Seedling Leaf Structure of New England
Maples (Acer) in Relation to
Light Environment
P. Mark S. Ashton, Hae Soon Yoon, Rajesh Thadani,
Graeme P. Berlyn
and
ABSTRACT.Seedlingleavesof the genusAcerfromsouthernNew Englandwere comparedin relation
to light.The species investigatedwere red maple (A. rubrumL.), a species tolerant of xericand hydric
sites; silver maple (A. saccharinum L.), a species restricted to riparian sites that are periodically
flooded; and sugar maple (A. saccharum Marsh.), a mesic species of lower slopes and valleys.
Germinatingseedlingsof all species were collectedand grownwithinfour shade treatments that had
contrastinglightquantityand quality:(1) approximately100% of full sunlight,red:far-redratio = 1.27;
(2) 40% of full sunlight,ratio= 0.97; (3) 15% of full sunlight,ratio = 0.85; and (4) 4% of full sunlight,
ratio = 0.46. Leaves, cuticles, and epidermal and palisade mesophyllcell layers were all thicker, and
stomatal densities were higher for all three species in the full sun treatment. Dimensionsof leaf
structure (leaf thickness, palisade mesophyllthickness, lowerepidermal thickness) were between 25
and 35% smaller for silver maple as compared to the other maples. Silver maple also allocated less
biomass to roots (about 15% less) and more to stems. Its thin upper surface cuticle, thin leaves, and
large leaf area predispose this species to desiccation. Phenotypic plasticity of leaf anatomical
measures was greatest for red maple, suggestingit to be more of a generalist than its congeners. Red
maple allocated greater biomass to roots in shade (17% and 27% more than sugar and silver maple
respectively),with thicker leaves and cuticle, making it least prone to desiccation. Sugar maple had
greater dry mass and total leaf area in the deepest shade than the other maples. Measures of leaf
structurecan provideusefulinsightsintoknownecologicalaffinitiesof site and shade-toleranceamong
maples. FoR.Sc•. 45(4):512-519.
Additional Key Words: Acer rubrum, A. saccharinum, A. saccharum, leaf anatomy, red:far red ratio.
Researchers
have focusedon the regenerationstageof
succession,
becauseit is a periodthatdetermines
futuretree
species
composition
formostforesttypes(Egler1954,Grubb
1977,Ashton1992).Therefore,thisstageprovidesa critical
windowof timeforunderstanding
differences
amongspecies
in anatomy,physiology,and ecology(Ashtonand Berlyn
1992, 1994). By usingmore refinedfield and greenhouse
studies,theregeneration
stagecanbeusedto examinedifferencesin shadetoleranceof closelyrelatedspecies.
T HE
MANIPULATION
OF
nFOREST
CANOPY
for
the
purpose
of alteringlightavailabilityis animportantsilviculturaltechniquefor favoringor excludingtreesof a
particularshadetolerance.Many studieshave soughtto
differentiatelightresponses
of temperatetreespeciesin order
to arrangethem into differentsuccessional
groupsfor the
purposeof silviculture(Jackson1967a,1967b,Loach1967,
1970, CarpenterandSmith1975, Bazzaz1979, Bazzazand
Carlson1982, Walters andReich 1996, Reich et al. 1998).
P. Mark S. Ashton,RajeshThadani,and Graeme P. Berlynare AssociateProfessorof Silviculture,DoctoralCandidate,and Professorof True Anatomy
and Physiologyrespectively,Schoolof Forests,and EnvironmentalStudies, Yale University,New Haven, Connecticut06511. Hae Soon Yoon •s
Professorof Biology,Departmentof Biology,Dong-A
University,
Pusan604-714, Korea.Authortowhomcorrespondence
shouldbe addressedis Mark
S. Ashton.
hone: (203) 432-9835; Fax: (203) 432-3809; E-maihmark.ashton@yale.edu.
Acknowledgments:
The studywas donewhileHae SoonYoonwas on sabbaticalat Yale University.Shewouldliketo thank Dong-AUniversity,Pusan,
Koreafor the fellowshipthat made this studypossible.We wouldalso like to acknowledgethe logistichelp receivedfrom SarojSivaramakdshnan
and lliana Ayala,
ManuscriptreceivedAugust17, 1998. AcceptedApril15, 1999.
512
ForestSctence
45(4)1999
Copyright¸ 1999 by the Societyof AmericanForesters
Formaples(Acerspp.),fieldstudies
havefocused
oncomparisons
between
canopy
andunderstory
species
in relationto
forestmicroenvironments
(Lei andLechowicz1990,Sipeand
Bazzaz1994,1995).Lei andLechowicz
(1990)studied
saplings
of co-occurring
maplespecies,
in a mesicnorthern
hardwood
forestin Quebec,
Canada.
Theunderstory
species
in theirstudy,
stripedmaple(A.pennsylvanicurn
L.) andmountain
maple(A.
sptcaturn
Lam.), had characteristics
(largeleaf area,planar
architecture)
thatmadethemmoreshade-adapted
thansugar
maple(A.saccharurn
Marsh.).Amongeightmaplespecies
from
AsiaandNorthAmerica,LeiandLechowicz
(1997,1998)found
differences
in photosynthesis
andwater-use
betweencanopy
andunderstory
species
andbetweenthosespecies
knownto be
light-demanding
versus
thosethatareshade-tolerant.
Similarly,
SlpeandBazzaz(1994,1995)showedA.
rubrumL. (redmaple)
survived
in a widerrangeof lightenvironments
ascompared
to
sugarandstripedmaple.All thesestudies
haveprovidednew
insightintoourunderstanding
of linkages
betweentheecology
andphysiology
of trees.
The objectiveof our studywas to build on this work by
examiningrelationships
betweenattributesof leaf structure
and the ecologicalsite affinitiesof threemaplespecies.
Certain attributesof leaf structure(i.e., cuticle thickness,
palisademesophylllayer thickness,stomataldensity)may
provideinsightinto someof the underlyingmechanisms
affectingthe shadetoleranceand site affinitiesamongred,
sugar,andsilvermaple(A. saccharinurn,
L.). We hypothesizethat speciesrankingsof leaf structureattributeswill
changeacrossthelight treatments
in a directionconsistent
with the knownsite affinity of the species.Basedon the
literature,
wewouldalsoexpectmaplespecies
thathavebeen
recorded
tobemoresitegeneralist
(i.e.,redmaple)toexhibit
greaterplasticityin leaf structure
betweenthebrightest
and
darkestshadetreatments
ascomparedto maplespeciesthat
areconsidered
sitespecialists
(i.e., sugarmaple).
The speciesselectedfor our studyall occurwithin the
mixed-deciduous
forestof southern
New England,buteach
species
appears
restricted
moreorlesstodifferentsiteconditions(BurnsandHonkala1990).Redmapleis a lightgenerahstthat growswell in shadeand sun.Red mapleis also
tolerantof shallowsoilsof uplands
thatareseasonally
xeric,
andalsohydricsoilsthatareseasonally
anaerobic,
although
ecotypic
differences
in physiology
andgrowthappearnotto
exist (Will et al. 1995). Sugarmaple is a shade-tolerant
species
thatoccupies
thelowertoe-slopes
withdeepsoilsthat
are mesicyear round.The third species,silver maple,is
considered
light-demanding
andisrestricted
to floodedalluvialsoilsthatareadjacent
tomovingwaters.It canbeplanted
andgrownon well-drainedsites,but seldom,if ever,reproducesthere(Gabriel 1990).
Materials
and Methods
Shade Treatments
Eightshelters
wereerected(1 x 1x 2.5m woodenframes)
andplacedonbenches
withina greenhouse
at YaleUniversity.We alteredlightquality(R.'FRratio)andphotosynthetically activeradiation(PAR, 400-700 nm) to createfour
treatments
(twoshelters
pertreatment)
thatsimulated
arange
offorestlightenvironments.
TheR:FRratiowasmeasured
as
theratioof quantumirradiancebetweenthewavebands
655665 nm and 725-735 nm (Lee 1985, Lee et al. 1996).
Treatments were based on measurements made across forest
openings
onridgeandvalleysitesat theYale-MyersForest
in thenortheastern
uplands
of Connecticut
(41ø57'N; 72o07
'
W) (AshtonandLarson1996).Thisforesttypeis dominated
byanoak-hickory
canopy,
witha subcanopy
ofredmapleand
sugarmaple(Westveld
etal. 1956).Compared
withamature
northernhardwoodforest,wheremaplespeciesoftendominatethecanopy,understory
R:FR ratiosof theoak-hickory
foresttypeareconsiderably
higher(R:FRratioof 0.47versus
0.25),because
of moreopenconditions
withproportionately
fewerstoriesof shade-tolerant
treesbelowtheforestcanopy
(Canhamet al. 1990).
Thequalityandamountof lightfor threeof thetreatments
was alteredby sprayinga ratio of selectedpaintpigments
mixedin a varnishbaseontoclearplastic(Lee 1985,Ashton
andBerlyn1994).Quantumsensors
andthermocouples
(LI190 SZ, 190 SA, LI-1000-16, LI-COR, Lincoln, Nebraska)
were usedto obtainan estimateof daily PAR anddiurnal
temperature
variation.Measurements
weremadeevery 10 s
on severalsunnydaysat the beginningof the experiment
(June1994).Lightandtemperature
sensors
werepositioned
horizontally15 cm abovethegreenhouse
benchandwithin
the shelters. Ten minute means for each shelter were calcu-
latedbasedonthe 10 sreadings.Thesemeansweresimultaneouslyrecordedfrom sunriseto sunset(approximately15
hr) usinga datalogger(LiCor 1000).
Shadetreatmentsprovidedseedlingswith 4%, 15%,
40%, and100%of sunlight,basedondallyestimated
totalsof
PAR received(seeTable 1 for details).It shouldbenotedthat
the 100% treatment is less than incident PAR because of
somereflectionfrom the greenhouse.
Germinatingseedof redmaplewerecollectedduringthe
last2 wk of May 1994fromatleastfourdifferentparenttrees
in separate
locationswithin the Yale-MyersForest,Union,
Connecticut.All seedlingscollectedwere at the earliest
stagesof cotyledonexpansion,andnoneexhibitedany ob-
servable
leafinitiation.Germinating
seedlings
ofsilvermaple
of a similardevelopmental
stagewere collectedat four
separate
locationsalongthebanksof theQuinipiacriver in
Tabla 1. Light traatmants; PAR--photosynthatic activa radiation as a maasura of amount of light; R:FR--rad to far
red ratio of light as a measura of light quality.
Full sun(100%)
Diffuseshade(40% sunlight)
Brightunderstory(15% sunlight)
Darkunderstory
(4% sunlight)
PAR
MaximumPAR
Maximumtemp
R:FRratio
(molsm-2d-l)
(pmols
m-2s-l)
('C)
1.27
36.62
1,600
32
0.97
0.85
0.46
14.65
5.31
1.50
700
300
60
30
30
29
Forest
Sctence
45(4)1999 513
Hamden,Connecticut,
duringthe lastweek of May 1994.
Sugarmapleseeds
thathadbeendispersed
theprevious
fall
werecollected
in thesamemannerasredmapleattheYaleMyers forestduringthe secondweek of May 1994.Each
younggerminantwasimmediatelyplantedintoa plasticpot
(15 cm depth,10 cm diameter)that containedPromix(a
mixtureof sphagnum
moss,perlite,vermiculite,dolomite
andcalcitelimestone,and wettingagent,PremierBrands,
Inc.,Quebec,Canada).
A smallamountof foresttopsoilfrom
the seedlingcollectionsiteswasaddedto eachpot at the
beginning
of theexperiment
to ensurea sourceof vesiculararbuscular
mycorrhizae
(VAM) innoculum
for theseedling
roots.Fivepotsfor eachspecies
wererandomlyassigned
to
positions
withina shelter.All germinating
seedwasplaced
withintheshelters
beforeshootextension
to ensureproper
exposure
to thetreatments
duringleaf expansion
anddevelopment.To ensureagainstpossible
environmental
variations
in differentpartsof the greenhouse,
the positionof each
shelterwasrotatedmonthlyandwateringwasregulatedto
maintainthePromixat fieldcapacity.A standard
strengthof
Miracle-Gro,an NPK fertilizer (15-30-15), was addedat
monthlyintervals.
The seedlings
weregrownwithintheselight treatments
foratleastfourmonths(June1-September
30, 1994).At the
endof thisperiod,all seedlings
weremeasured
for height,
root collar diameter,and leaf area. Seedlingswere then
harvestedandrootswashedfree of soil,thenroots,stem,and
leaveswereseparated
anddriedfor 48 hr at 80øCfor determi-
nationof dryweights.Leafdryweightsincludedbothlamina
andpetiole.
AnatomyMeasurements
Foreachspecies,
a singleleaffromfiveseparate
seedlings
wererandomlychosenwithin sheltersfor eachshadetreatment.Onlyundamaged,
fullyexpanded
leaveswereselected.
To determinestomatadensity,stomataaperturelength,
andepidermalcelldensityleaf sections
(1 x 1 cm)weretaken
fromthesampleleafin themiddleportionof thelamina.Each
sectionwasincubated
in a 50øCovenin 5% sodiumhydroxideto clearleafpigments.
Sections
werethenstainedwith 12 dropsof 0.5% aqueous
toluidinebluesolutionandmounted
in Karolightcornsyrupona viewingslide.Foreachsection,
thetotalnumberof stomata
andepidermal
cellswerecounted
and three stomaaperturelengthswere measuredfor five
fields of view on the abaxial side of the leaf. No stomata were
observed on the adaxial leaf surfaces.
For cross-sections,
another1 x 0.5 cm piecewastaken
acrossthemidrib, adjacentto the sectionusedfor stomata
and epidermal measurement.This sectionwas cut into
threethinstripsof aboutI x 0.2 cmandimmediatelyfixed
in cold FAA (formalin:aceticacid: alcohol).The strips
weredehydratedin a tertiarybutyl alcoholseriesandthen
embeddedin separatewax blocks(Berlyn and Miksche
1976). Cross-sections
werecut of eachstripat 12 gxnwith
a cryotomeand mountedon a slide. The tissuewas then
stainedwith safraninandfastgreen(Berlyn andMiksche
1976). For each of the three slides, three measurements
weremadeof leaf thickness,
cuticlethickness
of theupper
leaf surface,upperandlowerepidermalcell thickness,and
spongyand palisadecell layer thickness.Each slide was
measuredin different positionsthat avoided the midrib
region.Threeleaf sectionsweremeasuredfor eachsingle
leaf selectedfrom eachof five seedlingsper speciesand
shade treatment. Measurements
of cell dimensions were
madeusinga 12.5 x filar micrometereye-pieceandsintable objectivesfor the variousmeasurements.
Statistics
We investigateddifferencesin leaf anatomyusingan
analysisof variance(SAS 1990) for a split-plotexperimental design where shadetreatments(two replicates)
were the main plots and tree specieswere subplots.For
eachmeasure,we testedfor main differencesamongshade
treatments;subplotdifferencesamongspecies;and for
interactionsamongspeciesand shadetreatments(Table
2). Whereshadetreatments
werepooled,differencesamong
specieswere analyzedat the 5% significancelevel using
Fisher's PLSD post hoc test. Responsecurve analys•s
using orthogonalpolynomialcontrastswere carried out
for each speciesacrossthe shadetreatments(4%, 15%,
40%, and 100% of full sunlight).Contrastscompared
relationships
betweenthe variousleaf structuremeasurements and light levels using both linear and quadratic
constraints(Table 2). We usedboth linear and quadratic
constraints
to examinewhetherspeciesexhibiteddifferent
contrastrelationships.
For a measure of the variation in anatomical attributes we
usedan indexof phenotypicplasticity(P = [1-(x/X)]) that
includedcomparisons
betweenmeanvaluesfor the darkest
(x) andbrightest(X) shadetreatments.
To obtaina relatave
comparison
amongspecies
of theamountof stomata
areaper
unit areaof leaf we usedthe productof stomataaperture
Table 2. F-valuesfor analysesof varianceof variousanatomicaland growth measuresusinga split-plotdesignwhere shadetreatments
were the main treatments and the subplots were species.Variable codes are: LT--leaf thickness;CT--cuticle thickness;UE--upper
epidermis;PM--palisade mesophyll;LE--Iower epidermis;EP--upper epidermal density; SF--stomatal frequency; DW--dry weight;
HT-- height;RC-- root collardiameter;SLA- specificleafarea;TLA--total leaf area;LMR--leafmass ratio;SMR--stem massratio;RMR-root mass ratio. Levels of significance: P< 0.05, *; P< 0.01, **; P< 0.001, ***
Shade
Residual
df
3
4
Species 2
LT
10.1'*
CT
3.6*
UE
6.5*
PM
19.3'**
LE
4.8*
EP
1.4ns
SF
DW
2.4ns 62.5***
HT
75.1'**
RC
111.4'**
SLA
4.2*
TLA
60.1'**
LMR
SMR
1.6ns 1.3ns
RMR
2.0ns
23.8*** 2.4ns 26.4***
30.8***
11.3'*
5.74*
2.35ns 26.5***
83.8***
46.4***
3.4ns
15.6'*
2.2ns
2.4ns
3.5*
0.9ns 0.9ns 0.9ns
1.9ns
0.9ns
0.6ns
10.2'*
13.8'**
3.1ns
4.5ns
0.9ns
1.0ns
1.0ns
Shade x
species 6
Subplot
residual 8
Error
23
514
Forest
Sctence
45(4)1999
l.lns
5.8ns
lengthandstomata
density,andcalledit stomata
areaindex
(SAI) (AshtonandBerlyn1994).We alsousedSalisbury's
stomatal
indexwhichistheratioof guardcellnumberto total
epidermalcell number(excludingguard cells) to better
understand
howstomata
densityisinfluencedbylightduring
leafdevelopment
(Salisbury1928).
Results
Leaf Anatomy
Analysesshowedthat differencesamongleaf samples
taken from the samespeciesand within the samelight
treatmentwerenot significantly
differentfromeachother.
Comparisons
amongspecies,
andamonglighttreatments,
all
showedhighly significantF values(? < 0.01) (Table 2).
Interestingly,interactions
betweenspeciesand light treatmentwere not significant,suggesting
that speciesdid not
changerankin relationto eachotheracrosslight levelsfor
anyof the anatomicalmeasures.
Leaf thickness
andupperepidermal,palisademesophyll
and lower epidermallayerswere greatestfor red maple.
Cuticle thicknesswas an exceptionwhere red and sugar
maplehadthe samethicknesses.
Thicknesses
for almostall
attributesmeasured,exceptfor the upperepidermallayer
thickness,
wereleastfor silvermaple(Table3).
Phenotypicplasticity(P) of leaf blade,and upperand
lowerepidermallayerthicknesses,
wasgreaterforredmaple
ascompared
totheothermaples(Table3). Bothredandsugar
maple,however,hadgreaterplasticitiesof cuticleandpalisademesophyllthicknesses
thansilvermaple.
For all species,leaf thicknessexhibitedeffectsin contrast that were significantwith increasein light levels.
Contrastsshowedapproximatelymonotonicupwardsloping relationshipsas leaf thicknessincreasedwith light
Tabla3. F-valuesfor responsecurveanalysescomparingmaasuresof tha variousleaf attributasacrossthe four light treatmantsusing
linaar and quadraticcontrasts(laveIsof significanceP< 0.05, *; P< 0.01'*). Maans ara givan with standarderrorsin paranthesasfor the
various leaf anatomical attributes for aach light traatment and for all traatments combined. Fishar'sPLSDtast (P < 0.05) was usad to
comparepooledmaansof aachspecies[lattersdenotedifferencesamongspacies(A> B> C)].P= Plasticity[1 (x/X)] whare xis tha value
in 4% sunlightand Xis the valuain 100%sunlight.
Comparisons
amongspecies
Contrasts
(means
over
Linear Quadratic all treatments)
4%
Comparisons
among
treatments
foreachspecies
15%
40%
100%
P
Leaf thickness(gm)
A. rubrum
A. saccharinum
A. saccharum
15.49'*
25.47**
8.56**
26.12'*
10.07'
4.13ns
93.36(2.68)A
67.83(1.83)C
81.90(2.88)B
77.39(3.20)
59.19(2.48)
71.79(5.35)
84.98(2.82)
62.74(2.89)
71.81(3.46)
98.83(2.57)
73.89(2.79)
87.63(4.53)
108.92(5.14)
72.61(3.72)
90.76(6.11)
0.29(0.03)
0.20(0.02)
0.20(0.03)
2.56 (0.14)
2.29 (0.06)
2.16 (0.10)
2.33(0.44)
2.37 (0.14)
2.59 (0.13)
2.63 (0.46)
2.52 (0.13)
2.51 (0.24)
3.10(0.22)
2.42 (0.17)
2.96 (0.30)
0.24(0.02)
0.09(0.01)
0.27 (0.03)
15.33(0.49)A
11.77(0.36)B
11.71(0.32)B
12.87(0.74)
10.64(0.95)
11.12(0.29)
14.60(0.98)
11.13(0.62)
11.31(0.45)
16.34(0.69)
12.89(0.70)
12.27(0.70)
17.04(0.99)
12.04(0.61)
11.85(0.73)
0.24(0.05)
0.16(0.02)
0.09(0.02)
40.65(1.62)A
27.58(1.02)C
32.78(1.85)B
29.99(1.34)
22.27(1.67)
25.64(2.70)
37.66(1.31)
24.87(1.04)
25.17(1.97)
44.49(2.04)
30.53(1.49)
36.58(2.18)
48.56(2.04)
30.88(2.25)
39.70(4.09)
0.38(0.06)
0.27(0.03)
0.37(0.03)
11.91(0.40)A
9.63(0.30)C
10.25(0.24)B
12.16(0.83)
8.86(0.34)
10.61(0.42)
10.30(0.56)
8.81(0.40)
9.47(0.40)
11.41(0.69)
10.11(0.80)
10.26(0.43)
13.69(0.76)
10.50(0.49)
10.72(0.54)
0.25(0.03)
0.15(0.02)
0.11(0.03)
3,092(105)B
4,226(101)A
3,999(165)A
3,168(72)
3,996(93)
4,158(148)
3,188(131)
4,628(97)
3,484(175)
2,685(114)
4,025(150)
3,576(146)
3,326(103) 0.19(0.03)
4,254(64)
0.13(0.03)
4,781(192) 0.27(0.04)
460 (11.9)B
516(12.3)A
406 (16.4)C
385 (11.6)
420 (6.1)
378 (17.6)
471 (10.0)
573(13.3)
339 (9.3)
439 (13.0)
576(16.4)
364 (7.9)
545 (13.1)
498(12.4)
543 (32.0)
0.29(0.03)
0.26(0.03)
0.38(0.05)
12.5(0.25)
10.6(0.22)
10.4(0.27)
13.0(0.22)
9.7 (0.26)
12.2(0.44)
14.4(0.30)
7.7 (0.11)
8.0 (0.26)
0.12(0.02)
0.27(0.03)
0.35(0.04)
Cuticlethickness
(gm)
A. rubrum
A. saccharinum
A. saccharum
7.19'
1.71ns
0.31 ns
62.49**
0.34ns
5.77*
2.67 (0.09)A
2.41 (0.06)B
2.61 (0.12)AB
Upperepidermallayerthickness
(gm)
A. rubrum
`4. saccharinum
`4. saccharum
16.14'*
3.95*
1.10ns
17.14'*
0.95ns
0.10ns
Pahsade
mesophyll
layerthickness
(gm)
`4. rubrum
`4, saccharinum
`4. saccharum
11.76'*
13.47'*
4.83ns
17.52'*
6.72*
2.88ns
Lowerepidermal
layerthickness
(gm)
`4. rubrum
`4. saccharinum
0.00ns
11.30'*
3.64ns
10.87'*
•4. saccharum
0.04ns
0.00ns
Epidermal
celldensity
(number/ram
2)
`4. rubrum
.4. saccharinum
.4. saccharum
0.47ns
2.59ns
1.14ns
0.28ns
0.25ns
6.58*
Stomata
density
(namber/mm
2)
.4. rubrum
.4. saccharinum
.4. saccharum
1.07ns
0.12ns
0.00ns
33.09***
0.05ns
2.20ns
Stomaaperture
length(gm)
.4. rubrum
0.45ns
0.89ns
.4. saccharinum
.4. saccharum
0.00ns
3.02ns
1.13ns
3.63ns
13.13(0.23)A
12.5(0.16)
9.30(0.17)B
9.2 (0.09)
10.13(0.27)B
9.9 (0.12)
Stomata
areaindex(number/mm
2* aperture
length)
.4.rubrum
1.91ns 18.83'
6,040(131)A
4,812(103)
.4.saccharinum 2.24ns 0.76ns 4,799(101)B
3,864(44)
.4.saccharum 0.49ns 0.07ns 4,113(138)C
3,742(108)
Stomatal
index(guardcellnumber/epidermal
cellnumber)
.4. rubrum
0.25ns 0.35ns
.4. saccharinum
.4. saccharum
5.52ns
0.24ns
0.01ns
0.09ns
5,887(121)
5,707(164)
7,848(176) 0.39(0.05)
6,074(130)
3,526(100)
5,587(153)
4,441(128)
3,835(75)
4,344(198)
0.297(0.030)A 0.243 (0.026)
0.244(0.023)AB 0.210(0.018)
0.295(0.031)
0.276(0.022)
0.327(0.036)
0.286(0.032)
0.328(0.027} 0.26 (0.03)
0.234(0.012) 0.27(0.04)
0.203(0.034)B 0.182(0.041)
0.195(0.038)
0.203(0.031)
0.227(0.049) 0.20(0.03)
0.38 (0.06)
0.21(0.06)
ForestSctence
45(4)1999 515
Whole-Plant Size
level, with linear constraintsshowinglevels of significancefor all species,and quadraticconstraintsshowing
significancefor red andsilvermaplesonly (Table 3).
Increases
in cuticlethickness
showedsignificanteffectsin
quadraticcontrast
withanincreasein lightlevelsfor redand
sugarmaplebutnotfor silvermaple.Linearcontrasteffects
wereonlysignificant
across
lightlevelsforredmaplecuticle
thickness.Upper epidermallayer thicknessalsoincreased
with an increasein light levels but this contrastwas only
significantfor redmapleandto a lesserdegreesilvermaple
(linear contrast).Increasesin palisadethicknessshowed
significantcontrasteffectswith increasein light levelsfor
bothredandsilvermaple.Onlysilvermapleshowedsignificantcontrasteffectsfor lowerepidermis.
With theexception
of thequadratic
contrast
forredmaple,
nosignificant
effectswereshownbetweenstomata
aperture
lengthor stomatadensityandincreasinglight levels(Table
3). Stomatadensitywasgreatestfor all treatmentsin silver
maple,followedin decliningorderby red mapleandsugar
maple(Table3). Stomataaperturelengthwasgreatest,but
plasticitywas lowest for all treatmentsin red maple as
comparedto silverandsugarmaple.The smallestaperture
lengthsfor silverandsugarmaplewere in the 100%treatment.However,redmaplehadthe largeststomataaperture
lengthatthislightlevel.Sugarmaplewasthemostplasticfor
stomatadensityandaperturelength.
Stomataareaindex(SAD indicatedredmapleto havethe
highestrelativestomataarea,followedin decliningorderby
silvermapleandsugarmaple.SAI plasticitywasalsohighest
in redmaplefollowedby silvermapleandthensugarmaple
(Table 3). Salisbury'sstomataindex demonstrated
similar
trends(Table 3).
Contrastsusinglight levelsagainstvariousmeasuresof
leaf size andarea,andthe variousmeasures
of plantsize
(height,rootcollardiameter,drymass)all showedsigmficantlinearandquadraticeffects,exceptfor ratio between
leaf areaandleaf mass(specificleaf area;SLA) (Table 4).
Specificleaf areawashighestfor all threespeciesin the
4% treatment and lowest in the 100% treatment, but
contrastswereonly significantfor silvermaple(Table4)
Thoughthe samegeneraltrendwasevidentfor all species,
relativedifferencesbetweenhigh andlow light treatments
were greatestfor red maple.Total leaf area per seedhng
wasgreatestfor the 100% treatmentandlowestfor the4%
treatment. In the 100 %treatment, the individual leaves are
thereforesmallerin area,but therewere sufficientlymore
leavessothattheoverallleaf areaof theplantswasgreater
Relative differences in total leaf area between the 4% and
100% treatmentswere greatest in both silver and red
maple as comparedto sugarmaple. In addition, they had
largertotal leaf areasper seedlingthansugarmaplein all
but the 4% treatment(Table 4).
All sizemeasurements,
namelyheight,diameterof root
collar,andtotaldry massof seedlings,werehighestin the
100%treatmentfor all species,andweregenerallylowest
in the 4% shadetreatment.Measuresof height and root
collarshowedsignificantinteractionbetweenspeciesand
light treatmentsindicatingthat specieschangedrank m
relationto eachotheracrossthe differentlight treatments.
In all cases,greatestdifferencesamongtreatmentswere
shownin silver and red maple (Table 4). Silver maple
allocatedproportionatelylessamountof biomassto roots
as comparedto the othermaple species(Figure 1).
Tabla 4. F-valuesfor response curve analyses comparing maasuras of growth acrosstha four light treatments using linaar and quadratic
contrasts(levalsof significanceP< 0.05, *; P < 0.01**). Meansare givenwith standarderrorsin parenthasasforthe variousleafanatomical
attributas for each light treatmant and for all treatments combined. Fisher's PLSDtast (P < 0.05) was usad to compare pooled means
of each species[letters denota diffarencesamong species(A > B > C)]. P = Plasticity[1 - (x / X)] where x is the value in 4% sunlightand
X is tha valua in 100% sunlight.
Comparisons
among
Contrasts
treamaents
for
Linear
Quadratic eachspecies
Height (cm)
d. rubrum
22.2**
d. saccharinurn63.5***
A. saccharum 4.41ns
Rootcollar diameter(mm)
d. rubrum
75.9***
d. saccharinurn76.7***
d. saccharurn 29.22**
Total dry mass(g)
d. rubrum
19.1'
d. saccharinurn35.0***
d. saccharum 12.6'*
4%
Comparisons
amongspecies
(meansoverall treatments)
15%
40%
100%
P
22.16 (1.26)B
28.97 (1.87)A
13.63(0.81)C
9.99 (0.75)
11.75(1.51)
10.53(1.11)
19.36(2.01)
26.14 (2.25)
10.51(0.98)
26.94(1.71)
36.51 (2.56)
14.82(1.75)
30.46(2.06)
41.49 (2.38)
17.47(1.60)
0.67 (0.06)
0.71 (0.06)
0.41 (0.05)
111.0'**
57.0***
73.8***
4.46 (0.22)A
3.52 (0.20)B
3.09 (0.15)B
2.18 (0.15)
1.61(0.08)
2.73 (0.16)
3.90 (0.26)
3.17 (0.28)
2.28 (0.10)
5.41 (0.27)
4.52 (0.28)
3.16 (0.20)
6.01 (0.38)
4.80 (0.26)
3.94 (0.39)
0.64 (0.06)
0.66 (0.05)
0.32 (0.04)
27.6**
34.5***
22.1'*
2.49 (0.25)A
1.84(0.23)B
1.10(0.12)C
0.42 (0.07)
0.13 (0.02)
0.69 (0.16)
1.47(0.24)
1.15(0.23)
0.52 (0.06)
3.32 (0.32)
2.68 (0.44)
1.24(0.21)
4.45 (0.50)
3.41 (0.42)
1.78(0.30)
0.90 (0.08)
0.97 (0.07)
0.61 (0.06)
3.82ns
42.16'*
1.75ns
3.96 (0.16)B
4.48 (0.26)A
4.08 (0.37)B
7.76 (0.46)
6.21 (0.36)
6.80 (0.70)
3.04 (0.09)
4.81 (0.21)
3.63 (0.37)
2.63 (0.09)
3.75 (0.24)
3.38 (0.68)
2.39 (0.13)
3.17 (0.22)
2.53 (0.16)
0.69 (0.06)
0.49 (0.05)
0.64 (0.07)
32.1'**
78.15'**
5.86*
Specific
leafarea(SLA;cm2/g)
d. rubrum
2.94ns
d. saccharinurn39.10'*
d. saccharum 0.12ns
Totalleafarea(cm2)
d. rubrum
30.44*
d. saccharinurn29.21'
14.65'
13.25'
199.42(19.09)B
250.01 (29.54)A
d. saccharurn 27.05*
17.32'
103.17(22.13)C 52.1(12.4)
516
ForestSctence
45(4)1999
38.6 (6.6)
34.7 (6.1)
175.4(24.9)
230.7 (30.2)
281.1 (13.8)
374.3 (51.7)
302.7 (30.9)
360.3 (30.3)
0.87 (0.11)
0.90 (0.08)
64.8(15.0)
140.3(33.0)
155.4(28.1)
0.67(0.07)
A.rubrum
A.sacchartnum
A.saccharum
[]
Leaves
[]
Stem
ß
Roots
to differinglight regimesare consistent
with the broad
distribution
of redmaple,ascompared
to theothermaple
species
in thisstudy.Thismaygiveredmaplea competitive
advantage
wherewaterislimitingandinmoreopen,desiccatingenvironments
(Will et al. 1995,Canhamet al. 1996).
Silvermaplegrowsalongstreams,
ponds,
lakesandrivers.
It growslargest
in rivervalleysonwet,poorlydrained
soils.
It isa medium-lived
tree(125-150yr)thatisshade
intolerant
(Gabriel 1990), andit can withstandseveralweeksof flood-
ing(Hosner
1960).Although
it iswidelyplanted
inyards
and
Percentage PPFD of the abada treatment•
Figure1. Proportionalallocationof dry massto roots,stem,and
leavesamongthelighttreatments
foreachofthespecies.
Light
treatment was measured as a percentage of the total
photosynthetic
photonflux density(PPFD)recordedin the full
sun treatment.
Discussion
Whenleafanatomical
measures
aretakenseparately,
they
did not changerank acrosslight levelsfor the different
species,
suggesting
thatrelationships
among
maplespecies
remained
consistent.
However,
comparing
measures
of leaf
anatomy
withgrossmeasures
of plantsize,maplespecies
showed
separate
relationships
different
fromeachother.Our
studyof leafstructure
variation
in relationto changes
in
whole-plant
sizesupports
evidence
thatmaplespecies
ofthe
southern
New Englandforestshavesite affinitiesthatare
bothdistinctyetoverlapping
in relationto eachotherwith
regardto availability
of lightandsoilwater.The study
showed
howleafanatomical
andplantsizeattributes
of the
threemaplespecies
aresuited
tothedifferent
habitats
they
occupy
ontheforestlandscape
fromstreamsides
tohilltops.
Inthenextfewparagraphs,
wediscuss
relationships
between
leafstructure,
measures
ofplantsize,andsiteaffinitysepa-
parks,it seldomregenerates
in thesesituations
dueto insufficientlight andwater(Gabriel1990).The thinnerdimensionsin leafstructure,
low proportional
allocation
to roots,
greaterheight growth,and smallerroot collar diameters
indicatethatsilvermaplewouldgrowfaster,relativeto the
othermaplesin highlightenvironments
wheresoilwaterwas
plentiful.
Incontrast
toredmaple,silvermaplegrows
talland
thin seedlings,
a growthhabit that wouldbe suitablefor
nutrient-rich
andever-moist
soilsof floodplains,andwhere
competitionfor light, ratherthan soil water, is the most
limiting factor. This is consistentwith resultsfrom other
studiesthatcompared
heightgrowthof shade-intolerants
withshade-tolerants;
shade-intolerants
havegreater
height
growththanshade-tolerants
evenin low lightconditions
(Loach1970•treatments
providing
3 and17%sunlight;
Walterset al., 1993a,b•treatment
providing15-20%sunlight;WaltersandReich1996--treatment
providing
8%).
However,
inverylowlightconditions
(e.g.,2%)Waltersand
Reich(1996)foundshade-intolerant
species
grewslower
thanshade-tolerants;
butwedidnotfindthisforour4%light
treatment.
Also,thelowerlevelsof responsiveness
thatwe
observed
in silvermaple,relativetoredmaple,in almostall
dimensions
ofleafstructure
(leafthickness,
cuticle,
palisdae
mesophyll,
upperandlowerepidermal
layers)isalsoconsistent with silver maple'srestrictionto certainsites.Our
findings
on theleafstructure
of silvermaplecorroborate
ecological
observations
thatit isalight-demanding
specialist
ratelyfor eachspecies.
requiring
moistsoilsandthefull sunof largecanopy
openRedmaple
grows
inalmost
two-thirds
ofthe88nontropi- ings.Unlikeredandsugarmaple,thereis no supporting
calforestcovertypesin eastern
NorthAmerica(Waltersand
literature
onthefunctional
properties
of silvermaple.
Yawney1990).It formsredmapleswamps
andoccurs
on
Sugarmaplegrowsin 24 forestcovertypesof eastern
drought-prone
hilltopsintheregion;
it maygrowinassocia- NorthAmericaandisa majorcomponent
in 7 (Godman
etal.
tionwithbothsugarandsilvermaple.It isconsidered
shade
1990).It isfairlylong-lived
(250-400yr)andoneofthemost
tolerantandgrowsfromsealevelto 2000m (Waltersand
shadetolerantmaplespecies.
It is restricted
to well-drained
Yawney1990,Harlowet al. 1991).Red maplehadthe
soilsanddoesnotoccur
in swamps
orsitesthatareperiodithickest
leavesunderall lighttreatments.
Thisthickness
was
callyinundated.
It alsodoesnottolerate
dry,shallow
soils.It
manifested
in allcelllayers
measured,
viz.epidermis,
paligrowsathighelevation
in thesouthern
Appalachians
(2,000
sademesophyll,
andcuticle.
Redmaplehadthegreatest
root
m), whereas
in NewEnglandit isseldomseenabove1,000m
collardiameter
for all lighttreatments
ascompared
to the
(Godman
etal. 1990).Theleafstructure
ofsugar
maple
is,in
most cases,intermediate in measureddimensionsbetween
other
species.
In thelowlighttreatment
(4%)redmaple
had
a highproportion
ofitsdrymass
allocated
toroots(54%and
redmaple
andsilvermaple.
Thehighdimensional
changes
of
30%greater
allocation
ascompared
tosugar
andsilver
maple sugar
maplepalisade
mesophyll
thicknesses
across
thelight
respectively),
supporting
similarfindingsof studies
donein
treatments
suggests
an abilityof sugarmapleto adaptto
shade
houses
(Gottschalk,
1994,Groninger
etal. 1996)and
varied
lightenvironments.
Thisisbecause
thepalisade
mesotheforestunderstory
(SipeandBazzaz1994,DeLuciaetal.
phylllayerisanimportant
siteforlightcapture
andphotosyn1998).Thismorphological
traitmayprovide
structural
bulk
thesis.
Sugar
maplehada greater
totaldrymass
(39%more),
andconsiderable
space
forcarbohydrate
andwaterstorage. rootcollardiameter(20%more),andtotalleaf area(26%
All these
attributes
andtheirhigher
levelsofresponsiveness more)inthelowlighttreatment
ascompared
toredmaple,
the
ForestSctence
45(4)1999 517
next highest.The lowerproportionalallocationto rootsof
sugarmaple(30% less)in low lightsuggests
it mightbemore
susceptible
to soil moisturestressthan red maple.Also,
becausemeasuresof plantsize acrossthe light treatments
weresmallerfor sugarmaple(height-63%less;rootcollar
diameter-50%less;totalleaf area-22%less;anddrymass32% less)thanthe othermaples,we suggest
thatit is less
responsive
(SipeandBazzaz1994,Canhamet al. 1996,Lei
andLechowicz1997).As concludedby Walterset al. (1993
a,b), sugarmaple may be lessresponsiverelative to other
species
because
a greaterconcentration
of resources
maybe
allocatedto productionof protectivecompounds
to resist
herbivores
andpathogens.
However,ourstudyshowedthat
changein palisademesophylldimensionis high, an indicationof abilityto photosynthesize
in differinglightlevels.All
thesedata supportthe ecologicalobserVations
that sugar
maplehasa competitiveadvantage,
relativeto redandsilver
maple, in mesic shadyconditionswhere it can investin
resourceconservation
for survivalratherthanheightgrowth
increase(Pacalaet al. 1994, Kobe et al. 1995).
Findingsin ourstudyareconsistent
withthoseof Sipeand
Bazzaz(1994, 1995) who showedthat red maple survives
better,overall, acrosscanopyopeningsin a centralNew
Englandforestascompared
to sugarmaple.Thiswouldfit the
"generalist"growthof red maple.Our studyalsoprovides
evidencefor theability of red mapleto endureshadewithin
theforestunderstory
particularlyondriersites,asreportedin
studiesby Lorimer (1984) andKelty et al. (1988), andfor its
capacityto establishandgrowwell in thehighlight environmentspresentin earlyseralstageforest(OliverandStephens
to investigate
effectsof competitionunderfield situations.
In conclusion,
thisstudyis thefirstto provideinsightinto
someof the linkagesbetweenleaf structureandecological
site affinitiesfor maples.For example,in silver maple,a
speciesknownto be restrictedto hydricsites,the thinner
dimensions
in leaf structure(anaverageof t 7% lessthanred
maple,the specieswith the thickestdimensions),
and the
overalllowerlevelof leaf responsiveness
to changein light
(anaverageof 23% lessthanredmaple,themostresponsive
species),make it the most susceptible
to desiccation
as
comparedto the other two maple species.Sugar maple
exhibitedchangesin cuticleandpalisademesophyllthicknesscomparableto red maplesuggesting
an ability to adapt
to varyinglightlevels.Ecologicalstudieshavedemonstrated
sugarmapletobethemostshadetolerantandin keepingwith
thisit hadthetallestheight,andgreatestrootcollardiameter
androot biomassof the threespeciesin the low light treatment.Red maplehadthe largestleaf structuredimensions
acrossalmostall lighttreatments,
andalsogreatestallocation
to root biomassunderdeepshadeas comparedto the other
maples, supportingits known toleranceto varying light
conditions
(opento deepshade)andwater-limitingenvironments.This studyshowsthat determinationof anatomical
and morphologicalcharacteristics
correlatewell with the
observedecologicaldistributionof thesespecies.Determining whereecologicalperformances
do not agreewith leaf
structuralandfunctionalattributespermitsexplorationof the
effectsof competition
onlandscape
patternsof distribution
of
thesespecies.
1977, Hibbs 1983).
Literature
Sipe and Bazzaz (1995) reportedsugarmapleto be the
leastresponsive
todifferences
inmicroenvironment.
Ellsworth
andReich(1992) suggestsugarmapleto be water-useeffiCientandconservative
in growthallocation.Our studyis
consistentwith their findings,but also demonstrates
that
sugarmaplehasthe leastoverallresponsiveness
in wholeplantsize(22-63% lessin height,rootcollardiameteranddry
mass)to differentlight treatmentsof the maplesthat we
examined.However,anatomicalmeasures(palisademesophyllthickness,
cuticlethickness)
of sugarmaplein ourstudy
demonstratedthat, at the leaf level, it was responsiveto
differences
in light.Similarly,Canham(1985, 1988)showed
that,thoughsugarmapleis shadetolerantandcanestablish
in forestunderstoryconditions,it growsbestunderhigher
lightregimesof canopyedgesandopenings.Canham(1988)
categorizedsugarmaple as a small gap specialistusing
Denslow's(1980) terminology.
Therearelimitationsto usingshort-termgreenhouse
experiments(wherecompetitionhasbeenexcluded)for comparinggrowthof plantsin differinglight environments,
and
then usingtheseresultsto relateto their knownecological
affinitiesof siteandshade-tolerance
in thewild.Forexample,
whengrownunderfield conditions,shadeintolerantspecies
die in low light regimes,and shadetolerantspecieswill
survive,making measuresof plasticityand performance
differentfrom thosegrownin the greenhouse
(Pacalaet al.
1994, Kobeet al. 1995).Furtherstudiesarethereforeneeded
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