwater
soils
are
because
most
bialdenitrification.
However,
grassland
a significanthuman healthrisk,becausedrinkingwatercan
well aerated, conversion of Nr to N2 through microbial
become contaminated.In the human body, NO3- is condenitrificationis probablynot an important process (Del
to nitrite,whichcan causemethemoglobinemiaby inverted
in
the
accumulated
If
et
retained
al.
Grosso
2001).
grassland,
of
loss
in
and
Nr canleadto increases productivity
terferingwith the abilityof hemoglobinto takeup 02. Most
biodiversity
cases of methemoglobinemiaoccur afterconsumingwater
and
Howarth
2000).
(Tartowski
suswith
are
animal
for
Grasslandsmanaged
high concentrationsof NO3; infantsareparticularly
production(e.g.,cattle)
treatment
who
receive
are
as
Nr.
The
adloss
of
added
with
to
much more"leaky"
kidneydialysis
people
ceptible,
respect
dition of fertilizeror grazinganimalsincreasesthe amount
(Follettand Follett2001). Forthis reason,the WorldHealth
of Nr that is availablefor loss, especiallythroughthe atmosOrganization recommends that NO3- concentrations in
and
and
drinkingwatershouldbe lessthan 10 milligrams(mg) N per
Hutchings 1997]
phere (e.g., NH3 [Sommer
N20
exceedthislevel
liter.In the UnitedStates,NO3-concentrations
the
effective
in
[Fowleret al. 1997]).Thus, managedecosystems
4 of the 33
from
than
of
in
more
15%
unless
than
for
to
be
the
have
residencetimes
groundwatersamples
potential
as
sourcesof
used
most
commonly
majorregionalaquifers
managedsystems.
40-
40
348 BioScience * April2003 / Vol.53 No. 4
Articles
drinkingwater(Nolan and Stoner2000). Othereffectsassociated with elevated concentrations of NO3- in drinking
waterincluderespiratoryinfection,alterationof thyroidmetabolism,and cancersinducedby conversionof NO3-to Nnitroso compoundsin the body (Follettand Follett2001).
In summary,groundwatersystemsareaccumulatingNr at
low ratescomparedwith ratesof human mobilizationof Nr
in the landscape,but the effects of contaminatedgroundwatercan nonethelessbe significant.Nr is lost from groundwaterthroughdenitrification,throughadvectionof NO3- to
surfacewaters,and throughconversionto gaseousNr forms
that diffuseor flow to the atmosphere.Justas thereis a lag in
Nr releasein forests because of N saturationphenomena
(figure4), there is also a lag for Nr releasefrom groundwaterto surfacewater,althoughthis is highlyvariableamong
sites (Groffmanet al. 1998,Puckettand Cowdery2002). At
sometime,the Nr introducedinto groundwaterwill be transferredto surfacewaterif the Nr is not permanentlystoredin
groundwateror denitrified to N2. If the inputs of Nr to
groundwater systems decrease, then the decrease of the
groundwaterNO3- burden can be delayedfor a significant
amount of time becauseof the significantresidencetime of
Nr in groundwaterreservoirs.
Wetlands,streams,lakes, and rivers.Surfacefreshwater
ecosystems consist of wetlands (e.g., bogs, fens, marshes,
swamps,and prairiepotholes),streams,lakes(includingartificialreservoirs),and rivers.Surfacefreshwaterecosystems
receivemostof theirNr fromtheirassociatedwatersheds,
from
BNF
within
the
and
from
atmosphericdeposition,
system.Niin
fixation
is
more
important eutrophic
generally
trogen
lakes and in some wetlands, where the process has been
found to contributebetween5%and 80%of totalNr inputs
(Howarthet al. 1988). Thereis limited potentialfor Nr accumulationwithin surfacewaterecosystemsbecausethe residencetime of Nr within surfacewaters,likethe wateritself,
is verybrief.Residencetimes may be relativelylongerin the
sedimentsassociatedwithwetlandsand somelargerlakes,but
they arestill shortwhen comparedwith the residencetimes
in terrestrialecosystems.
Despitea shortresidencetime, Nr cyclingin surfacefresh
watercan be very complex.In additionto dissolvedN2, inorganicoxidizedand reducedforms of Nr can occur,as can
organicformsof Nr.In mostheadwatersystems,the inorganic
formsof Nr (NO3-and NH4+)arepresentin low concentrationsunlessthe watersareassociatedwithN-saturatedforests,
grasslands,agroecosystems,or suburbanlandscapes.This is
primarilybecausethe intensecyclingof Nr in the terrestrial
portions of the watershedresults in little runoff of Nr to
streams.The little inorganicNr that does reachthe streams
in pristineregionsis usuallydenitrifiedor quicklyincorporatedintobiomassby aquaticplantsandthenrecycledthrough
the hierarchyof consumersand decomposersunlessNr concentrationsarehigh (Petersonet al. 2001). However,many
headwaterstreamsand lakes are now in highly disturbed
landscapesand thus havehigh NO3- concentrations,which
can leadto eutrophicationproblemslocallyor fartherdownstream.In addition,forheadwaterstreamsandlakesdraining
poorlybufferedsoils,increasedNO3- concentrationscan result in streamacidification,with resultantimpactson biota.
In undisturbedareasin the temperatezone, the major
terrestrialflux of Nr into surfacewatersmay be organicNr
in theformof detritusor dissolvedorganicmatterwashedinto
lakes and streams (Lewis 2002, Perakisand Hedin 2002).
Undisturbedtropicalregions can have significantlosses of
NO3- (Lewis et al. 1999). In the presenceof increasedatmosphericdepositionof inorganicNr or significantland-use
perturbations(e.g., urbanizationor agriculture)in the terrestrialwatershed,the amountof Nr deliveredto streamsand
lakesmay easilyexceedthe retentioncapacityof the aquatic
system.Therewill then be little delayin the transportof N
down the cascadeunlessthe Nr is denitrifiedbackto N2.As
discussedbelow,the potentialfor denitrificationin wetlands,
streams,lakes,and riversis large.
Wetlandscangenerallybe consideredaggradingecosystems
wherethe additionalNr can come from adjacentwatersand,
in some cases,from BNF and atmosphericdeposition.Wetlandsareso efficientat removingNr throughdenitrification
(seebelow)thattheyarefrequentlyconstructedto removeNr
from effluent waters from a number of human activities.
However,humans arealso acceleratingwetlandremoval.In
many areasof the world,wetlandsarebeing drained;nearly
half the wetlandsin the United Stateshave been destroyed
since 1780 (Gleick1993).Whilewetlandscan be efficientNr
sinks,their arealextentis limited (and becomingmore limited) comparedwith that of terrestrialand oceanic sinks.
In summary,the potentialforNr accumulationin streams,
lakes,rivers,and associatedwetlandsis small (table1).While
changesin Nr inputs to surfacewatersmay significantlyalter the internalcycles in these systems,from a global perspectivesuchchangesaremerelyextremelyefficientavenues
for propagatingthe effectsof the N cascadefrom higherto
lower components. Even though wetlands may delay or
preventthis transferlocally,and denitrificationmay shortcircuitsome of the Nr transportalongthe way,surfacefreshwaterecosystemsessentiallymoveNr fromthe mountainsto
the sea, ensuring that perturbations at one point in the
cascadequicklylead to changeselsewhere.
Coastalsystems. Coastalecosystems(e.g., estuaries)receive
most of their Nr from riverine and groundwaterinputs;
direct atmospheric deposition is an important source in
some systems,and inputs from the ocean are importantin
others.These inputs have increasedseveral-foldas a consequence of human activities(Howarthet al. 1996,Seitzinger
and Kroeze1998,NRC2000,Howarthet al.2002b).Because
of the dynamicnatureof coastalecosystems,thereis limited
potentialfor Nr accumulation.In addition,althoughthe potentialforNr transferto continentalshelfregionsis large,there
is limited transportto the shelf becauseof the high ratesof
*
April2003 / Vol.53 No. 4 BioScience 349
Articles(
denitrification(mostlyas N2), and the Nr that is transferred
is mostly convertedto N2 before its transportto the open
ocean.With coastalsystemsactingas Nr sinks,atmospheric
depositionbecomesa potentiallyimportantsourceof Nr for
the open ocean, especiallyin oligotrophicmidocean gyres
(figure2).
AlthoughNr has a short residencetime in coastalecosystems comparedwith terrestrialecosystems,the time it does
spendtherecanhavea profoundimpacton the coastalecosystem. Primaryproductionin most coastalrivers,bays,andseas
of the temperatezone is limitedby Nr supplies(Vitousekand
Howarth 1991, Nixon et al. 1996, NRC 2000). As a consequence,greaterNr inputslead to increasedgrowthof algae.
In moderation,this canbe viewedas beneficial,as it canlead
to increasedproductionof harvestablefish (Nixon 1988,Jorgensenand Richardson1996).However,high Nr inputs can
also lead to excessivealgalgrowth,or eutrophication.In the
United States,the increasedNr flux is now viewed as the
most seriouspollution problemin coastalwaters(Howarth
et al. 2000, Rabalaiset al. 2002). One-thirdof the nation's
coastalriversandbaysareseverelydegraded,andanotherthird
havebeenmoderatelydegradedfromnutrientoverenrichment
(Brickeret al. 1999).The situationis probablyequallysevere
in otherregionsof the globewherehumanactivityis leading
to highNr inputsto the coast(e.g.,theNorthSeaandtheBaltic
Sea).
In the tropics,P ratherthan N often limits relativelypristine coastalecosystems.However,increasednutrientloading
can shiftthesesystemstowardNr limitation(McGlatheryet
al. 1994,Howarthet al. 1995) and,as in temperate-zonesystems, Nr is a majorcontributorto coastaleutrophicationin
tropical coastal systems (Corredoret al. 1999, NRC 2000,
Rabalais2002).
One of the most obviousconsequencesof increasingNr inputs to coastalwatersoverthe past few decadeshas been an
increasein the sizeof watermassesthatareanoxic(completely
devoid of 02) or hypoxic (with concentrationsof 02 less
than 2 to 3 mg per liter).Theseso-calleddeadzones now occur in the Gulf of Mexico,the ChesapeakeBay,LongIsland
Sound,FloridaBay,the BalticSea,the AdriaticSea,and many
othercoastalareas(DiazandRosenberg1995,NRC2000).The
hypoxic water mass in the northern Gulf of Mexico has
grownin sizein recentsummersto about20,000squarekiloattributableto Nr pollution running
meters and is dclearly
down the MississippiRiver(Goolsbyet al. 1999,Rabalaiset
al. 1999,2002, NRC 2000).
Othermajoreffectsof increasingNr in coastalregionsinclude loss of seagrassbeds, macroalgalbeds,and changesin
coralreefs(Lapointeand O'Connell1989,Valielaet al. 1997,
Howarthet al.2000,NRC2000).ReactiveN additionscan increasethe incidenceand durationof harmfulalgalblooms
(NRC 2000). Anoxic or hypoxic events and harmful algal
bloomscanleadto fishkills.ReactiveN pollutioncanalsolead
to more subtleeffects,with alterationsof marinefood webs
that leadto decreasedfish production(NRC2000). Reactive
350 BioScience * April2003 / Vol.53 No. 4
N pollution is a leading cause of loss of biotic diversityin
marineecosystems(NRC 1996,2000).
In summary,Nr inputs to coastal ecosystems have increasedsignificantlyoverthe lastfew decades.Althoughmost
Nr is eventuallydenitrifiedto N2 within the coastalecosystems and associatedshelf,Nr pollution has significantand
widespreadimpactson variousecosystemcomponentsand
on human health (table 1).
Denitrificationpotentialin the wetland-stream-riverestuary-shelfcontinuum.Alongthe entireaquaticcontinuum,
fromwetlandsto headwaterstreamsto the continentalshelf
and eventuallyto the open ocean, not only is Nr rapidly
cycledamong the variousforms (e.g., NH4, NO3-, and particulateand dissolvedorganicN), thereis greatpotentialfor
loss of Nr from the biosphere through the conversion of
NO3-to N2 (denitrification).In this sectionwe aim to identifyplacesalongthe N cascadewhereNr canbe convertedback
into N2 or N20.
Conditionsrequiredforthisconversioninclude(a) thepresence of NO3-or nitrite(referredto collectivelyin this section
as nitrate),(b) the presenceof labileorganicmatter,and (c)
the absenceor low concentrationof dissolved02. The most
activesites for denitrificationin aquaticsystemsarebenthic
sediments,which are often anoxic below the first few millimeters,eventhoughthe overlyingwateris well oxygenated.
Evenwhen nitrateconcentrationsarelow in sediments,denitrificationrates could be high if other conditions are favorable,becauseof the close spatialand temporalcoupling
alsocanocof nitrificationanddenitrification.
Denitrification
curin anoxiczoneswithinthewatercolumn,withthe primary
sourceof nitratecoming from outsidethe zone of anoxia.
Increasedinputsof Nr fromanthropogenicsourcescanincreaseratesof denitrificationalong the entire aquaticcontinuum.As Nr inputs increase,they can increasethe nitrate
concentrationin the watercolumn and thus increasethe diffusivesupplyof nitrateto the sediments.Increasedinputsof
Nr can also enhanceprimaryproduction,particularlyin Nrlimited estuarineand continentalshelfwaters,thus increasing organicmatterdepositionto the sedimentsandsubsequent
sediment nitrificationand denitrification.However,if Nr
inputs result in the water column becoming anoxic, sediment nitrification and consequently denitrification can
markedlydecrease.Forexample,in the ChesapeakeBay,denitrificationin sedimentsunderlyinganoxicwaterswas low
comparedwith periods of well-oxygenatedbottom waters
(Kemp et al. 1990). However,the net effect of persistent
anoxicwaterin estuarineandcontinentalshelfsystems,where
nitrateconcentrationsand ratesof wateradvectionarelow,
on total denitrificationrates (in sedimentplus water)is not
well documented.On the other hand, in riverssuch as the
Seineand Scheldt,with high inputsof nitratefromupstream
agriculturalsources,moreNr was removedin the riverby denitrificationwhen the water was severelydepleted in 02,
comparedwithtimesafterimprovementsin sewagetreatment
Articles
whenthe 02 concentrations
in the riverincreased(Billen
estuariesor discharged
bylargeriversdirectlyontothecontinentalshelf.Inestuaries,
waterresidence
timeagainisanim1990).
Theproportionof Nr inputsremovedthroughdenitrififactor
the
portant
controlling proportionof Nr inputsthat
cationhas a similarrangefor lakes,rivers,and estuaries
areremovedby denitrification.
A similarfunctionalrelafromlessthan10%to morethan80%).Istherean
the
to
ones
demonstrated
forlakesandriversapplies
(generally
tionship
overallecosystempropertythatcan accountfor the wide
to estuaries.
Inestuaries
withawaterresidence
timeranging
intheproportion
oftheNrinputsremoved
from
0.1
month
to
over
a
the
total
Nr
variability
through
year,
inputsremoved
denitrification?
Theresidence
timeof wateris animportant
denitrification
from
less
than
to approxi10%
by
ranged
factorcontrollingremovalof Nr throughdenitrification
in
75%
et
al.
(Nixon
1996).
mately
Theeffectof waterresiNr thathasnotbeenremovedbydenitrification
in rivers
streams,lakes,rivers,andestuaries.
dencetimeis probablyrelatedto thetimethatNr hasto reorestuaries
issubjectto removal
onthecontinental
shelf(e.g.,
actin theecosystembeforeit is transported
to the adjacent
DevolandChristensen
1993,LaursenandSeitzinger
2001).
downstream
betweentheproportion
In fact,Nr removedby denitrification
in shelfsediments
system.Therelationship
of Nrinputsthataredenitrified
andthewaterresidence
time
exceedsNr exportedto coastalareasbyrivers.Deprobably
in anaquaticenvironment
wasoriginally
shownforwell-oxytailedNrbudgetsforcontinental
shelfregionsthroughout
the
North Atlanticbasin suggest that denitrificationin contigenatedandwell-mixedshallowlakes(Kellyet al. 1987).
Thisrelationship
wasextended
to riverreachesandreservoirs
nentalshelfsedimentsis equalto or greaterthaninputsof Nr
and indicatedthata smallerproportionof the Nr inputs
fromland-basedsources(SeitzingerandGiblin1996).Theadwereretainedin a riverreach(often5%to 20%)compared
ditionalNr requiredto supportthe estimateddenitrification
withmanylakesandreservoirs
ratesin shelf sedimentsprobablycomes from the transport
(fromabout10%to morethan
this relationship
for
of Nr fromoceanicregionsacrossthe slope-shelfboundary.
90%;Howarthet al. 1996).Recently,
streamandriverreacheswasincorporated
intoa streamand
Confirmingthis observationin another region, Chen and
rivernetworkwatershed
modelthatwasappliedto 15river
ratein the East
Wang(1999)foundthatthe net denitrification
networksin thenortheastern
UnitedStates(Seitzinger
et al.
ChinaSeashelfis greaterthanthe totalriverinesupplyto the
2002).ThemodelresultsindicatethattheNr removaleffiregion.Additionalmeasurementsof denitrificationand Nr
ciencyvariesthroughouta networkof riversandstreams.
inputs for other continental shelf regions throughout the
insmallerstreams
Reaches
removea greater
of the
world'soceans are needed to betterunderstandthe Nr balproportion
Nrinputsto thosereaches
thanreachesin largerriversperse.
anceandfinalfateof land-based
Nr inputs.
thetotalamountof Nrremovedbydenitrification
In summary,
However,
nearlyallof theNr thatis injectedintosurin downstream
isgreater
becausethetotalNrinputs,
facewatersis denitrified
reaches,
alongthestream-river-estuary-shelf
fromtheupstream
arelarger.
Atthescale
continuum(figure6).Whilemostof thisNr is converted
to
watershed,
primarily
of awholewetland-stream-river
thecumulative
efa
is
fraction
converted
to
and
NO.
Model
estimates
network,
N2,
N20
fectof continuedNrremovalalongtheentire
flowpathfromwetlandsto smallstreamsto
Denitrificationreduces the downstream transport of N
riversdownstream
canresultindenitrifilarger
cationof asmuchas30%to 70%of thetotal
externalNr inputsto the river,althoughthe
of Nrinputsremovedbydenitrifiproportion
cationin a particular
reachis generallyquite
1
small(often1%to 20%).
alterations
to rivers,suchaschanPhysical
candecreasewaterresidencetime
nelization,
30-70%entering
andthusdecrease
denitrification
withina river.
G-N.
Channelization
of riversalsodestroys
riparian
whichhavea considerable
wetlands,
capacity
for Nr removal(Billenand Garnier2000).
Wetlandrestoration
andthe construction
of
estuaries denitrified
newwetlands
havebeenconsidered
asoptions
fordecreasing
Nrloadingatlocalandregional
> 80%entering
scales.Whileindividualwetlandsareclearly
shelves
denitrified
activesitesfordenitrification,
theoverallcontributionof wetlandsto Nr removalat the
whole-watershed
scalegenerallyis not well
] Ocean
documented
andwarrants
furtheranalysis.
Reactive N not removed within the Figure6. Thetransportof reactivenitrogenfromterrestrialto oceanicsystems
at eachstepalongtheriver-estuarine-continental
wetland-rivernetworkis transportedto decreases
shelfsystem.
-
351
April2003/ Vol.53No.4 o BioScience
Articles i
of globalN20 emissionssuggestthatrivers,estuaries,andcontinentalshelvesaccountfor approximately30%of the total
globalanthropogenicN20 emissions(Seitzingeret al.2000).
As injections of Nr to rivers increase,so will the rates of
creationof NO and N20 (Seitzingerand Kroeze1998).
Thenitrogencascade:Linkageswithotherelements
ElevatedatmosphericNr can increaseozone, increaseatmospheric fine particulateloadings, and enhance the impacts of aerosol sulfate on the atmosphericradiationbalance. These are not the only important linkages.Because
many naturalecosystemsareN limited (e.g., temperateand
borealforests,grasslands,and temperatecoastalwaters),the
increasedabundanceof Nr leadsto increasesin productivity,
whichin turnleadto increasesin uptakeof allotherelements
tied to productivity(e.g., calcium [Ca],C, P,potassium,and
magnesium).Eventually,anotherelement may replaceN as
the limitingelement.Forexample,when temperateforested
ecosystemsreachstage3 of N saturation,N becomesa nonlimiting element for plant growth (figure4). At that point,
something else becomes limiting, and the basic biogeochemicalnatureof the forestchanges.Otherpossiblelimiting materialsarebasecations,P,light,andwater(e.g.,Schulze
1989,DeHayeset al. 1999).
Matsonand colleagues(2002) discusshow the globalization of Nr deposition raises questions concerning consequencesof anthropogenicNr for ecosystemsin tropicalregions,whereP or Camost likelylimitsproductionin humid
tropicalforestandsavannaecosystemswith highlyweathered
soils.In manyof these systems,Nr mayalreadybe a nutrient
in excess,so manytropicalhumid forestsmaybe naturallyN
saturated(Hall and Matson 1999).
Thenitrogencascade:Possibilitiesfor intervention
Nr accumulationin environmentalreservoirsenhancesthe
N cascadeand its consequenceson people and ecosystems.
However,just as anthropogenicactivitieshave substantially
increasedthe rateof Nr formation,it is possibleto intervene
at criticalpoints alongthe N cascadeand makeNr less abundant.Therearetwo waysto decreasetotalNr:(1) decreasethe
rateof Nr creationduringenergyandfood productionor (2)
convertNr backto N2 followingNr creationand use.
Decreasingthe rateof reactivenitrogencreation.Thereis no
benefit to the Nr createdduringfossil fuel combustion.Nitrogen oxides are formed inadvertentlyduringcombustion
eitherthrough oxidation of fossil-organicNr in the fuel or
throughoxidationof atmosphericN2. In both cases,the options for significantlydecreasingNO emissionsarenumerous, eitherby using an alternativemethod to provideenergy
fuelcells)or by eliminatingNOxand
(e.g.,hydrocarbon-based
other Nr species from the combustion products (Bradley
and Jones2002, Moomaw 2002). It is now technicallyfeasible to decreaseNr creationfrom fossil fuel combustionto a
pointwhereit becomesjusta minordisturbanceto the global
352 BioScience * April2003 / Vol.53 No. 4
cycle(Cowlinget al. 2002). If that occurs,NO depositionto
global ecosystemswill decreaseby about half, and the remainingmajorNOxsourceswill be emissionsfrombiomass
burning and agriculturalsoils. Nr deposition to regional
systemswill also decrease.In the northeasternUnitedStates,
if fossilfuel combustionwereno longera sourceof NOx,Nr
deposition to the researchsites in the study by Aber and
colleagues(2003)woulddecreaseby morethan50%(Ollinger
et al. 1993). Kroezeand colleagues(2001) examinedthe effectof institutingthe maximumtechnicalpotentialto decrease
emissionsin Europeon DIN exportby Europeanrivers
NOx
in the year2050.This scenarioassumedthat all countriesapply maximum emission control in electricity generation,
transport,and industry.This resultedin a decreaseof approximately80%in NOydepositionto Europeanwatersheds
relativeto a business-as-usualscenario.
In food production,thereis a benefitto Nr creationthrough
the Haber-Boschprocessand through cultivation-induced
BNE However,thereis also inefficiency.Of about 170 Tg N
of Nr added to global crop agroecosystemsin 1995, only
about 12% entered human mouths (figure 3; Smil 1999,
2002). Most of the restwas distributedto the environment
without servingthe purposefor which it was created.
Thereis ampleopportunityto increasethe efficiencyof Nr
use in food productionandthusdecreasethe Nr creationrate.
Therearemanywaysof achievingthis goal:(a) increasethe
efficiencyof N use in cropand animalagriculture(Cassman
et al. 2002), (b) increaseNr recyclingwithin agroecosystems
(i.e.,if Nr is not incorporatedinto food the firsttime around,
send it aroundagain;Smil 2002), (c) increaseuse of cultivation-inducedBNF (Royet al.2002), (d) provideincentivesto
reduceoverfertilization(Howarthet al. 2002b), and (e) redistributeNr from areaswith high Nr productionto areas
wherethereis a need for Nr for food production(Erismanet
al. 2001).
CAFOsofferlargeopportunitiesforimprovementof N-use
efficiency.In recentdecades,livestockand meat processing
industrieshavebeentransformedin manycountries.Bothverticaland horizontalintegrationhavegreatpotentialto maximizeN-use efficiencywithintegratedeconomicandadvisoryservicelinkagesamongfarmers,feedsuppliers,animal-rearing
advisers,and food-processing companies. These changes
often lead to largelyunforeseenNr-inducedenvironmental
problems,mainly on local and regional scales.Thus, emphasison economicefficiencywithoutattentionto Nr-induced
rather
healthand environmentalrisksleadsto externalization
than internalizationof these realcosts.
If societies decreasedtheir consumption of meat, there
wouldbe lessdemandforNr createdto producefood (Bleken
1997,Kroezeet al.2001,Smil2002).Howarthand colleagues
(2002a)projectthatif the US populationadopteda Mediterraneandiet of approximately6.3 kg meatper capitaperyear
(about one-seventhof the supplyin the UnitedStates),total
inorganicN fertilizerconsumptionwould decreaseto about
6.9 Tg N per year by 2030-a 65% decrease.Kroezeand
Articles
colleagues(2001)reportsimilarfindingsforthe UnitedStates
and Europe.
Theprojectionsfor futureNr creationthroughthe HaberBosch processdepend to a largeextenton the degreeof intervention and on assumptionsand preferencesregarding
human diets.A studyof futurefertilizerrequirementsup to
the year2030 projectsthat annualincreasesin fertilizeruse
will range from 0.7% to 1.3%,dependingon assumptions
aboutN-use efficiency(FAO2000, Fixenand West2002). In
absoluteterms,this means that N fertilizeruse in 2030 will
rangefromabout96 Tg N peryearto 118Tg N peryear,compared with about 78 Tg N per year for the base period
1995-1997.Tilmanand colleagues(2001)projectthatN fertilizeruse will increasefrom 87 Tg N peryearin 2000 to 135
Tg N per yearin 2020.Whilethe actualproductionof Nr in
the futurefor fertilizeruse is uncertain,it is clearthat N demands for food productionwill increase.
theconversion
ofreactive
to N2.Inmost
nitrogen
Increasing
environmentalreservoirs,N2 formationis verylimited (e.g.,
atmosphere,grasslands,andforestedecosystems)or counterproductiveto the purposeof the system(e.g.,agroecosystems).
The wetland-stream-river-estuary-shelfcontinuum is the
only systemthat providesthis servicenaturally,at ratesthat
arelargerelativeto Nr inputs.However,beforeNr is converted
to N2 in the continuum,a numberof detrimentaleffectsoccur in forests,grasslands,and surfacewaterecosystems.For
this reason,the next opportunityfor interventionis immediatelyafterNr is used as a resourcebut beforeit is distributed to the environment.While there are probablyother
suitablepoints for intervention,we choosetwo: (1) Nr losses
from animal and human waste and (2) Nr transferfrom
agroecosystemsto surfacewaters.
Globally,animalsand humans excreteabout 75 Tg N per
year and about 23 Tg N per year,respectively(Smil 1999).
While this is about 80%of the Nr createdfor food production, some of it is reused,and not all of the remainderis easily collectible.Foranimals,of about 75 Tg N per year,about
28 Tg N per yearareproducedin CAFOs,and of that about
18 Tg N per year are recycledto agroecosystems,leaving
about 10 Tg N per yearas easilycollectiblewasteNr.Forhumans,in 2000,47%of the world'spopulationlivedin an urban environment;of this 47%,84%had theirwastecollected
by a sewagesystem(6 March2003;www.worldbank.org/data/
So, of about 23 Tg N per yearcontainedin
dataquery.html).
humanwastethatis generatedannually,municipalsewageoperationscollectabout9 Tg N peryear.Thus,of about 100Tg
N per yearproducedas Nr-containingwasteby animalsand
humans,about21 TgN peryearis not reusedandis easilycolinlectible,whichincreasesthe potentialfor a "denitrification
tervention"unlessothervalue-addedproductscan be made
using this N-rich resource (Cassmanet al. 2002, Oenema
and Pietrzak2002).
The secondinterventionpoint is betweenagroecosystems
and streamsor rivers.Acceptingthat Nr leakageswill occur
from most agroecosystemsand some forests, there is an
opportunityto takeadvantageof the factthat denitrification
does occur in wetlandand riparianareas(Hill 1996,Hill et
al.2000,Steinhartet al.2000,Mitschet al.2001), and specific
managementactivitiescan be used to createan environment
that will increase this rate (e.g., Schipper and VojvodicVukovic 2001). However,it is not enough to increasedetheproductionof N2 mustalsobe optimizedrelnitrification;
ativeto N20 formation.
Summary
The atmospheredirectlyreceivesabout15%of the Nr created
by human activitiesas a consequenceof energyproduction;
all of it is deposited as Nr. Agroecosystemsreceive 75%,
most of which is eithertransferreddirectlyinto the atmosphereor hydrosphereor lost to the environmentduringthe
processof food productionand consumption.The remaining 10%of the Nr is usedin industrialprocesses.Theprimary
beneficial effect of Nr introduced into agroecosystemsis
human nutrition;other effectsoccur as the Nr from agroecosystemscascadesthroughother environmentalsystems.
In the atmosphere,increasedNr concentrationshave directandindirectimpactson humanand ecosystemhealthon
a regionaland globalbasis.Most of the Nr emittedto the atmosphereis depositedbackto Earth'ssurfaceafterhours to
days.IncreasedNr depositionto grasslandsand forestshas a
residencetime of yearsto centuries,introducingthe potentialfor a largelagtime in the cascade.Becausethe production
of N2 is smallrelativeto Nr inputs,N accumulatesin a reactive form, resultingin initially increasedproductivityand
some loss of biodiversity,and ultimatelysome loss of productivity.Severalregionsof the world havealreadyreached
the point whereaccumulationhas slowed and loss of Nr to
the atmosphereand hydrospherehas increased.
Transferof Nr from the atmosphere, agroecosystems,
forests, and grasslands into the wetland-stream-riverestuary hydrospherecontinuum is increasingand has resultedin numerouseffects,includingacidification,eutrophication,and human healthproblems.However,throughout
the continuumthereis a largepotentialfor conversionof Nr
to N2, especiallyin wetlands,largerivers,estuaries,andthe continentalshelf.Thus,while the N cascadebegins at the point
of Nr creation,and while Nr will accumulatein and cycle
among,most terrestrialsystems,the cascadereachesan end
at the continentalmargins,where its primarycontinuation
is N20 productionduringnitrification.
Acknowledgments
A topic of this scalerequiresexpertisefrom a diversecollection of disciplines.In that regard,we aregratefulfor the advice andcounselof BethBoyer,EricDavidson,LindaDeegan,
SteveDel Grosso,RussellDickerson,NancyDise,HowardEpstein, Christy Goodale, Peter Groffman, Bill Keene, Tom
Nolan, and JeffStoner.We also appreciatethe constructive
commentsof TonBresser,PaulFixen,RickHaeuber,Kathleen
Lohse, JerryMelillo, Bill Moomaw, Oene Oenema, Nancy
Rabalais,RabindraRoy,VaclavSmil,Rob Socolow,Klaasvan
*
April2003 / Vol.53 No. 4 BioScience 353
Articles
Egmond,Dan Walters,FordWest,and XunhuaZheng,who
providedcommentsaboutthe N cascadeduringthe Plenary
SpeakerWorkshopheld in April2001 beforethe SecondInternationalNitrogenConferenceheld the followingOctober.
We thank MaryAnn Seifertfor putting the paper into the
correct format and Sue Donovan for assistancein figure
preparation.JamesN. Gallowayis gratefulto the Ecosystems
Centerof the MarineBiologicalLaboratoryand the Woods
Hole OceanographicInstitutionfor providinga sabbatical
home to writethis paperand to the Universityof Virginiafor
the SesquicentennialFellowship.
cited
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