J. Ecol. (1977), 65, 847-865
GROWTH RESPONSES OF COASTAL HALOPHYTES
TO INORGANIC NITROGEN
R. L. JEFFERIES
of East Anglia,Norwich*
School of BiologicalSciences,University
SUMMARY
(NH+ or
nitrogen
responsesto inorganic
variationin growth
Intra-and interspecific
speciesgrownin sandculture.
NO-) has beenstudiedin halophytic
Populationsof Aster tripolium,Plantago maritima,Salicornia europaea agg. and
Norfolk,have
fromtheupperlevelsof a salt marshat Stiffkey,
Triglochinmaritimna
populationsfroma low marshat thesame
slowergrowthratesthancorresponding
locality.PopulationsofAstertripoliumandPlantago maritimafromtheuppermarsh
closeto channels.
awayfromdrainagechannelsgrowslowerthanpopulations
of thelow marshsuchas Halimioneportulacoides,Aster triSpeciescharacteristic
ratescomparedwiththeratesofspecies
poliumand Suaeda maritimahavefastgrowth
abundantin theuppermarshsuchas ArmeriamaritimaandLimoniumvulgare.
nitrointheconcentrations
ofsolubleinorganic
thereis seasonalvariation
Although
of thetwo marshes,thevaluesobtainedare similarforboth
gen in thesediments
insummer.
marshes,
buttheuppermarsh,unlikethelowermarsh,becomeshypersaline
ofplantsfromtheupper
responsetonitrogen
It is suggested
thattheslowergrowth
marshawayfromdrainagechannelsis theresultofselectionforplantswithrelatively
low growthrates,whichare able to survivetheperiodof stressduringthesummer
monthswhenthesoil is hypersaline.
INTRODUCTION
The frequenCyand amplitudeof tides stronglymodulate environmentalconditions
tidalcoverageoftheupperlevelsofsome
withincoastalmarshes.For example,infrequent
and often
withhighratesofevapotranspiration
together
saltmarshesduringthesummer,
conditions(Chapman
low amountsof rainfall,resultin the developmentof hypersaline
1960; Ranwellet al. 1964; Tyler1971).
complexityof salt marshes,as well as thesepredictable
Moreover,thephysiographic
temporal fluctuationsin edaphic conditions,result in considerableenvironmental
withinsalt marshspeciesin responseto environGeneticdifferentiation
heterogeneity.
is well established(Gregor1930, 1946; Chapman 1960; Aston &
menitalheterogeneity
Bradshaw1966; Sharrock1967; Hannon & Bradshaw1968; Waisel 1972; Gray 1974).
may occur even
Only recentlyhas it become clear that such populationdifferentiation
withinsmall distancesover whichtherecould be considerablegene flow.Most of the
variationwhichhas been recognizedin salt marshpopulationsrelatesto morphological
* Present
ofToronto,Toronto,Ontario,Canada M5S lAl.
ofBotany,University
address:Department
847
848
to nitrogen
Growthresponsesof halophytes
such as leaf size and shape, and thereis littledirectevidenceof intracharacteristics,
specificvariationin physiologicalprocessesamongsthalophytespecies.
The growthof certainspeciesin theupperlevelsof some coastal marshesappearsto
be limitedbytheavailabilityof nitrogen(Tyler1967; Pigott1969; Stewart,Lee & Orebamjo 1972,1973; Valiela & Teal 1974; Patrick& Delaune 1975). Pigott(1969) cultured
plantsof Salicorniaeuropaeaagg. and Suaeda maritimain sedimentcorescollectedfrom
different
siteson a coastalmarshin Norfolkand foundthatplantsfromtheuppermarsh
showeda markedgrowthresponseto additionsof nitrogen.Stewart,Lee & Orebamjo
(1972, 1973) examinedthe levelsof nitratereductasein the leaves of a numberof halopartsof saltmarshes,and found,forexample,that
phytespecieswhichgrowin different
plantsof S. maritimafromtheuppermarshhad a low levelof nitratereductaseactivity
as comparedwithplantsof the same speciesgrowingin thelow marsh.Theysuggested
thatthe growthof speciessuch as S. maritimais limitedin theuppermarshbecause of
and that thereis an increasein nitrogensupplydown the
lack of nitrate-availability,
marsh.
Because of this evidenceof contrastingedaphic conditionsbetweenthe upper and
lowermarshes,a comparativestudywas undertakenof thegrowthresponsesto nitrogen
sites. One objectiveof the studywas to establish
of plants which occur at different
growthresponsesto nitrogen
whetherunderglasshouseconditionsthereweredifferent
to
the prevailingsalinities,the
differences
to
and
relate
any
different
species,
between
of inorganicnitrogenin thesoil
and theconcentrations
watercontentsof thesediments,
solutionsat thevarioussiteswithinthemarshwherethespeciesweregrowing.The other
whetherindividualsof the same speciesfromthe upperand
objectivewas to determine
growthresponsesto nitrogen.
lowermarshesshoweddifferent
MATERIALS AND METHODS
Thestudysite
Seeds, seedlingsand soil sampleswere collectedfroman upper marshand a lower
on thenorthNorfolkcoast (Nat. Grid ref.TF 964441)(Fig. 1). These
marshat Stiffkey
two marshesare separatedby an old sand dune whichrunsparallelto thecoast. Chapthevegetationofthearea. Specieswhich
man(1938, 1939,1960)has describedpreviously
Salicorniaeuropaea
on thelowermarshincludeAstertripolium,*
are at a highfrequency
marsh
at theedgeof
of
lower
the
line
strand
Along
the
and
portulacoides.
Halimione
agg.
abundant.
are
and
maritima
maritima
Triglochin
Plantago
maritimus,
old
the
duneJuncus
Armeriamaritima
At one sitein thelow marshadjacentto theold dune Astertripolium,
and Plantagomaritimagrowin graveland sand. In contrast,thereis a relativelyrich
on theflatareas of theuppermarshaway fromthedrainagechannels,
plantcommunity
a community
whichincludesArmeriamaritima,Limoniumvulgare,Plantatomaritima,
maritimaand Salicorniaeuropaeaagg. Some areas on the uppermarshare at
Triglochin
a slightlylowerelevation(13-15 cm lower)thanthe flatareas mentionedabove; these
areas at a lowerelevationappear to be the remainsof old pools and drainagechannels
in theseareas includes
whichhave becomefilledwithsediment.The plant community
Limoniumvulgare,Puccinelliamaritimaand Salicorniaeuropaea agg. Seedlingsof S.
europaeaagg. werecollectedfroma sitein an area of low elevationin theuppermarsh,
but theremainderof theplantmaterialfromthe uDDer marshwas obtainedfroma site
* Nomenclature
plantsfollowsClapham,Tutin& Warburg(1962).
offlowering
R. L. JEFFERIES
849
in a flatarea (highelevationsite).Salicorniaeuropaeaagg. is rareor absentin theselatter
areas.
On theleveesofthecreeksin boththeupperand lowermarshHalimioneportulacoides
and Plantagomaritima.
growstogetherwithAstertripolium
procedures
Analytical
Intactturfs(30 x 30 x 30 cm) wereperiodicallycut at randomat the followingsites
whereseed and seedlingswerecollected(Table l): highand low elevationsitesin the
uppermarsh,the bank of a drainagechannelin the uppermarshand a sitein the low
25 m2, and one turfwas taken on each sampling
marsh.Each site was approximately
betweenconsecutivesamplingdates throughout1974 was
occasion. The time-interval
alwaysless than 1 monthand duringtheperiodAprilto September1974it was 2 weeks
or less. The turfswere transportedto the laboratory,wherethreesoil cores were cut
at a depth of between3 and 15 cm below the surfaceof the turfand waterexpressed
fromthe coreswiththe use of an Apex hydraulicpress.On certainoccasionswhenthe
was low thenumberof corestakenwas lessthanthree,as
watercontentofthesediments
fromsome sediments,especiallythose cores fromthe
water
express
to
difficult
it was
which containedwoody undergroundtissue of
Cores
channel.
bank of the drainage
ofsodiumin theexpressedsamplesof
The
concentration
perennialplantswerediscarded.
The sulphanilic
spectrophotometer.
SP90A
Unicam
of
a
use
with
the
waterwas measured
was used to
1972)
&
Parsons
(Strickland
method
diamine
diethylene
acid/N-naphthyl
in the
Ammonia
present
dust.
zinc
with
of
the
sample
estimatenitrateafterreduction
Parsons
&
(Strickland
method
phenol-hypochlorite
the
using
water was estimated
1972). Additionalcoresweretakenfromthe turfsat a similardepth,weighed,driedat
80 OC,and weighedagain in orderto obtainestimatesof thewatercontentof thecores.
Culturemethods
in sand moistenedwitha dilutesolutionof
Seeds of all populationsweregerminated
NaCl, 2-5x 10- 2M; MgSO4,2-5x 10- 3M;
composition:
following
of
the
water
sea
artificial
1 x 10-3M. Iron and traceelementswere
KCl,
1
X
x
10-3M;
2
10-3M;
CaC12,
NaH2PO4,
as
byJohnsonet al. (1957). This sodium
final
used
concentrations
same
the
added to give
of salinityon the growthof halothe
effects
because
when
was
chosen
concentration
in thoseculturesin whichthe
observed
were
rates
maximum
growth
studied,
were
phytes
x
L.
unpublished).No
10-2M
(R.
Jefferies,
2-5
was
of
chloride
sodium
concentration
of thesame
populations
different
from
in
of
seeds
the
germination
differences
detectable
contained
which
12
5
pots
into
cm
transplanted
were
Seedlings
observed.
specieswere
sea water.
artificial
diluted
of
2
litres
with
previously
that
had
been
wetted
quartz sand
into pots.
directly
soil
and
planted
free
of
washed
field
in
the
were
Seedlingscollected
illumination
of
artificial
in
the
absence
in
an
unheated
glasshouse
The plantsweregrown
duringthe summerof 1974.
the growthresponsesof plantsto nitrogensuppliedas
In the majorityof treatments
culture
of sodiumnitratein the different
nitratewerestudied.The finalconcentrations
of
solutionswere1 x 10' M,1 X 10-4 Mand 1 x 10-3 M. In orderto comparetheeffects
the additionof nitrogenas nitrateand as an ammoniumsalt,ammoniumchloridewas
This comadded to a culturesolutionas thesole sourceof nitrogenin sometreatments.
of the appropriatesourceof
parisonwas limitedto culturesin whichtheconcentration
nitrogenwas 1 x 10-4 M. The additionof solutionscontainingnitrogenbegan 3 days
850
Growthresponsesof halophytes
to nitrogen
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R. L.
JEFFERIES
851
salt marsh,Norfolk
Table 1. Seed and seedlingcollectionsat Stiffkey
Date of
Dominantspecies
Site
collection
Species
(a) Seed collections
July1973 Uppermarsh,highelevation Plantagomaritima,
Armeria
maritima
vulgare,
Limonium
site
Armeria
maritima
Salicorniaeuropaea
October1973 Lowermarsh
Astertripolium
agg.,Astertripolium
October1973 Uppermarsh,highelevation Plantagomaritima,
A. tripolium
vulgare,
Limonium
site
Armeria
maritima
Halimione
portulacoides
October1973 Drainagechannellevee,
A. tripolium
uppermarsh
Plantagomaritima,
October1973 Sandysite,lowermarsh
A. tripolium
maritima
Armeria
Plantago
maritima,
high
elevation
Limonium
vulgare August1973 Uppermarsh,
Limonium
vulgare,
site
Armeria
maritima
maritima,
Triglochin
Plantagomaritima August1973 Lowermarsh,strandline
Plantagomaritima
August1973 Uppermarsh,highelevation Plantagomaritima,
P. maritima
Limonium
vulgare,
site
Armeria
maritima
portulacoides
Halimione
August1973 Drainagechannellevee,
P. maritima
uppermarsh
maritima,
Triglochin
Triglochin
maritima August1973 Lowermarsh,strandline
Plantagomaritima
T. maritima
August1973 Uppermarsh,highelevation Plantagomaritima,
Limonium
site
vulgare,
Armeriamaritima,
(b) Seedlingcollections
May 1974
Halimione
portulacoides
Salicorniaeuropaea
May 1974
agg.
S. europaea
May 1974
agg.
Suaeda maritima
Astertripolium,
Salicorniaeuropaeaagg.
Astertripolium,
Lowermarsh
Salicorniaeuropaeaagg.
maritima,
Uppermarsh,lowelevation Puccinellia
Limonium
vulgare,
site
Salicorniaeuropaeaagg.
Astertripolium,
May 1974 Lowermarsh
Salicorniaeuropaeaagg.
Lowermarsh
aftertheseedlingswereplantedin thepots.Normally,100ml oftheappropriatesolution
were added to each cultureeveryotherday, but in hot weatheradditionswere made
daily.
was set up as a completelyrandomizeddesign,and six replicatesper
Each experiment
treatment
wereharvestedon each of threeseparateoccasions.Dependingon thegrowth
was between40 and 62 days.
rateof plantsin culturesthe durationof each experiment
Afterharvesting,
theplantswerewashedfreeof sand and thefreshweightof the shoot
852
to nitrogen
Growthresponsesofhalophytes
and root measured.Subsequentlytheplant organsweredriedat 80 ?C and weighedto
obtainthedryweights.
RESULTS
Edaphicconditions
of sodiumin thesoil waterat thetwo uppermarshsitesawayfrom
The concentration
thedrainagechannelsapproaches1 M duringthesummermonths(Fig. 2), whereasearly
in the yearthe values are between0 2 and 0 3 M. Changesin the watercontentsof the
in summer.The low
sedimentsshowtheoppositetrend,withthelowestvaluesoccurring
of the
watercontentsof the sedimentsand the highsalinitiesare, in part,a reflection
oftheuppermarshand ofthelow rainfallduringthisperiod.
absenceoftidalimmersion
conditions,the occurrence
Althoughthereis considerableamplitudein environmental
in theuppermarsheach yearis a predictablephenomenon.By contrast,
of hypersalinity
coverthe lowermarshin summer,and tidal waterentersthe drainage
tidesfrequently
conditionsfailto developat these
hypersaline
channelsin theuppermarshso thatextreme
in the salinityand watercontentsof
sites.As a resultthereis littleseasonal periodicity
soilsfromthelowermarshand fromthebanksofthedrainagechannelintheuppermarsh
(Fig. 2). The amplitudeof salinityin the lowermarshis 0l3 M comparedwith0l85 M at
sitesin theuppermarsh,and seasonal changesin watercontentof the sedimentsof the
lowermarshare small. The lowerwatercontentsof the sedimentsfromthe bank of a
drainagechanneland fromthe low marshcomparedwiththosefromthe uppermarsh
away fromthe drainagechannelsare a consequenceof theirhigherbulk density.The
of sedimentsoflow organiccontentwhichhaveunderhighbulkdensityis characteristic
(Glopper 1964).
gone somepedogeneticdevelopment
of nitrateand ammoniumions in the soil solutionschangedconThe concentrations
in the
siderablyduring1974 (Fig. 3). However,at any giventimethe concentrations
uppermarshawayfromthedrainagechannelsand in thelowermarshweresimilar.Two
sitesoccur,in late March or April
of nitrateat thesedifferent
peaks in theconcentration
and in earlyJune,whenvalues eitherapproach or exceed 1 x 10' M. In late Apriland
earlyMay thelevelof nitratein thesoil solutionsfallsto 1 x 10-5 M or below,and after
falloccursin theavailabilityof nitratefortheremainderof
theJunepeak a progressive
the growingseason. As will be shownelsewhere,thepeaks in the availabilityof nitrate
beimmediately
precedea phase of vegetativegrowth.Thereis an inverserelationship
in
soil
solutions
ammonium
ions
the
of
ions
and
tween the concentrations nitrate
of nitrate
betweenMarch and July.For example,in earlyJunewhentheconcentration
x
of
is
1
M. After
x
ions
below
10-5
exceeds 1 I0-4 M at all sites,the level ammonium
nitrate
and
of
ammonium
both
no longerholds,as theavailabilities
Julythisrelationship
conin
the
ammonium
rise
a
is
temporary
ions declineuntilthelate autumn,whenthere
the
from
The
results
with
litterdecomposition.
at all sites,probablyassociated
centration
above
in
do
into
not
the
marsh
fall
a
the
upper
bank siteadjacentto drainagechannel
of thesetwo ions are muchless pronounced
pattern.Fluctuationsin the concentrations
and
the
availabilityof nitrateexceeds1 x 10-4 M
at thissiteduringthegrowingseason,
formuchof the summer.
studies
Growth
of theanalysesof varianceis large
component
In mostcases,thebetween-population
853
R. L. JEFFERIES
.
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Growthresponsesof halophytes
854
10-3-
((a)
(b)
|c)
(d)
10-4
0
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20
E
10
0
E
E
0JFMAMJJASOND
JFMAMJJASOND
JFMAMJJASOND
JFMAMJJASOND
1974
of ammoniumand nitrateions in the bulk solution
FIG. 3. The mean concentrations
saltmarsh,Norfolk.(a), Uppermarsh
sitesin Stiffkey
withintherootingzoneat different
of bank of a
(low elevationsite); (b), uppermarsh(highelevationsite); (c), sediments
drainagechannelin theuppermarsh;(d), lowermarsh.
populations
between
ingrowth
differences
thattherearesignificant
(Table2), indicating
that
suggests
which
x treatment
areoftensignificant,
interactions
ofa species.Population
Populations
to nitrogen.
responses
growth
different
show,in addition,
thepopulations
(Fig.
maritima(Fig. 4), Astertripolium
of Salicorniaeuropaeaagg.(Fig. 4), Triglochin
in
differences
significant
variation;
5), andPlantagomaritima(Fig.6) showintraspecific
in
harvest
to thesecondand third
are restricted
populations
individual
yieldbetween
of 1 x 1O' M or 1x 1i-3 M. Shootsof
is addedat a concentration
cultures
wherenitrate
Salicornia
Plantagomaritima,
ofAstertripolium,
thelowermarshpopulations
plantsfrom
greatergrowththanthe
europaea agg. and Triglochinmaritimashowedsignificantly
shootsofplantsofthesamespeciesfromtheflatareasoftheuppermarsh.Intraspecific
plantsofpopulawithin
theuppermarshis also evident;
between
variation
populations
ofa drainage
levee
(Fig.7) fromthe
tionsofAstertripolium
(Fig.5) andPlantagomaritima
shootgrowth
thanplantsofthesamespeciesfrom
greater
significantly
channel
produced
populations
between
havedeveloped
theflatareasoftheuppermarsh.Thesedifferences
R. L.
JEFFERIES
855
whichare separatedbya distanceoflessthan10 m. In mostcases variationin thegrowth
populationsgave a similarpatternof results.
ofrootsbetweentherespective
variationin the responseof
variation,considerableinterspecific
Besidesintraspecific
occurs(Table 3). Speciesabundant
of nitrate-nitrogen
concentrations
speciesto different
(Fig. 8) and
(Fig. 5), Halimioneportulacoides
in the lowermarsh,suchas Astertripolium
Suaeda maritima(Fig. 8), showeda markedgrowthresponsein culturesin whichthe
between
differences
of nitratewas 1 x 10-3 M. In contrast,no significant
concentration
(Fig. 8) wererecorded,and the
in thedryweightofshootsofArmeriamaritima
treatments
values
meandryweightperplantat each harvestwas low comparedwithcorresponding
forotherspecies.
A comparisonof the growthresponsesof plantsto the presenceof ammoniumions
of 1 x 10- M was also made. With
and of nitrateions in theculturesat a concentration
maritima,whichall
Limoniumvulgareand Triglochin
the exceptionof Astertripolium,
showedpoor growthin cultureswhereammoniumchloridewas thesole sourceof nitrowere
in the growthof plantsbetweenthe two treatments
differences
gen,no significant
recorded.
variationwas observedin Plantagomaritima,therewas conAlthoughintraspecific
siderablevariationin growthbetweenindividualswithina population.Gregor(1930)
growthformsof individualsof thisspecies,rangingfromprosrecognizedsix different
away fromdrainagechannels,prostrateto erecttypes.On theuppermarshat Stiffkey
whereastheerecttypesare confinednormallyto
trateformsofthisplantainare frequent,
the leveesof drainagechannelsand to the low marsh.Because of theserespectivedistributions,the prostrateand erecttypeswere grownin culturein orderto establish
Erect and prostrate
responseto nitrate-nitrogen.
whethertheyshowed a differential
of the
formswere selectedat the seedlingstage froma seed populationrepresentative
to cultureswhich received
flat areas away fromdrainage channels,and transferred
difference
amountsof nitrogen.The results(Fig. 7) clearlyindicatea significant
different
in thegrowthof thetwo types.
DISCUSSION
Plantagomaritima,Salicorniaeuropaeaagg.
Individualpopulationsof Astertripolium,
differences
of themarshshowedsignificant
different
from
parts
maritima
and Triglochin
uniformglasshouseconditions;consequentlyit is likelythat
in growthunderrelatively
The findingsof Durrant
geneticcomponentto thesedifferences.
thereis a significant
throughseeds for
be
can
transmitted
effects
that
environmental
Hill
(1967)
and
(1972)
the differin
ascribing
must
be
exercised
some
caution
that
means
severalgenerations
studies
such
use
in
to
the
applies
A
argument
similar
of
selection.
entiationto theeffects
1964).
habitats
(Heslop-Harrison
from
natural
collected
been
have
of seedlingswhich
workand
other
in
terms,
adaptive
can
be
understood
observed
However,thedifferences
have
reported
and
&
(1974),
Bradshaw
Gray
Aston
(1966)
ers,notablyGregor(1946),
Jain&
of populationsof halophytesin a coastal salineenvironment.
the differentiation
is deof
localized
populations
that
such
differentiation
argued
have
(1966)
Bradshaw
clear
It
is
flow.
and
gene
selection
of
natural
of
the
outcome
on
interplay
the
pendent
sufficiare
that
if
selection
above
pressures
those
mentioned
from
and
study
fromtheir
can occur. In the studiesreportedin thispaper, intraentlyhigh,local differentiation
to nitrogenwere foundin both annual and perennial
in
differences
response
specific
to nitrogen
Growthresponsesof halophytes
856
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857
R. L. JEFFERIES
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Growthresponsesof halophytes
858
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18
36
48
in sand
FiG. 6. The meandryweightof plantsfrompopulationsof Plantagomaritima
of inorganicnitrogen.1, population
concentrations
cultureswhichreceiveddifferent
fromstrandlineoflowermarsh;2, populationfromuppermarsh(highelevationsite);3,
populationfrombankof a drainagechannelin uppermarsh;(a), shootdryweight;(b),
* ---- 10-4 M
as follows:*- *10-3 M nitrate-nitrogen;
rootdryweight.Treatments
* e e e e 10-5 M nitrate0 - .-- -10-4 M ammonium-nitrogen;
nitrate-nitrogen;
betweenmeans.
difference
theleastsignificant
The verticalbarsrepresent
nitrogen.
fromdifferent
partsofthelowmarshshoweda morerapidgrowth
species.Populations
fromtheflatareasoftheuppermarsh.These
inculture
populations
thancorresponding
in
at a concentrawhichreceived
nitrate
cultures
apparent
differences
wereparticularly
were
examined,
of
species
1
x
M.
different
of
where
populations
tion
Furthermore,
10'Halimione
and
as
Suaeda
maritima
lower
marsh,such
thosespeciescollectedfromthe
in
of
in
of
levels
nitrogen,
rate thepresence high
showeda fastgrowth
portulacoides,
marsh.
from
the
a
upper
ofArmeria
maritima,speciesobtained
contrast
tothebehaviour
on
forselection
coefficients
As indicated
byAston& Bradshaw(1966),theultimate
on
accumulate
forces
selective
indeed,
as
high
be
very
can
genotypes
perennial
long-lived
species
plantsofperennial
individual
overmanyyears.Theage ofindividual
genotypes
to
is
of
estimated
counts
root
stocks,
based
on
ring
at
Stiffkey,
suchas Limonium
vulgare
from
can
of
spread
in
some
of
these
species
Individuals
perennial
of
be excess 40 years.
so thatthedeleterious
theirpointof originbypurelyclonalmeansintonewhabitats,
there
showthatalthough
fieldobservations
ofgeneflowareavoided.At Stiffkey
effects
fromtheupperandlowermarsh,
populations
timebetween
is someoverlapinflowering
the
Forexample,
or theotheris flowering.
thereareperiodswhenonlyonepopulation
maritimaflowered10 days
strandlive populationsof Plantagomaritimaand Triglochin
R. L.
859
JEFFERIES
4-4 /a
0
Q.,
C..;,
0
0
75
0
.4-b
O
X,
X
O
.4-b0 cd .4.,
cd -=
Cd
-4
OD
(\j
0
cd
$-4
C\j
0
0
0
0
4-i
OD
o
O
0
cd C-4
O
0
cd 4
cd
E
O
:j
(Z)
0
4-1
PO
cd
OD
Oj
V,
0
4-i Cd 0 s-,
0
t.t:
+5
0
Cd
'= C: s-, Cd
Cd
+-A
-
0
$..,
0
Cd
cts
4--i
0
O
Cd
Cd
OD
;>
cd
0
4-4
0
cd
0
0
C13
0
0
0
0
0
K)
C\j
0
0
0
0
(bw) m A)p ur)A
V,
4
O
Cd
0
ct
860
Growthresponsesof halophytes
to nitrogen
C
10N"'~~~~1
O
S
O
t
O
n
O
Ct
(6UJ)
O
XM ^Jp
UD@W
O
Q~~~~~~~~~~~~~r
.~~~~~~~~~~~~~~~~~X
00
?
2 .0
.=S
0
R. L.
861
JEFFERIES
Table 2. Analysisof varianceof the growthresponsesof populationsof
levelsofnitrogen
Marsh to different
speciesat Stiffkey
halophytic
Sources
Treatments
(T)
Harvests(H)
Populations (P)
TxH
PxT
PxH
PxTxH
Error
Total
Treatments
(T)
Harvests(H)
Populations(P)
TxH
PxT
PxH
PxHxT
Error
Total
Roots
Shoots
Significance Significance
level
d.f.
level
Astertripolium
3
2
d.f.
3
2
3
2
*
6
9
6
18
240
287
NS
NS
NS
NS
NS
6
6
4
12
180
215
Plantagomaritima
(uppermarsh,highelevation
siteand drainagechannel
populations
only)
3
2
1
6
*
NS
3
2
*
**
NS
6
120
143
NS
NS
Salicorniaeuropaeaagg.
Treatments(T)
Harvests(H)
Populations(P)
TxH
PxT
PxH
PxTxH
Error
Total
3
Shoots
Roots
Significance Significance
level
level
Plantagomaritima
*
NS
**
NS
NS
*
NS
NS
Plantagomaritima
(erectand prostrate
populations)
NS
NS
NS
NS
NS
NS
**
maritima
Triglochin
**
*
2
1
**
6
3
2
6
**
**
NS
*
**
120
143
*
NS
*
**
**
NS
*
P<005; **P<0.01; ***P<0001.
to 2 weeksin advance of the corresponding
populationsin the upper marsh in 1974,
in flowering
timebetweenthe populationsmay reducethe
1975 and 1976. Differences
of geneflowon thegeneticcompositionof thepopulations.
effects
and Plantagomaritimafromthebanks of the drainage
Populationsof Astertripolium
differences
channelsand fromtheopen areas on theupper marshalso showedsignificant
in theirgrowthin thepresenceof nitrogen.The morevigorousgrowthis characteristic
ofpopulationsfromthebanksofthedrainagechannels.Field observationsindicatethat
erectformsof these two species grow amongstthe shrubbyHalimioneportulacoides
whichis widespreadalongthebanksofthedrainagechannels,whereasat opensiteson the
and plantsof
predominates,
uppermarshthesmallprostrateformofPlantagomaritima
Astertripolium
are dwarf.As theprogenyfromthe two populationsof Plantagomarisugtimacontainboth theuprightand prostrateformsin sizeablenumbers,it strongly
to nitrogen
Growthresponsesofhalophytes
862
at Stiffkey
ofhalophytes
responses
Table 3. Analysisofvarianceofthegrowth
levelsofnitrogen
Marsh to different
Sources
(T)
Treatments
Harvests(H)
TxH
Error
Total
d.f.
3
2
6
60
71
Roots
Shoots
Roots
Shoots
Significance Significance Significance Significance
level
level
level
level
maritima
Armeria
**
NS
**
vulgare
Limonium
Treatments
(T)
Harvests(H)
TxH
Error
Total
3
2
6
60
71
portulacoides
Halimione
Suaeda maritima
*
*
NS
*P<O05; **P<001; ***P<0001.
at each
geststhatselectionoperatesat theseedlingstageso thatone formpredominates
site.
In theglasshouse,populationsof theannualspeciesSalicorniaeuropaeaagg. fromthe
in growthrate,and thesetwo populaupperand lowermarshalso showeda difference
of seedlingsof the lowermarsh
density
The
well.
in
field
as
tionsbehavedifferentlythe
m-2
and duringthesummerthere
season,
in
the
early
000
50
populationmayapproach
In contrast,the densityof
mortality.
density-dependent
intensive
certainly
almost
is
100
m-2, and thereis little
under
is
often
marsh
upper
on
the
Salicornia
seedlingsof
of largenumbersof
presence
The
season.
growing
of
the
end
the
until
of
plants
mortality
individualsof Salicorniain the lowermarshand in the low elevationareas of theupper
marsh,and in particularthehighdensityofindividualsin thelowermarsh,indicatesthat
forgeneflowbetweenthe populations.Thereis strong
theremay be littleopportunity
occurs,plantsof thisspeciesseta highproporevidencethatalthoughwind-pollination
1962; Ranwell 1972). Ball & Brown (1970)
(Dalby
self-fertilization
tion of seed by
someripeseedsfellout of plants,but
S.
dolichostachya
and
S.
europaea
in
reportedthat
in situ.The seeds bear an
germinated
and
plants
on
retained
were
seeds
in manycases
it is assumedthatthese
and
hooked,
of
them
many
hairs,
mucilaginous
of
indumentum
1968). All of theabove
Swann
&
(Petch
hairsassistin anchoringseed to the substratum
and lower marsh
upper
from
the
would tend to keep the populations
characteristics
groupswithin
different
of
the
However,untilthe taxonomicstatus
distinctgenetically.
populaparapatric
as
regarded
be
theyshould
theaggregatespeciesis fullydetermined,
tionsbetweenwhichbreedingbarriersexist.
nitrogenlevelsis that
As indicatedabove, thegeneralpatternof responseto different
and thatthereare
growth,
poor
relatively
show
marsh
the
upper
all populationsfrom
as compared
nitrogen
to
in
responses
their
growth
betweenthepopulations
differences
of nitrate
of
availability
pattern
the
seasonal
However,
withlowermarshpopulations.
differlarge
in
similar;
both
marshes
is
in
soil
solutions
and ammoniumions the bulk
not
do
ions
of
in
these
marsh
concentrations
lower
the
ences betweenthe upper and
differto
detect
of
who
was
unable
those
Pigott(1969),
exist.These findingsconfirm
R. L. JEFFERIES
863
ences in the amountsof nitrogendissolvedin waterpressedout of freshsoil samples
siteson Scolt Head marshesin Norfolk.
obtainedfromdifferent
betweentheupperand lowermarshis thelack oftidalimmersion
One majordifference
of theuppermarshduringmuchof thegrowingseason. Not onlydoes thisresultin the
of the
conditionsin theuppermarsh,butalso thedrying-out
ofhypersaline
development
a
down
may
develop
stress
water
soil. Pigott(1969) reportsthat a steep gradientin
Limonium
of
that
the
leaves
marshduringdry periods in summer,and he observed
vulgarewerewiltedand witheredat thetop ofthemarshbutwereturgidand undamaged
themajority
at lowerlevels.Duringthedrysummerof 1975in theuppermarshat Stiffkey
In
of
desiccation.
died
June
in
early
of seedlingsof Suaeda maritimawhichgerminated
as
Plantago
such
plants,
perennial
certain
of
leaves
of
the
mostyears,earlysenescence
maritimaand Limoniumvulgare,occursin late Junein the upper
maritima,Triglochin
marsh.It is suggestedthatthepresenceof a low soil waterpotentialand a highsalinity
duringmuch of the growingseason has resultedin selectionforplantsof low growth
poor growth
potential,whichare able to toleratetheseextremeconditions.The relatively
appearsto
nitrogen
of
presence
in
the
plants
oftheuppermarshpopulationsofperennial
A
paper
subsequent
salinity.
high
of
and
be an adaptationto theadverseeffects drought
4
proyears
of
a
period
over
marsh
the
upper
showsthatadditionsof nitrogento
and
Ernst
(1965)
of
vegetation.
the
duced little-change in the overall composition
growth
relative
low
the
that
indicated
have
Antonovics,Bradshaw & Turner(1971)
theadaptation
soilsmaynot onlyreflect
ratesof plantsgrowingon metal-contaminated
to soils of low
adaptation
their
but
also
conditions
of theseplantsto adversenutritional
to
occur
where
environmental
is
most
likely
waterpotential.Populationdifferentiation
conditionsvarygreatlyin space, but are relativelystable in time (Levins 1962, 1963;
marsh,spatialdifferMaynard-Smith1966; Snaydon & Davies 1972).WithinStiffkey
large
and
corresponding
3
and
although
4),
in
conditions
are
evident
(Figs
ences edaphic
data
preannual
the
hence
cycle;
of
a
predictable
are
part
occur
they
temporalchanges
generalization.
in
the
above
this
support
paper
sented
The effectof grazingis an additionalselectionforcewhichmayaccountforprostrate
growthformsin populationsof some species,such as Plantagomaritima.These upper
marsheson the northNorfolkcoast wereused in historicaltimesfor sheep grazing,a
practicewhichcontinueduntilthe outbreakof the second worldwar. Althoughfarm
stocksno longergraze thesemarshes,rabbitgrazingis prevalentin some areas of the
heads of Triupper marshin late spring.The leaves of P. maritimaand the flowering
In thecase of thelatterspeciesthisgrazingis an
glochinmaritimaare grazedselectively.
additionalmechanismwhichrestrictsgene flowbetweenthe upper and lower marsh
populations.However,dwarfplantswitha prostrategrowthformare foundin theupper
marsheson Scolt Head Island where,accordingto theWarden(Mr R. Chestney),sheep
grazinghas not occurredand whererabbitgrazingis absentat sitesaway fromdunes.
These observationsindicatethatgrazingalone cannotaccountforthe observedgrowth
speciesin theuppermarshesalong the northNorfolkcoast.
formsof the different
in a
in late Julyor earlyAugust,resulting
marshat Stiffkey
the
upper
tide
covers
The
fallin salinityand an increasein thewatercontentof thesedimentsof theuppermarsh.
Salicorniaeuropaeaagg. and
Halimioneportulacoides,
At thistimeofyearAstertripolium,
Suaeda maritimaundergoconsiderablegrowthand development,primarilyassociated
of ammoniumand nitrateions fallsin the
The concentration
withsexual reproduction.
bulk soil solutionsin late summerin both the upperand lowermarshes.Pigott(1969)
864
Growthresponsesofhalophytes
to nitrogen
has suggestedthata significant
difference
betweenthelowerand upperpartsofthemarsh
is theextentto whichthesedimentis exploitedby therootsof perennialspeciesalready
present.In the uppermarsh,the rootsof the annual species,whichoftenare less than
1-5cm in length,are unable to exploitthe sedimentsat a timewhen,in any event,the
concentrationof ammoniumand nitrateions is fallingin the bulk soil solution.The
observedgrowthresponsesof uppermarshannualssuchas Salicorniaeuropaeaagg. and
Suaeda maritimawhenadditionsof nitrateto the soil are made (Pigott 1969; Stewart
et al. 1972) indicatesthatthe annualsare subjectto nitrogen-limitation
at thisstagein
theirlife-cycle.
The larger,morerobustplantsof Salicorniain the lowermarsh,which
growin purestands,are probablytetraploidand havea moreextensiverootsystemthan
annual Salicorniaplantsfromtheuppermarsh.Not onlyare theseplantsable to exploit
the sediments,but competitionfromperennialplantsis absentover muchof the lower
in theseplants
marsh,and consequentlythereis littleindicationof nitrogendeficiency
(Pigott1969; Stewartet al. 1972). Pigott(1969) has suggestedthatthe perennialplant
is also apparently
Halimioneportulacoides
dependentforvigorousgrowthon unexploited
in freshsediment.The markedgrowthresponseto nitrogenwhichthisspecies
nutrients
showsin culture,and thehighlevelsof solubleinorganicnitrogenin thesedimentsofthe
leveesof creeks,supportthissuggestion.
ACKNOWLEDGMENTS
Thanksare due to Miss K. Hiramoni,Miss D. Omotomiand Mr N. Perkinsforskilled
technicalassistance;to Mrs J. Crook,Mrs D. Hunn and Mrs N. Nolan forpreparation
of thetypescript;
and to Drs J.Antonovics,J.Dainty,A. J. Davy, A. J. Grayand D. S.
Ranwellforconstructive
criticismof themanuscript.Part of thisstudywas financedby
a grantfromtheNational ResearchCouncil of Canada.
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