Journalof
AppliedEcology
1996,33,
1441-1450
The vegetation
N:P ratio:a newtoolto detectthenature
ofnutrient
limitation
WILLEM
KOERSELMAN
and ARTHUR
F.M. MEULEMAN
Kiwa N. V. Research& Consultancy,
PO Box 1072,3430 BB Nieuwegein,The Netherlands
Summary
1. Nutrientlimitation(mostlyN or P) is a drivingforcein ecosystemdevelopment.
Currenttechniquesto determinethenatureof nutrientlimitationuse laboriousfertilizationexperiments.
2. It was hypothesized
thattheN:P ratioofthevegetationdirectly
indicatesthenature
of nutrient
P
limitationon a community
level(N vs. limitation).This hypothesis
was
testedby reviewingdata on fertilization
studiesin a varietyof European freshwater
wetlandecosystems(bogs, fens,wet heathlands,dune slacks,wet grasslands).In a
subsetof the data (dune slacks) between-site
variationand within-site
intraspecific
interspecific
variationin nutrientcontentand N:P ratio was studiedin fiveplant
species.
3. A reviewof 40 fertilization
studiesreveals that an N:P ratio > 16 indicatesP
limitationon a community
level,whilean N:P ratio < 14 is indicativeofN limitation.
At N:P ratiosbetween14 and 16,eitherN or P can be limitingor plantgrowthis colimitedby N and P together.In onlyone out of 40 fertilization
studies,theN:P ratio
gave a falseindicationof thenatureof nutrientlimitation.MeasuringtheN:P ratio
ofthevegetationis a simpleand cheap alternative
to fertilization
studies.The method
can onlybe used underconditionswhereeitherN or P controlsplantgrowth.
4. The datasetcontainsa largevarietyof vegetationtypesand plantspecies,and 11
of the40 siteswerenear-monocultures.
This suggeststhatinterspecific
in
differences
criticalN:P ratiosamong speciesmay be insignificant.
However,a rigoroustestof
thishypothesisis required.
5. A surveyin 18 dune slacks showedlargewithin-site
variationin N:P ratioamong
fivespecies(Calamagrostisepigejos,Phragmites
australis,Lycopuseuropaeus,Mentha
aquatica and Eupatoriumcannabinum).
The N:P ratios of the fivespeciessuggested
thatwithinplantcommunitiesspeciescan be differentially
limitedby N or P. Morewith
an
N:P
ratio
that
over,species
werefoundat siteswhereN
suggestedP-limitation
controlledcommunity
biomassproduction,and viceversa.Between-site
intraspecific
variationin N and P contentsand N:P ratioswas also large,and about equal forthe
fivespecies.This illustratesthe plasticityof plant specieswithrespectto N and P
in N and P supplyratios.
contents,probablyin responseto differences
6. The vegetationN:P ratio is of diagnosticvalue and its use may 'increaseour
of numerousfacetsofphysiological,population,community
understanding
and ecosystemecology.
Key-words:
nutrient
fertilization,
availability,tissueN, tissueP, wetland.
JournalofAppliedEcology(1996) 33, 1441-1450
& Aarsen 1989; Grace & Tilman 1990; Vitousek&
Howarth 1991). Nutrientlimitationstronglyaffects
Resourceavailability
is a driving
forcein ecosystem competitionbetweenplant species,as speciesvaryin
succession
and nutrients
areamongthemostimpor- theirabilityto cope withlow nutrient
resources.There
tantplantresources
thatstructure
plantcommunities is an evolutionarytrade-offbetweenplant features
(Tilman1985;Vitousek& Walker1987;DiTomasso advantageousundernutrient-poor
conditionsand fea-
Introduction
? 1996 British
Ecological Society
1441
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All use subject to JSTOR Terms and Conditions
1442
N:P ratiosand the
natureofnutrient
limitation
? 1996British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
conturesthat serveas adaptationsto nutrient-rich
adapditions(Berendse& Elberse 1990). Moreover,
plant features
tationto low-P sitesrequiresdifferent
thanadaptationto low-N sites(Tilman 1985).
Case studiesillustrateclearlyhow nutrientavailabilityaffectsthe speciescompositionof plant communities.High species densitiesare associated with
and occurparfornutrients,
competition
interspecific
ticularlyat moderatenutrientavailabilityand low
biomassproduction(summerabove-groundbiomass
c. 100-500g drywt m-2). At fertilesites withhigh
biomassproduction(summerabove-groundbiomass
> 1200g drywt m-2), thereis exclusionofshortspecies by taller species throughcompetitionfor light.
forlightthereis little
Underconditionsofcompetition
and as a resultthe vegetationis
nichedifferentiation
species-poor(Grime 1979; Tilman 1985; Moore &
Keddy 1989).
the natureof nutrient
In additionto site fertility,
limitation(N vs. P limitation)has been reportedto
affectthe speciescompositionof the vegetation.The
addition of P in the absence of N encouragesparticularlythe growthof leguminousspecies,that are
capable of dinitrogenfixation.In contrast,applicationsof N in theabsenceof P has been reportedto
stimulatethe growthof grass species in particular
(DiTomasso & Aarsen 1989).
In individualplants,nutrientlimitationis recognized by an increase in growthin response to an
additionof the limitingnutrient.Accordingto Von
Liebig's Law of the Minimum(Von Liebig 1840),
to individualplants is governedby the
site fertility
availabilityof the limitingnutrient.Other nutrients
are availablein relativeabundanceand are lessimportantforplantgrowth.
levelthe analogous responseto
At thecommunity
an additionof the limitingnutrientis an increasein
total primaryproduction(Chapin, Vitousek& Van
biomass
Cleve 1986). Reviewsshow thatcommunity
productionis usuallycontrolledby N and P. K limitationshave been reportedonlyoccasionally(DiTomasso & Aarsen 1989; Morris 1991; Vitousek &
Howarth1991;Koerselman& Verhoeven1995). In a
however,plantspeciesmay
community,
multi-species
limitedby N and P. A
co-existthatare differentially
site where certain species encounter severe Pmay be P-richto speciesthathave special
deficiency
adaptationsforP uptake (cf. DiTomasso & Aarsen
1989; Verhoeven,Kemmers & Koerselman 1993).
is expectedto increasethe
This nichedifferentiation
speciesrichnessof naturalvegetation(Tilman 1985).
thefactorthatlimitsplantgrowthat
Traditionally,
levelis establishedin a factorialfertilizer
a community
experimentwithmajor plant nutrientsN, P and K
(Chapin et al. 1986). Although performinga feris themostcertainway to estabtilizationexperiment
are time
lish the limitingnutrient,such experiments
to thesite.Thus,
consuming,laboriousand disturbing
it would be beneficialto have a tool that gives the
but
experiment,
same informationas a fertilization
with
less
disturbance.
and
cheaper
faster,
In thispaper we show thatthe natureof nutrient
limitationcan be directlyestablishedfromthe N:P
ratio in plant tissue.The 'N:P tool' is conceptually
simpleand accuratelypredictsthe limitingnutrient
levelin a varietyof
forplantgrowthon a community
wetlands.The N:P tool is of
European freshwater
diagnosticvalue, and its use may solve currentscientificdebateand practicaldilemmasin variousresearch
fields.
Rationaleand generalmethods
HYPOTHESES
We postulatedthatthe ratio of N, P and K in plant
tissuegivesan indicationoftherelativeavailabilityof
in thesoil. As N and P are mostoften
thesenutrients
the limitingfactorsfor plant growth,the research
focused on those two elements.We assumed that
low P supplyand high
underconditionsof relatively
N supply,plantstake up moreN thanP. Due to the
luxuryconsumptionofN, theN:P ratioin planttissue
will be relativelyhigh.In contrast,underconditions
of relativelyhigh P supply and low N supply,we
expecta lower N:P ratio in plant tissue (cf. Shaver
& Melillo 1984; Redente,Friedlander& McLendon
that
1992; Koerselman1992). Thus, we hypothesized
plant specieshave a 'critical'N:P ratio,that tellsus
whethergrowthof the species is N-limitedor Plimited.In thispaper,we testthishypothesisat the
level of plant communities,i.e. that the N:P ratio
of bulk vegetationsamples indicatesthe nature of
nutrientlimitationat the communitylevel (P vs. N
limitation).In addition, we discuss whetherplant
in theirrelativeN and P requirements,
speciesdiffer
criticalN:P ratios.
and thushave different
Elemental ratios have been successfullyused to
establishthe natureof nutrientlimitationin aquatic
ecology (e.g. Redfield,Ketchum & Richards 1963;
Rhee 1978; Smith1982;Downing& McCauley 1992)
and in agriculturalsciences(e.g. Tisdale, Nelson &
ecology, however,this
Beaton 1985). In terrestrial
approach has been largelyignored(but see Wassen
1990;Koerselman1992).
DATA AND ANALYSES
limiVegetationN:P ratioand thenatureof nutrient
level
tationat a community
To testthe hypothesisthatthe vegetationN:P ratio
limitationat thecomindicatesthenatureofnutrient
munitylevel (P vs. N limitation)we reviewedfertilizationstudiesin whichboth communitybiomass
additionsand planttissue
responsefollowingnutrient
controlplots
nutrientconcentrationsin unfertilized
our
wererecorded.For practicalreasons,we restricted
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1443
W. Koerselman&
A.F.M. Meuleman
literaturesurveyto European freshwater
wetlands,
includingrichfens,poor fens,bogs, wet heathlands,
duneslacksand wetgrasslands.The varietyofwetland
ecosystems
sampledshouldgivea generalapplicability
to theresults.
enrichment
We selectednutrient
under
experiments
fieldconditionswith intactplant communities,but
also included two studies using a test plant ('phytometer')thatwas grownon enrichedsoil substratum
(Loach 1968;Boyer& Wheeler1989). Althoughphytometerexperiments
do not yieldconclusiveevidence
on the natureof nutrientlimitationunderfieldconditions,theirdesign is adequate for studieson the
relationshipbetweenplant tissueN:P ratiosand the
natureof nutrient
limitation.
Fertilizationstudies were selected using the followingcriteria.
1. Plantgrowthwas eitherlimitedbyN or byP, byN
or by N or P in co-limitation
and P together,
withK.
StudieswhereK was primarily
limitingplantgrowth
were omittedfromthe database. In studiesin which
no inferential
statisticswere applied, we considered
a response significantif the relativeresponseto a
treatment
was greaterthan 1 25.
2. Appropriateexperimentaldesign. (a) The experimentaldesignassessedsingle-nutrient
effects
(includingN and P vs. control),singlevs. combinednutrient
effects(incl. N, P and NP vs. control),or, the best
case, all singleand combinedeffects
(factorialdesign,
usuallywith N, P and K). As an exceptionto this
condition,one studywas includedthatassessed only
the effectof various P giftson biomass production
(Boyer & Wheeler 1989). In this case, the biomass
responseto P additionalone was so large(factorc. 6)
that thiswas consideredadequate proofforP limitation.
watersolublefertilizers
(b) In wetecosystems,
may
be leached readily from the experimentalplot if
applied beforethe onsetof the growingseason. This
risk is particularlyhigh for N, which is poorly
adsorbedonto thesoil matrix.In addition,N maybe
lost fromthe ecosystemowing to denitrification.
If
fertilizer
additionsresultin increasednutrientavailabilityto the vegetation,theyshould eitherresultin
(i) increasedplantgrowthor (ii) an increaseof plant
tissuenutrientconcentration.Studieswherenutrient
additionsdid not produceany of thesetwo responses
were omittedfromthe database, as we feltthat the
experimental
designwas inadequate.
in
3. PlanttissueanalysesofN and P wereperformed
unfertilized
controlplotsat thetimeof harvest.
? 1996British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
A literature
surveyincludinginternational
journals,
as well as scientific
reportsrevealedthat in total 40
studiesin a varietyof wetland ecosystemsmet the
above criteria.The set of studiespresentedin Table 1
wereall carriedout in areas witha vegetationof per-
ennialherbsamongwhichgrassesorCyperaceae were
oftendominantand thegroundwater
tablewas usually
within0 7 m of the soil surface.They wereused for
further
analysesof the relationshipbetweenthe N:P
ratioofthevegetationand thenatureofnutrient
limitation.
Based on the biomass response to nutrient
additions,each of the 40 wetlandsiteswas classified
intoone of thefollowingcategories:(1) P-limited,(2)
N-limited,(3) co-limitedby N and P, (4) co-limited
by N and K, and (5) co-limitedby P and K.
VegetationN:P ratiosreportedhere are based on
total nutrientcontentsin biomass samplesof unfertilizedcontrolplots at the momentof harvest.N:P
ratios thus representaverage values for the community;theyare calculatedas mass.
VariationofN:P ratiosinduneslack species
We selecteda subsetofthedata (dune slacks;Table 1)
forfurther
studyto examinebetween-site
intraspecific
variation in
variation,and within-siteinterspecific
nutrientcontents and N:P ratios. The combined
resultsof the fertilization
studiesand the dune slack
in
differences
studyare used to discuss interspecific
criticalN:P ratios,and within-site
variinterspecific
ationin thenatureof nutrient
limitation.
We studiedN and P contents,and N:P ratiosin five
dune slack speciesin 18 dune slacks along theDutch
was
coast,in some ofwhicha fertilization
experiment
performedsimultaneouslyto detectwhich nutrient
controlledcommunitybiomass production (Koerselman& Meuleman 1994). The speciesselectedwere
Calamagrostisepigejos,Phragmites
australis,Lycopus
europaeus,Mentha aquatica and Eupatoriumcannabinum.
Above-groundbiomass sampleswere collectedin
August, at peak biomass, from vegetationstands
wherethe selectedplant speciesgrewin close proximity.At each site,threesub-sampleswerecollected
per species.
The sub-sampleswere mixedand dried (70'C for
48 h). Total N and P contentin planttissuewas determined by acid digestion(340'C) of ground plant
materialwitha mixtureof salicylicacid and sulphuric
acid using a seleniummixtureas catalyst(a modification of the Kjeldahl method; Page, Miller &
Keeney 1982). The nitrogenand phosphorusconcentration in the digests were determinedcolorimetrically
usingtheammoniummolybdatemethod
forphosphorusand the indophenolblue methodfor
nitrogen.
Resultsand discussion
THE N:P RATIO
NATURE
AS INDICATOR
OF NUTRIENT
COMMUNITY
OF THE
LIMITATION
ON A
LEVEL
Figure 1 showsN and P contentsin unfertilized
controlplots forthe followingcategories:(i) siteswhere
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All use subject to JSTOR Terms and Conditions
1444
N:P ratiosand the
natureofnutrient
limitation
Table 1. Sitesincludedin thisstudy(n = 40)
Ecosystemtype
site(location)
(a) Bogs (n = 3)
M6rhultsMosse (South Sweden)
Stordalen(northSweden)
Akhult(southSweden)
(b) Poorfens(n = 5)
Biebrzavalley(NE-Poland)
Molenpolder(Vechtplassen,NL)
't Hol (Vechtplassen,NL)
ChophamCommon(NE-Hampshire,UK)
Kismeldon(Devon, UK)
(c) Richfens(n = 13)
Buitengoor(Mol, Belgium)
Goorken(Arendonk,Belgium)
ZwarteBeek (Hasselt,Belgium)
BrackloonLough (Crossmolina,Ireland)
Biebrzavalley(NE-Poland)
Westbroek(Vechtplassen,NL)
Gagelpolder(Vechtplassen,NL)
Groot Zandbrink(GelderseVallei,NL)
Zwartebroek(GelderseVallei,NL)
Westbroek(Vechtplassen,NL)
BadleyMoor (Norfolk,UK)
Valleyof Reuss (Zurich,Switzerland)
(d) Wetheathlands(n = 3)
Chopham Common(NE-Hampshire,UK)
KruishaarseHeide (N-Brabant,NL)
(e) Wetgrasslands(n = 7)
Veenkampen(Wageningen,NL)
Born-Zuid(Wageningen,NL)
Ossekampen(Wageningen,NL)
DrentseAa (Groningen,NL)
(f) Dune slacks(n = 9)
Berkheide(Katwijk,NL)
Meijendel(Den Haag, NL)
NoordhollandsDuinreservaat(Castricum,NL)
Verklikkervallei
(Schouwen,NL)
(Haarlem,NL)
Kennemerduinen
Numberof studies
Reference
1
1
1
Tamm (1954)
Aertset al. (1992)
Aertset al. (1992)
1
1
1
1
1
Verhoevenet al. (1994)
Verhoeven& Schmitz(1991)
Verhoeven& Schmitz(1991)
Loach (1968)
Van Oorschot(1996)
1
1
1
1
2
1
1
1
1
1
1
1
Boeye & Verheijen(unpublished)
Boeye & Verheijen(unpublished
Boeye & Verheijen(unpublished)
Kooijman (1993)
Verhoevenet al. (1994)
Vermeer(1986a)
Vermeer(1986a)
Vermeer(1986b)
Vermeer(1986b)
Verhoeven& Schmitz(1991)
Boyer& Wheeler(1989)
Egloff(1983)
2
1
Loach (1968)
Aerts& Berendse(1988)
1
1
1
4
Oomes (1995)
Bloemhof(unpublished)
Bloemhof(unpublished)
Olff(1992)
1
1
5
1
1
Koerselman&
Koerselman&
Koerselman&
Koerselman&
Koerselman&
4-
35 -
E 2.5
E
2
0
.
04
:;
15
0.5
? 1996 British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
=co-limitation
jN:P<141
1.5
0
o=P-limitation
* = N-limitation
0
*
U)3 -
2
4
6
8
-:1N:P>1
Meuleman(1994)
Meuleman(1994)
Meuleman(1994)
Meuleman(1994)
Meuleman(1994)
___
I
6.00
N andP
v
61
=co-limitation
N and K
10 12 14 16 18 20 22 24 26
(mgg-1)
N-content
limitationin 40 Europeanwetlands(bogs,
Fig.1. RelationshipbetweenvegetationN and P contentand thenatureof nutrient
showingevidencefor
poor fens,richfens,wetheathlands,wetgrasslandsand dune slacks).Data pointsare fromexperiments
(see Table 1 fordata sources).Nutrientcontents
experiments
by fertilization
each typeof nutrientlimitation,as determined
controlplots.Dashed linesdepictN:P ratiosof 14 and 16,by mass.
in unfertilized
shownweredetermined
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All use subject to JSTOR Terms and Conditions
1445
W. Koerselman&
A.F.M. Meuleman
? 1996British
EcologicalSociety,
JournalofApplied
Ecology,33,
1441-1450
fertilization
experiments
wereinterpreted
as evidence
forP-limitation,
(ii) siteswhereN-limitation
occurred,
(iii) siteswhereplantgrowthwas co-limitedbyN and
by N and K was
P, and (iv) siteswhereco-limitation
observed.The dataset did not contain sites where
resultsof a fertilization
experiment
indicatedco-limitationby P and K. Three main conclusionsemerge
fromthedata in Fig. 1.
First,thevegetationN:P ratioclearlydiscriminates
betweenN- and P-limitedsites(Fig. 1). At N:P ratios
> 16,community
biomassproductionis P-limited.At
N:P-values < 14,N limitsplantgrowthin all but one
study.At N:P ratiosbetween14 and 16,eitherN or P
may limitplantgrowthor both elementsare equally
limiting('co-limitation').All threesitesthatappeared
co-limitedby N and P have N:P ratiosin the range
14-16. Onlyin one out of 40 studiesin whichN or P
was establishedas a limitingnutrient
in a fertilization
experiment,
does theuse of criticalN:P ratioslead to
a falseindication.This 'outlier'is a species-richrich
fencommunitystudiedby Vermeer(1986a) in which
N controlledplant growthwhilethe vegetationN:P
ratiowas 20.
In conclusion,Fig. 1 strongly
supportsour hypothesis thatthe N:P ratioaccuratelypredictsthe nature
ofcommunity
nutrient
limitation
in a varietyoffreshwaterwetlands.
A second pointof interestis the largevariationin
N content(rangingfrom6 to 20 mgN g' drywt)and
P content(0 2-3 3 mg P g'- drywt) that
particularly
emergesfromFig. 1. This variationis most likelyto
reflect
in thesupplyratioofN and P rather
differences
thandifferences
in absoluteN and P availability.
Shaver& Melillo (1984) demonstrated
thatplants
may regulatetheirN and P balance onlyto a certain
extent.The N and P contentsof Carex lacustris,Calamagrostiscanadensisand Typhalatifoliavariedtwoto four-fold
whenexposedto growthmediawithinorganic N:P supplyratiosrangingfrom0 8-61. Moreover, the N:P ratio in the plants was stronglycorrelatedwiththeN:P supplyratio.
If the observedvariationin N and P contentsof
wetlandvegetationweredue to differences
in absolute
N and P availabilities,we would expectfertilesites
to have highernutrientcontentsin plant tissuethan
infertile
sites.In theabsenceofdata fornutrient
availabilityat the sites,we used above-groundsummer
biomass as an index of site fertility.
This parameter
was determinedin 36 of the 40 studies that we
reviewed.Figure2 clearlyshows thatthe vegetation
at fertilesites(highbiomass) does not have higherN
and P contentsthan the vegetationat infertilesites
(low biomass). The correlation between summer
biomass and plant tissue nutrientcontentsis very
poor, both forthe whole dataset (Fig. 2ab) and for
partsof it [N contentvs. biomass forN-limitedsites
and P content vs. biomass for P-limited sites
(Fig. 2c,d)].
Fromthestudyby Shaver& Melillo (1984) and the
data in Fig. 2 we concludethatthe N and P content
in plant tissue is mainlydeterminedby the supply
ratiosof N and P, e.g. a highN contentreflects
situationswherehighN is available relativeto P. In such
situations,the absolute N availabilityis not necessarilyhigh.Presumably,
absoluteN and P availability
mainlyaffectsbiomass production,and the species
compositionof the vegetationratherthan N and P
contentin planttissue.
A thirdconclusionthatemergesfromFig.1 is that
no clear relationshipexistsbetweenthenutrient
contentin plant tissueand the natureof nutrientlimitation.In wet grasslandsN controlledplant growth
at relativelyhigh concentrationsof c. 20mg N g-1
drywt [Olff1992; Oomes 1995; Bloemhof(in prep.)],
whereasitdid notlimitplantgrowthinwetheathlands
and richfensat muchlowerconcentrations
ofc. 10 mg
N/g dry wt (Loach 1968; Aerts & Berendse 1988;
Boyer & Wheeler 1989). The patternforP is more
complex.Data indicatethata thresholdconcentration
exists(1 1 mg P g-l drywt) above whichP will not
limit plant growth (see also Fig. 2b,d). At concentrationsbelow this threshold,however,P is not
necessarily controlling plant growth (Vermeer
1986ab; Koerselman& Meuleman 1994; Verhoeven
et al. 1994).
Thus,it is theratiobetweenN and P thatindicates
whetherN or P limitsplantgrowth,not theabsolute
N and P contentin planttissue.
DO PLANT
CRITICAL
SPECIES
HAVE
IDENTICAL
N:P RATIOS?
Figure 1 provesthatcriticalN:P ratiosexistforwetland communities.This, however,does not prove
indisputablythatall wetlandplantspecieswithinthe
communitiesstudiedhave identicalrelativeN and P
requirements,
and thus identicalcriticalN:P ratios.
in criticalN:P ratiosmayhave
differences
Interspecific
been maskedin our study,as we relatedthe average
N:P ratio of a multi-species
vegetationto the nature
of nutrient
limitationat thecommunity
level.
A clear test of the hypothesisthat wetlandplant
specieshave identicalcriticalN:P ratiosrequiresdata
fromexperiments
inwhichpopulationsofspecieswith
different
N:P ratiosare exposedto additionsofN and
P, and subsequentgrowthresponsesare recorded.
suchdata are notavailable,preventing
Unfortunately,
an unequivocaltestof thehypothesis.
However, circumstantialevidence suggests that
in criticalN:P ratioare likely
interspecific
differences
to be insignificant.
Figure1 includesa largevarietyof
vegetationtypesand plantspecies.It is highlyunlikely
thatcorporatecriticalN:P ratioswouldhave emerged
fromthedata ifinterspecific
differences
in criticalN:P
ratios among plant species were significant
at these
sites,because at least 11 ofthe40 sitesincludedin our
studywerenear-monocultures,
whereonlyone species
accountedforover 80% of total biomass,viz. Erica
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All use subject to JSTOR Terms and Conditions
1446
N:P ratiosand the
natureofnutrient
limitation
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Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
This content downloaded on Fri, 8 Mar 2013 14:22:35 PM
All use subject to JSTOR Terms and Conditions
k
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1447
W. Koerselman&
A.F.M. Meuleman
and P contents,probablyin responseto differences
in
N and P supplyratios(Shaver& Melillo 1984).
Within-site
variationin N:P ratioscan
interspecific
be explainedfromdifferences
innutrient
uptakemechanismsbetweenspeciesor differences
inrootingdepth.
For example,Phragmitesaustralisusuallyhas a considerablyhigherN:P ratiothanotherspecies(Fig. 3)
and throughdeep rootingPhragmitesaustralisprobablyexploitslargersoil compartments
thantheother
species, which exploit mainly the upper soil compartments.
If we accept the suggestionpresentedin the foredifferences
in critical
going sectionthat interspecific
N:P ratiomaybe insignificant,
we mustconcludethat
at sites 1, 2 and 4 species co-occur that are differentiallylimitedby N or P (Fig. 3).
VARIATION
IN NUTRIENT
CONTENT
AND N:P
Fertilization studies showed that community
RATIO AMONG SPECIES
OCCUPYING
DUNE
biomass productionat site4 is P-limited,whereasN
SLACK SITES
controlscommunity
biomassproductionat theother
In thedune slack studywe observedhugewithin-site four sites (Koerselman & Meuleman 1994). Within
theplantcommunitiesof threeof thesesiteswe find
interspecific
variationin N:P ratio among fiveplant
plant species with N:P ratios indicatingthat their
species(Fig. 3). Between-site
intraspecific
rangesofN
growthis controlledby an elementthatdoes notconcontent,P contentand N:P ratiowerealso large,but
trolcommunity
biomassproduction(Phragmites
about equal forthefiveplant species(Table 2); they
australisand Calamagrostisepigejosat site 1, Phragmites
encompassed almost the total range of these parametersdepictedin Fig. 1. Between-siteand within- australisat site2, and Calamagrostis
epigejos,Lycopus
sitevariationin N and P contentis wellknownfrom europaeus,Mentha aquatic and Eupatoriumcanotherstudies(e.g. Boyd 1978;Ohlson 1988;Hayati &
nabinumat site 4). The species were not important
of the vegetation,and therefore
Proctor1991).
constituents
did not
contributesignificantly
to communitybiomass and
Between-site
variationoncemoreillusintraspecific
bulkvegetationN:P ratios.
tratestheplasticityof plantspecieswithrespectto N
tetralix(Aerts& Berendse1988),Phragmites
australis
(Koerselman& Meuleman1994),Eriophorum
vaginatum(Tamm 1954),Sphagnumbalticum(Aerts,Wallen
& Malmer 1992), Sphagnummagellanicum(Aertset
al. 1992), Agrostisstolonifera(Olff 1992), Molinia
caerulea (Egloff1983; Loach 1968; threesites) and
Juncussubnodulosus(Boyer & Wheeler 1989). In
addition, Shaver & Melillo (1984) presentexperimentalevidence that indicatesthat threewetland
plantspecieshave similaroptimumN:P ratios.
However,theevidencein favourof theassumption
thatplantspeciesdo not significantly
differ
in respect
of theiroptimal N:P ratio is circumstantialand a
rigoroustestof thishypothesisis required.
30
0
25O
o 20-
0
A_
Z
o
i~~
3
45
51
.
?
1996British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
Vegetation
o Lycopus
2
Site number
?
Phragmites
* Eupatorium
A
Mentha
A
Calamagrostis
Fig. 3. VegetationN:P ratios(mg mg-') and N:P ratiosin Phragmitesaustralis,Lycopuseuropaeus,Menthaaquatic, Calin fiveDutch dune slacks.The plantspecieswerenot importantconstituents
amagrostisepigejosand Eupatoriumcannabinum
controlplots of
of thevegetationat thesesites.VegetationN:P ratiosreferto the bulk vegetationsamplesfromunfertilized
fertilization
experiments
by Koerselman& Meuleman(1994).
This content downloaded on Fri, 8 Mar 2013 14:22:35 PM
All use subject to JSTOR Terms and Conditions
1448
N. P ratiosand the
natureofnutrient
limitation
Table 2. Range in planttissueN and P content(mg g-' drywt) and N:P ratioin fivespeciesthatweresampledfromDutch
dune slacks
Species
N content
P content
N:P ratio
Numberof sites
Phragmites
australis
Lycopuseuropaeus
Menthaaquatic
Calamagrostisepigejos
Eupatoriumcannabinum
13-31
9-35
9-30
9-22
13-26
1 0-3 1
0 9-3 6
0 9-3 6
0 8-2 4
1 1-3 8
5-29
5-25
4-18
5-33
5-29
11
11
14
17
10
the
Our assumptionthatwithinplantcommunities
growthofindividualspeciescan be limitedbydifferent
data reviewed
is supportedby experimental
nutrients
by DiTomasso & Aarsen (1989). The co-existenceof
limitedby N and
plant speciesthatare differentially
P helps explain the common observationthat complant
munitybiomass productionin a multi-species
communityis increasedparticularlyby the addition
of one element(being 'primarilylimiting'to plant
growth),but also to a lesserextentby otherelements
('secondarily'and 'tertiarily'limitingon the comThese otherelementsare
munitylevel,respectively).
probably primarilylimitinggrowthof non-dominatingspecieswithinthatcommunity.
CONSTRAINTS
AND
APPLICATIONS
OF THE
N:P
TOOL
The use of the N:P tool is a quick and simplealternative to laborious fertilization
experimentswhich
levelin a widerangeof
could be used at a community
wetlandtypes.
The maindrawbackto theuse ofN:P ratiosis that
theycan onlybe used as an indicatorof thenatureof
nutrientlimitationunderconditionswhereeitherN
or P limitsplant growth.As K seldom limitsplant
growth(Koerselman& Verhoeven1995; DiTomasso
is,
& Aarsen 1989), the risk of misinterpretation
however, small. As more data on K limitation
becomesavailable,we can establishcriticalN:K and
K:P ratiosas well.This willaid diagnosisof theorder
methods
inwhichN-P-K limitplantgrowth,following
suchas thosedescribedby Tisdale et al. (1985).
Anotherlimitationof the N:P tool is thatit does
not indicatethe absolute nutrientavailabilityat the
site,only the N and P supplyratio. This drawback
can be partlyovercomeif the N:P tool is combined
with data on biomass to produce an index of site
based on N and P stocksin biomass(g N m-2,
fertility
limitation
limitedknowledgeofthenatureofnutrient
in various ecosystemtypes (DiTomasso & Aarsen
1989; Vitousek& Howarth 1991). This may be particularlyusefulin remoteand inhospitableareas, as
information
can be gainedduringveryshortsummer
field trips. In combinationwith data on summer
biomass,theN:P tool can be used to estimateP and
N availabilityof sites(g N m-2,g P m-2).
2. The N:P tool can be used in restorationprojects
as thisrequires
aimingat a reductionof sitefertility,
a reductionof the availabilityof the nutrientthat
controls plant growth (Koerselman & Verhoeven
1995).Often,reducingP availabilityrequiresdifferent
measuresthanreducingN availability.The use of the
themostefficient
way
N:P tool mayhelpto determine
to reducethe site fertility.
For restorationpurposes,
however,it is importantto have an insightintointerin N:P ratio among plant species
specificdifferences
at therestorationsite.If suchvariationoccurs,and if
plant speciesdo have similarcriticalN:P ratios,certainmeasuresto reducesitefertility
maynotaffectall
speciesto thesame extent.Thus, apartfromreducing
biomass production,measures may also affectthe
speciescompositionofthevegetation(see Koerselman
& Verhoeven1995).
3. The N:P tool can be used to testTilman's theory
(Tilman1985),thatpredictsmaximumspeciesdensity
undercircumstances
whereN- and P-limitedspecies
mayco-exist,viz. whenN and P co-occuras limiting
resourcesat thecommunitylevel.A testof Tilman's
wherethe
theoryis ofinterestto natureconservation,
aim is oftento increasespeciesrichness.
4. Finally,theN:P tool can be used to testthehypothesis by Vitousek& Walker(1987) thata shiftfromN
limitation
towardsP limitationoccursduringprimary
ecosystemsuccession,as P availabilityin soils essentiallydeclinesthroughthecourseofsoil development,
while N availabilityincreaseswith humus accumulation.
gPm-2).
?
1996British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
limitation
is a drivingforceinecosystem
As nutrient
succession,use of the N:P tool may increase our
understandingof numerousfacetsof physiological,
population,communityand ecosystemecology. As
an illustration,
we give fourexamplesfromvarious
researchfields.
1. The use of the N:P tool may increasegreatlyour
Concludingremarks
From the data presentedhere,we concludethatthe
vegetationN:P ratiocan accuratelypredictthenature
at a community
ofnutrient
limitation
level.The variety
ofwetlandecosystemsincludedin our studywarrants
a generalapplicability
ofthecriticalN:P ratios(14 and
This content downloaded on Fri, 8 Mar 2013 14:22:35 PM
All use subject to JSTOR Terms and Conditions
1449
W. Koerselman&
A.F.M. Meuleman
? 1996British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
pp. 189-199. Balkema,
and M.J. Sheehy-Skeffington),
Rotterdam.
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Kiwa
valleien; resultatenvan bemestingsexperimenten.
N.V. Research and Consultancy, Nieuwegein, SWE
94.020. (In Dutch.)
Koerselman,W. & Verhoeven,J.T.A.(1995) Eutrophication
of fenecosystems;externaland internalnutrientsources
and restorationstrategies.Restorationof TemperateWetlands(eds B. Wheeler,S. Shaw,W. Fojt and R.A. Robertson),pp. 91-112. JohnWileyand Sons Ltd, Chichester.
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Kooijman, A.M. (1993) Changesin the bryophyte
and eutrophication.
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Received14 March 1995; revisionreceived9 March 1996
@ 1996 British
Ecological Society,
JournalofApplied
Ecology,33,
1441-1450
This content downloaded on Fri, 8 Mar 2013 14:22:35 PM
All use subject to JSTOR Terms and Conditions