A Comparison of Leaf Physiology and Anatomy of Quercus (Section Erythrobalanus-Fagaceae)
Species in Different Light Environments
Author(s): P. M. S. Ashton and G. P. Berlyn
Reviewed work(s):
Source: American Journal of Botany, Vol. 81, No. 5 (May, 1994), pp. 589-597
Published by: Botanical Society of America
Stable URL: http://www.jstor.org/stable/2445734 .
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American Journalof Botany 8 1(5): 589-597. 1994.
A COMPARISON
Q UERCUS
SPECIES
OF LEAF PHYSIOLOGY
(SECTION
AND ANATOMY OF
ER YTHROBALANUS- FAGACEAE)
IN DIFFERENT
LIGHT ENVIRONMENTS'
P. M. S. ASHTON2 AND G. P. BERLYN
School of Forestryand EnvironmentalStudies,Yale University,New Haven, Connecticut06511
Physiologicaland anatomical attribut-es
of leaves were examined of threespecies of QuercussectionErythrobalanus.All
threespecies occur in moist temperatedeciduous forestsof easternNorth America. Seedlingsof each species were grown
in different
lightconditionsforcomparison.The attributesmeasuredwere net photosynthesis,
stomatalconductivity,blade
and cuticle thickness,stomatal density,thicknessof upper and lower epidermis,and thicknessof palisade mesophyll.The
resultsgenerallydemonstratethe close association betweenanatomical adaptationsand efficiency
of physiologicalprocesses;
they also elucidate the distributionpatternsof the three Quercus species across the foresttopographyin southernNew
England. The most drought-tolerant
and light-demanding
species, Q. velutina(Lam.), exhibitedthe greatestleaf anatomical
plasticity,the highestnet photosynthesisin the different
lightconditions,and the lowest stomatalarea per unit area of leaf.
The mostdrought-intolerant
species,Q. rubra(L.), exhibitedtheleastleafanatomical plasticity,thelowestnetphotosynthesis
in the different
lightconditions,and the higheststomatal area per unit area of leaf. Quercus coccinea (Muenchh.) usually
exhibitedvalues thatwere intermediatebetweenQ. rubraand Q. velutina.
Physiologicalprocesses and anatomical adaptations of
leaves differdramaticallybetween tree species. Physiological differencesin rates of photosynthesis,transpiration,and stomatalconductivityof treespecies have been
relatedto theirsuccessional status,theirage (juvenile vs.
mature),and theircrownposition in the canopy (Boardmann, 1977; Hinckley et al., 1978; Lichtenthaleret al.,
1981; Fetcher,Strain,and Oberbauer, 1983; Bahari, Pallardy, and Parker, 1985; Abrams and Knapp, 1986;
Abrams, 1988; Strauss-Debenedettiand Bazzaz, 1991).
in stomataldensity,leafthickness,
Anatomicaldifferences
epidermal thickness,and palisade mesophyll thickness
have been similarlydescribed(Wylie, 1951, 1954; Jackson, 1967a, b; Carpenterand Smith,1975; Givnish, 1988;
Lee et al., 1990).
Selectingseedlingsof closely relatedspecies thatoccur
withinthe same forestfacilitatescomparison of physiological and anatomical characteristics
(Jurik,Chabot, and
Chabot, 1982). Some comparativestudiesof seedlingsin
thetropicalevergreenforesthave demonstrated
thatclosely
relatedspecies thatoccur withinthe same foresttype,but
that differin successional status and crown stratumof
occupation, have physiologicalprocesses that appear to
be unrelated to their anatomical adaptations (StraussDebenedetti, 1989). Other tropical studies of seedlings
withinevergreenforesthave examinedcloselyrelatedspecies that occur withinthe same foresttype but that are
ofthesame successionalstatusand crownstratum.Under
these circumstancesresultsdemonstratethe close association between anatomical adaptation and efficiency
in
physiological process of seedlings (Ashton and Berlyn,
1992). Also, fewstudieshave examined fordifferences
in
seedling physiologyand anatomy under differentlight
' Manuscript received 4 February 1993; revision accepted 18 November 1993.
The authorsthankDavid Smith,Bruce Larson, Patricia Tomlinson,
and JuddIsebrandsforhelpfulcomments.This studywas made possible
by supportfromthe Yale UniversityForests.
2
Authorforcorrespondence.
qualities (Taylor and Davies, 1988; Lee et al., 1990; Ashton and Berlyn,1992).
The objectiveof thisstudywas to observeand measure
the physiologicalprocesses and anatomical adaptations
of seedlings belongingto closely related species of the
genus Quercus sectionErythrobalanus(Fagaceae) within
a moist temperatedeciduous forestof southernNew England, USA. Seedlings of three species (Q. coccinea
[Muenchh.], Q. rubra [L.], Q. velutina[Lam.]) were examined underdifferent
lightquantitiesand qualities. The
studyspecies are mid- to late successionaltreesthatdominate thecanopy stratumof mixed-speciesforestsof easternNorthAmerica. In southernNew Englandeach ofthe
threespecies occupy a different
part of the foresttopography.The lower slopes and swales have Q. rubra.These
sites have deep soils and are mesic year-round.Quercus
velutinaoccurson bedrockridgeswithshallowsoils. Quercus coccinea has a puzzling patternof occurrence,but
predominateson drysitesthathave deep but coarse soils.
All species have wide overlapping ranges and can frequently,althoughnot predominantly,occuron any ofthe
aforementionedsites (Burns and Honkala, 1991).
The studytestedthehypothesisthatthesespecies,which
are consideredofthesame successionalstatus(sensuWatt,
1947) and occupy similar crown strata withina forest,
have distinctrates of photosynthesisand stomatal conductivityand thatthisreflectstheanatomical adaptations
of theirleaves. The patternof relationshipsbetweenleaf
anatomyand physiologymay explainwhysimilarspecies
may occur togetherbut occupydifferent
ecological niches
withina forest(Bourdeau, 1954; Abrams, 1990).
MATERIALS AND METHODS
Design of theenvironment
shelters-Environmentshelters were constructedto investigateseedling leaf physiologyand anatomyundersimulatedforestlightenvironmentsthatcontrolledthe quality(changesin R:FR ratio)
and quantityoflight.These shelterswereplaced outdoors
in a largeopen area at the fieldstationof the Yale-Myers
589
590
[Vol. 81
AMERICAN JOURNAL OF BOTANY
photon flux(PPF) and temperaturemeasurementsforthe lighttreatmentsof the shelters.Data are means
Summaryof photosynthetic
fromfoursunnydays in Juneand July.Values are means withtheirstandarderrorsin parentheses.M = morning(0600); N = noon (1200);
TABLE 1.
E = evening (1800).
Lighttreatments
(umols m 2 sec ')
PPF mols m-2 day-'
50
350
800
1,600
2.25 (0.13)
11.70 (0.51)
23.82 (1.20)
41.93 (3.61)
Soil temperature
(@20 cm below soil surface)
M
N
E
13.03 (0.18)
17.10 (0.78)
17.73 (0.72)
13.37 (0.19)
17.67 (0.17)
19.13 (0.20)
14.77 (0.35)
19.63 (1.48)
20.30 (1.25)
16.53 (1.39)
20.20 (0.12)
21.70 (1.11)
Surfacesoil temperature
M
N
E
14.50 (0.10)
24.40 (0.90)
19.63 (0.55)
14.97 (0.12)
25.03 (0.26)
21.20 (0.12)
17.77 (0.48)
27.33 (1.63)
23.57 (1.15)
25.93 (0.84)
39.43 (2.69)
24.80 (0.90)
Air temperature
M
N
E
18.10 (0.21)
23.77 (0.13)
19.70 (0.06)
18.03 (0.23)
24.67 (0.12)
20.97 (0.09)
19.97 (0.07)
25.30 (0.15)
21.10 (0.12)
22.43 (0.15)
28.27 (0.19)
20.20 (0.42)
Research and DemonstrationForest(4 15 7'N; 72?07'W).
Environmentshelterswereconstructedin the same manner as Ashton and Berlyn(1992).
Four shelterswere constructedto examine effectsof
different
quantitiesof lightquality similarto that found
in the forestunderstory.Light quality was altered by
sprayinga particularratioofpaintpigmentsthathad been
mixed in a varnishbase onto clearplasticfilm(Lee, 1985).
The pigmentswereselectedto simulatetheeffectofupper
canopy foliage on interceptionand transmissionof full
lightwithappropriatered
sunlight,providingtransmitted
to farredratios(as definedbySmith,1982). Lightintensity
was alteredby theamountofpigmentsprayedon thefilm.
Samples of the lightqualityand quantityfilmtreatments
were firstdone in consultationwithD. W. Lee (personal
communication, Florida InternationalUniversity,Mi(Li Cor
ami, FL) and werevalidatedby spectroradiometer
1800, Lincoln, NE). One shelterprovided seedlingswith
understorylightquality(R:FR ratioof 0.46) witha maxflux(PPF) of 50 ,umolm-2
imum photon photosynthetic
sec-1. The second shelterprovided a lightquality R:FR
ratio of 0.97 with a maximum PPF of 350 ,umolm-2
sec-1. The third shelterprovided a lightquality R:FR
ratio of 1.15 with maximum PPF 800 ,umolm-2 sec-1.
There was also a fourthcontrol sheltercovered with a
clear filmthatprovided fullsunlightquality (R:FR ratio
1.27) witha maximumquantityof 1,600 ,umolm-2 sec- 1.
Each species had 100 seedlingsassignedto fourblocks
withina singleshelter.Each block thereforecontained25
seedlingsper species. Blocks foreach species minimized
interspeciesshading that would occur due to different
growthrates. To make sure the blocks of seedlings for
each species were representedacross the whole shelter
environment,theposition of each block fora species was
randomlyselectedfromfourrows.These rowswerealigned
north-southadjacent to each otherand representeda part
of the shelterenvironment.The limitationsimposed by
thispseudo-replicationdesign(sensu Hurlbert,1984) were
reduced by the large number of seedlingsused foreach
species and by the rotationof the blocks among the rows
withineach shelterover the course of the lighttreatment.
Seed of each species was collected in equal amounts
fromfourwidely dispersed (> 1 mile) parenttree populations located withinthe Yale-Myers Forest area. This
seed was collected in September 1988. Aftercollection,
viable seed was mixed togetherforeach species and cold
stratifiedin moist sand at 1-4 C fora 5-monthperiod.
In March of the followingyearthe acorns of each species
were individuallyplanted in plastic bags filledwith soil.
The plasticbags were30 cm in depthand contained2,355
cm3 of packed foresttop soil obtained fromone valley
location within the forest.Bags were placed in regular
lines withinthe sheltersat a 10 x 10-cmspacingbetween
bag centers.
Wateringwas regulatedto maintain soils at fieldcapacity.To provide forregulationof the wateringregime
gypsumblockswereburiedin seedlingsoil bags randomly
distributedthroughouteach environmentshelter.Over
the course of the investigation,blocks were monitored
daily forrelativemoisturecontentusing a battery-operated soil moisturemeter(Bouyoucos, 1954, 1972). Relative moisturecontentswere successfullymaintainedin
all shelters,by applying1 liter/M2
of waterover the seedlings every Monday, Wednesday, and Friday. A black
plasticliningwas used beneaththeseedlingbagsto prevent
theircontact with the ground. Any water that collected
on this floorwas allowed to drain away throughsmall
holes in the plastic.
Soil temperature,soil surfacetemperature,air temperature 30 cm above the ground,and PPF were monitored
foreach shelteron sunnydays duringthe late springand
summergrowingseason of 1989. Temperaturemeasurementsof theair and at 0 and 20 cm soil depthweremade
with a portable battery-operatedthermocouplepotentiometer (Cole Palmer Inc., Model J, Chicago, IL) with
detachable probes. Soil measurementswere made by
plunginga single thermocoupleinto threerandomlyselected seedlingbags foreach shelter.Measurementswere
recordedat threesamplingtimes(600, 1,200, 1,800) distributedover a 12-hourperiodduringthecourseofa day.
Light sensors(Li Cor 190SA and 190 SZ) were set up to
takereadingsofPPF every10 seconds.Ten-minutemeans
foreach shelterwere simultaneouslyrecordedover a 14hour period using a data logger(Li Cor 1000). Sensors
were positioned horizontally30 cm above the ground
within each shelter.Measurements of temperatureand
PPF were made on the same days forall sheltersand are
summarizedin Table 1. Diurnal temperaturefluctuations
May
1994]
ASHTON AND BERLYN-LEAF
PHYSIOLOGY AND ANATOMY OF QUERCUS
of the soil were the most moderatedcompared to surface
and air temperatures.The highesttemperaturesrecorded
were forsurfacetemperaturesat midday. Highersoil and
air temperatureswere associated with sheltersreceiving
greaterPPF.
Physiologyexperiments-Gas exchangewas measured
duringJuly 1989. Measurementsdeterminedthe rate of
net CO2 assimilation (net photosynthesis,PN) and stomatal conductivity(g) of seedlingleafsamples underconditions that approximated the environmentsin the appropriateshelters.Seedlingsofeach specieswererandomly
selectedfromeach ofthefourshelters,and weremeasured
with a closed-systemLi Cor 6200 infraredgas analyzer
(Welles, 1986) with a 1-literleaf chamber. The system
was assembled in a well-ventilatedroom that attaineda
measured atmosphericCO2 level of 350 Al liter-1. The
apparatus was periodicallychecked throughoutthe day,
and calibrated according to Welles (1986) in the early
morning,and in the afternoonbeforethe startof measurements.Measurementswere made on singleattached
leaves of seedlingsthat were well watered.To minimize
ontogeneticdifferences
(Hanson et al., 1988), leaves were
all selected fromthe firstflushof seedlingsof the same
age. Only undamaged leaves with no sign of scarring,
disease, or herbivorywere selected.
A lightsource(Sylvaniametalarclamp,1000 BU-HOR)
was used to obtain an illuminationsimilarto the amount
and qualityprovided by fullsun (1,600,umol m-2 sec-'),
with a projected area that allowed all selected seedlings
fora lighttreatmentto be positionedbeneath.To emulate
the lightenvironmentof the shelters,plastic filmswith
the correspondingamounts of paint-spraypigmentwere
placed immediatelybeneath the lightsource and above
the seedlings.The lightintensitywas more finelyadjusted
by moving the metalarclamp up or down and checking
intensitybeneathwitha quantum sensor(Li Cor 190SA)
that was placed at the level of the seedling leaf canopy.
The heat generatedby the lightsource was impeded by
a glass plate thathad been positionedimmediatelybelow
the light source. The heat was removed by a series of
extractorfans. The heightof the lightsource varied between 1 and 1.5 m above the seedlingcanopy.
Measurementsweremade on leaves ofat leasttenseedlingsover fourpseudo-replicatesof each species foreach
of the four light treatments.For each light treatment,
measurementswere taken on only those seedlings that
had grownunder that same lighttreatmentin the environmentshelters.To make a measurement,the chamber
of the photosynthesissystemwas kept open over the selected leaf until chamber CO2 equaled atmosphericCO2
(350 Al liter-1). It was then sealed, and measurements
startedaftera steady CO2 decline was observed on the
monitorscreen.Chamber temperatureswere maintained
at approximately24-27 C, and relativehumiditywas kept
between 50% and 70% duringmeasurements.Each measurementof a leaf consisted of a set of threesequential
readings.
To avoid bias fromdiurnaleffects,
samplingforall light
treatmentscommenced at 8:00 a.m. and lasted until6:00
p.m. Each species was sequentiallymeasuredat least five
times over the course of thistime period. Differentseed-
591
lingsforthesemeasurementswererandomlychosenwithin each species. During the period of the experiment,
seedlingsand theirappropriatelighttreatmentwere run
separatelyon 8 consecutive days, each treatmentbeing
repeatedonce.
Anatomy experiments-Leaves from seedlings were
taken fromtwo sheltersand examined to identifyanatomical traitsthatmightrelateto the physiologyof each
species. Measurementswere designed to investigatestomatal frequency,size, and distribution;dimensions of
upper and lower epidermis,and of palisade mesophyll;
and cuticle and leaf thickness.Sample leaves were taken
fromseedlingsof each species growingin the sheltersthat
simulated full-sun(sun leaves) and understorylight(50
umol m-2 sec-') (shade leaves). Only fullyexpanded,
undamaged leaves with no signs of scarring,disease, or
herbivorywere chosen foreach stomateexamination or
sectioning.The leaves were ca. 2 months old and were
randomlyselectedfromthose belongingto the firstflush
of a seedling.
To examine stomatedensity,size, and distribution,
leaf
peels were taken using a razor to skim the surfaceof the
upper and lower epidermis. Each peel was placed on a
slide and immersedin a drop of waterunderneatha coverslipand observedat x 200. The numberof stomatawas
counted on both the upper and lower epidermis,and the
lengthsof ten stomata were taken using a x 10 filarmicrometereye-piecefora measure of size. Each peel was
taken froma separate leaf and each leaf froma separate
seedling.Five leaf peels each were used foreach species
and lighttreatment,
and foreach surface(upperand lower
fieldsofview were
epidermis).For each peel fivedifferent
counted and lumped togetheras pseudoreplicates.
To examine and measure the dimensionsand number
of layers of epidermis and mesophyll,and to gauge the
cuticle and leaf thickness,leaf cross-sectionswere prepared formicroscopicexamination.Three 0.5 x 1.0-cm
stripswere taken fromthe middle portionof the lamina
across the midrib,each froma different
seedling.Strips
were immediatelyfixed in cold FAA (formalin:acetic
acid: alcohol, formulaofBerlynand Miksche, 1976). The
materialwas thendehydratedthrougha xyleneseriesand
embedded in wax. Cross sectionswere cut at 12 ,umwith
a rotarymicrotome.The tissuewas stainedwithsafranin
and fastgreenfollowinga modifiedprocedureof Berlyn
and Miksche (1976).
Slides were examined foreach species and lighttreatment,with each slide representinga different
leaf strip.
For each slide, five measurementswere made of length
and breadthofupperand lowerepidermis,and ofpalisade
mesophyll.Cuticle and leaf thicknesswere measured on
different
sectionsoftheslide,and in different
places within
each section,avoidingtheregionaroundthemidrib.Measurementsweremade witha lightmicroscopeusinga x 10
filarmicrometereye-pieceand suitableobjectives forthe
resolutionrequired.Measures of the leaf thicknesswere
made at x 400; cell dimensionswere done at x 630; and
cuticle thickness,at x 1,000.
Statistics-Analysis ofvariancewas performedon each
physiologicalmeasure (PN; g) using the ANOVA procedure oftheStatisticalAnalysisSystem(SAS) (Ray, 1982).
592
AMERICAN JOURNAL OF BOTANY
[Vol. 81
2. Summaryof physiologicalvariables (untransformed)
forthreespecies of Quercusain each of the lighttreatments.Values are means of
102 measurementstaken fromten different
leaves withtheirstandarderrorsin brackets.
TABLE
Lighttreatment(,umolsm
50
2
sec ')
350
800
1,600
Net photosynthesis(PN) (,umols m-2 sec-')
4.67 (0.09)a
5.27 (0.1 I)a
3.66 (0.09)b
3.66 (0.09)b
4.63 (0.08)a
5.02 (0.48)a
Quercus coccinea
Quercus rubra
Quercus velutina
1.56 (0.04)a
1.53 (0.03)a
1.45 (0.04)a
Quercus coccinea
Quercus rubra
Quercus velutina
0.061 (0.005)a
0.054 (0.006)a
0.069 (0.006)a
Stomatal conductivity(g) (umol cm-2 sec-')
0.089 (0.004)b
0.093 (0.005)a
0.075 (0.005)b
0.062 (0.004)b
0.120 (0.007)a
0.099 (0.006)a
P
4.57 (0.19)b
3.11 (0.13)c
5.65 (0.24)a
2.93
2.03
3.89
0.116 (0.007)b
0.079 (0.004)c
0.183 (0.009)a
1.90
1.46
2.65
a Lowercase lettersdenote differences
in log transformeddata at the 5% level of significanceamong species withina lighttreatment.Species
followedby the same lowercaseletterwithina treatmentare not significantly
Values are also given forphysiologicalplasticityP (sun' 600/
different.
shade50).
All data were log transformedpriorto analysis.Analyses
tested for differencesamong species, among lighttreatments,and forinteractionsamong species and lighttreatment. All F statisticswere significant(P < 0.001), and
differences
among species wereevaluated at the
therefore
5% significancelevel using Tukey's StudentizedRange.
Data forthe anatomical attributeswere also analyzed
by the ANOVA procedureof SAS (Ray, 1982). Analyses
tested fordifferencesamong species, among lighttreatments,and forinteractionsamong species and lighttreatment.Tukey's StudentizedRange was used to determine
differences
among the treatmentsand species at the 5%
significancelevel. Where appropriate,correlationswere
obtainedbetweenanatomicaland physiologicalattributes
usingthe regressionprocedureof SAS (Ray, 1982). Physiological attributeswere analyzed using log-transformed
data.
RESULTS
Physiology- Resultsshowedstatistically
significant
differencesin rateof netphotosynthesis(PN) per unitof leaf
area between species and lighttreatment(Table 2; Fig.
1). At low values of PPF (50 ,umolm-2 sec-1), Q. rubra,
Q. coccinea, and Q. velutinahad similarvalues of PN. At
PPF amounts of 350 to 800 umol m-2 sec-', Q. velutina
C,,
o
4
E
~
cn
~
~ ~
~
~
~
~
~
~
~
~~~
.rubra
LU Q. coccinea
Q. velutina
5
cn>~2
0
0)
0
50
3 50
PPF
8 00
1 60 0
(ptmol m-2 s-1)
lighttreatments.
Fig. 1. Mean net photosynthesisrates(PN) of the threeQuercus species forthe different
LEAF THICKNESS
3. Summaryof leafanatomical variables forthe threeQuercusa
species for full sun (sun leaves; 1,600 Amols m-2 sec-') and understoryshade (shade leaves; 50 Amolsmr-2 sec- '). Values are given
foranatomical plasticityP (sun/shade).Data are means fromfour
differentleaves. Values are means with their standard errorsin
parentheses.
200 -
TABLE
E
10Quercus
150
E
Quercuscoccinea
rubra
Quercusvelutina
Treatments
Shade
Species
Sun
P
Quercuscoccinea
Quercusrubra
Quercusvelutina
Blade thickness(,um)
132.659 (2.39)a
84.079 (2.20)b
125.289 (5.54)a
90.152 (1.08)b
134.659 (9.26)a
93.952 (1.05)b
1.58
1.39
1.43
Quercuscoccinea
Quercusrubra
Quercusvelutina
Cuticle thickness(,um)
1.120 (0.05)d
3.051 (0.15)b
3.174 (0. I O)b
1.62 1 (0.13)cd
3.860 (0.23)a
1.766 (0.08)c
2.72
1.96
2.18
Quercuscoccinea
Quercusrubra
Quercusvelutina
Stomatal length(rAm)
8.65 (0.57)b
8.69 (0.41)b
17.39 (0.97)a
17.40 (1.23)a
17.90 (1.50)a
17.88 (l.l1 )a
1.03
1.00
0.98
Quercuscoccinea
Quercusrubra
Quercusvelutina
Quercuscoccinea
Quercusrubra
Quercusvelutina
Stomatal density(no./mm2)
1,032 (20)a
765 (40)b
695 (16)c
583 (19)d
293 (7)e
196 (8)f
Stomate Area Index (SAI)
8,978
6,655
12,093
10,144
5,244
3,508
LL
50_
w
SUN
CUTICLE
SHADE
1.35
1.19
1.49
Lower epidermal cell thickness(,um)
7.123 (0.25)c
9.051 (0.23)a
9.927 (0.17)a
9.368 (0.33)a
8.793 (0.19)b
8.937 (0.23)ab
1.27
0.98
1.02
Upper epidermal cell thickness(,Am)
18.930 (1.62)bc
13.540 (0.64)d
Quercuscoccinea
20.644 (l.19)b
26.304 (0.87)a
Quercusrubra
27.019 (0.83)a
17.720 (0.66)c
Quercusvelutina
1.37
1.27
1.52
Palisade cell thickness(,um)
43.862 (1.34)a
19.659 (2.47)d
20.414 (0.62)d
40.184 (1.32)a
29.187 (1.53)b
24.404 (0.22)c
100
1.35
1.19
1.49
Quercuscoccinea
Quercusrubra
Quercusvelutina
Quercuscoccinea
Quercusrubra
Quercusvelutina
w
2.23
1.97
1.19
among treatLowercase lettersbeside the means denote difference
mentsand species at the 5% level. Species withtreatmentsfollowedby
different.
The Stomate
the same lowercase letterare not significantly
and
Area Index (SAI) is the productof the mean stomate length(plem)
stomatal density.
a
and Q. coccineahad higherPN than Q. rubra.At amounts
of PPF equal to that of fullsun (1,600 ,umol m-2 sec-1)
Q. velutinahad higherPN than Q. coccinea,whichin turn
had greaterPN than Q. rubra.
Results show thateach ofthethreeQuercusspecies had
PPF spectralqualities and
optimum PN ratesat different
intensities.The highestPN ratesforQ. rubrawereachieved
at PPF beteen 350 Amol m-2 sec-t and 800 Amol m-2
sec- 1.For Q. coccinea,highestPN was at PPF of 800 ,umol
m-2 sec-', and forQ. velutinaPN was highestat PPF of
1,600,mol m-2 sec-'.
Fig. 2. Blade thickness(top),cuticlethickness(middle),and stomatal
density(bottom) forsun and shade leaves of Quercusspecies.
w
-J-
0
0
_
800
s,S
SUN
SHADE
STOMATAL DENSITY
'4 1200
E
E
60-
w
C,)
I-
^
0
03i
1200
Z
sst
rSUN
SHAD
594
AMERICAN JOURNAL OF BOTANY
[Vol. 81
2OjJm~~~~~~~~~S
May
1994]
ASHTON AND BERLYN-LEAF
PHYSIOLOGY AND ANATOMY OF QUERCUS
595
Trendswereshownforstomatalconductivity(g) among
species and across lighttreatmentsas those describedfor
PN (Table 2), but therewere some noticeable differences.
All species increasedg with increasingam'ountsof PPF.
Highestratesofg werethereforeassociated withamounts
of PPF thatwere equivalent to fullsun (1,600 umolm-2
werealso shownamong spedifferences
sec- 1).Significant
cies withina lighttreatment.In all lighttreatmentsQ.
velutinahad higherrates of g than Q. coccinea, which in
turnhad higherratesof g than Q. rubra.Differencesin g
among species were more accentuatedwith higherPPF.
was exGreatestphysiologicalplasticity(sunl"600/shade50)
hibitedby Q. velutina,followedin orderby Q. coccinea,
and then by Q. rubra(Table 2).
Species and lighttreatmentscaused significantdifferences in lowerand upperepidermalcell thicknesses;these
were more marked for upper epidermis than for lower
epidermis. Thicknesses of upper epidermal cells for all
greaterforsun leaves than for
species were significantly
shade. For thelowerepidermalcells onlyQ. coccinea was
thickerforsun leaves in comparisonto shade
significantly
leaves. In most all cases species had upperepidermalcell
dimensions that were twice that of the lower epidermal
cells. Quercusvelutinaand Q. rubrahad thickerepidermal
cells thanQ. coccinea,exceptforthelowerepidermalcells
of sun leaves. No correlationwas found between leaf
epidermalcell dimensionsand physiologicalmeasuresfor
any species or lighttreatment.
longerforsunleaves
Palisade celllengthsare significantly
thickerleaf than shade leaves for all species. Quercus coccinea and
Anatomy-All speciesproducedsignificantly
Q. rubra had longer palisade cells than Q. velutinafor
blades whengrownin fullsunas comparedto shade (Table
3; Figs. 2, 3). No significantdifferencesin thicknessof leaves grownin the sun, but this was reversedforleaves
leaf blades were found among species for a given light grown in the shade. Palisade cell lengthswere not well
correlatedwith other anatomical or physiologicalattritreatment,and this thicknesswas not correlatedwithPN
or g. However, a correlationwas foundbetweenrelative butes.
Anatomicalmeasuresofplasticity(P), exhibitedbysun/
wateruse (PN/g)and blade thickness(R2 = 0.60*) (* hereshade ratio (Table 3), in some cases showed close corafterdenotes significanceat 0.05 level).
There were significantdifferencesin cuticle thickness relationswith physiologicalmeasures of plasticity(P =
(Table 2). Stomataldensityplasticitywas
sun"600/shade50)
among species and betweenleaves grownin fullsun and
correlatedwith PN plasticity(R2 = 0.99*), and with g
those grownin shade (Table 3; Fig. 2). Cuticles of both
shade and sun leaves of Q. velutinawere significantly plasticity(R2 = 0.96*). Upper epidermal cell thickness
thickerthan those of Q. coccinea, and the sun leaves of was correlatedwith g (R2 = 0.99*), and with PN (R2 =
0.99*). Greatestplasticityof upper epidermal cell thickQ. rubra. In all species cuticle thicknessesof sun leaves
thickerthan those leaves grownin the ness, stomataldensity,and thephysiologicalmeasures(g,
were significantly
shade. AlthoughQ. velutina,the species withthe greatest PN) was demonstratedby Q. velutina,and least was with
Q. rubra.Also, plasticityofSAI was greatestforQ. velutina
PN and g, had the thickestcuticlein comparisonwiththe
least forQ. rubra.However,forstomatelengthslittle
and
not
did
appear
and
g
with
PN
ranking
otherspecies, the
to hold whencomparingQ. coccinea withQ. rubra,where plasticitywas exhibitedbetweenshade and sun leaves of
each species. For blade and cuticlethicknesses,and lower
the relationshipwithcuticle thicknesswas reversed.
epidermalcell thickness,greatestplasticitybetweenshade
Stomata forseedlingsof Quercusspecies are located on
the lower leaf surfaceonly. There were significantdiffer- and sun leaves was exhibitedby Q. coccinea and least by
Q. rubra.
ences in the numberof stomatesper unitarea among the
species. Highestdensitieswere obtained forQ. coccinea,
followedin orderby Q. rubraand Q. velutina.All Quercus
DISCUSSION
highernumbersof stomatesper
species had significantly
Resultsclearlydemonstratecorrelationbetweencertain
unitarea in leaves thatwereexposed to fullsun,compared
to those exposed to shade. Stomatal densityand relative anatomical adaptations and physiological processes of
seedlings.Particularlyevidentis the relationof g and PN
water use (PN/g)among Quercus species were not well
withSAI. This index is the most representativemeasure
correlated.
The mean lengthsof the stomates were not different examined thatcan be associated withthesiteswhereeach
species predominates.The species with the highestSAI,
betweenshade and sun leaves withineach species. However, stomate lengthsof Q. coccinea were significantly Q. rubra,is associated withthe mesic sites of the valleys
smallerthanQ. rubraand Q. velutina.An indexofstomate and lower slopes. This species, compared withthe other
in fullsun (Seidel,
species, has a low wateruse efficiency
area per unit area of leaf foreach species (Table 3) was
calculated by taking the product of the mean stomate 1972; Abrams, 1990). The species with the lowest SAI,
lengthand thestomatedensityperunitarea. This Stomate Q. velutina,occupies ridgesthathave shallow soils. This
of wateruse in fullsun. SAI
species has a highefficiency
Area Index (SAI) is correlatedwiththephysiologicalmeasurements.Correlationsbetween SAI and PN among the may be a usefulmethod of approximatingstomate area
per unit area of leaf and could be used to predict the
Quercus species had an R2 = 0.98* forsun leaves. There
droughttolerance of species. In this studySAI suggests
was also a similarcorrelationamong species betweenSAI
Q. velutinato be the most droughttolerantand Q. rubra
and g (sun R2 = 0.99*; shade R2 = 0.99*), and SAI and
to
be the most droughtintolerant.
=
R2
0.97*).
=
R2
shade
0.80*;
(sun
PN/g
Fig. 3.
Photomicrographsof leaf sections forQ. coccinea-sun (A), shade (B); Q. rubra-sun (C), shade (D); Q. velutina-sun (E), shade (F).
596
AMERICANJOURNALOF BOTANY
The index also reflectslighttolerancewithQ. velutina,
the species havingthelowestSAI measurebeingthemost
lightdemanding,and Q. rubra,thespecieswiththehighest
SAI measure being the most shade tolerant.These interpretationsare reinforcedby certainmeasures of physiological (PN, g) and anatomical (stomatefrequency,upper
epidermal cell thickness)plasticity.The most droughttolerantspecies, Q. velutina,exhibitedthe highestlevel
of plasticity,and Q. rubra,the most drought-proneand
shade-tolerantspecies, showed the lowest plasticity.
No clear patterncould be found in the droughtand
lighttoleranceof the Quercus species that could be correlatedwiththeircuticle and leaf blade thickness.However, there do appear to be trends in plasticityamong
thesemeasures. Leaf blade and cuticlethicknessshow Q.
coccinea to have greatestplasticityand Q. rubrato have
the least. This flexibilityof attributeswould suggesta
greaterabilityto adapt to heterogeneousenvironments.
This mightsuggestwhy Q. coccinea can be foundon the
deep coarse soils thatare more droughtprone than those
soils usually occupied by Q. rubra.In the otherattributes
thatwere measured, Q. coccinea generallyexhibitedvalues thatwereintermediatebetweenthose of Q. rubraand
Q. velutinaand this is consistentwith its intermediate
status in droughttolerance.Therefore,Q. coccinea may
not be able to compete successfullywithQ. velutinawhen
growingon the most drought-prone,shallow soils. This
correspondsto its position withinthe foresttopography
in relationto its associates.
Althoughresultsclearly indicate why Q. rubra is restrictedto the more mesic sites,theydo not suggestwhy
Q. rubrais more common on these siteswhen compared
to Q. velutinaand Q. coccinea. However, althoughPN of
greaterthan
Q. coccinea and Q. velutinaare significantly
Q. rubra under ever-moistconditions, we suggestthat
theirratesofrespirationare also higher.This would mean
greateramounts of carbohydratecan be stored or used
forgrowthratherthanmaintenanceand repairin Q. rubra
compared with the otherQuercus spp.
Differencesin cuticleand leafblade thickness,and epidermal and palisade cell thicknessamong shade and sun
leaves of Quercus produced similar resultsto those reportedin many otherstudiesforothertemperatespecies
(Wylie, 1951, 1954; Jackson 1967a, b; Carpenter and
Smith,1975; Taylorand Davies, 1988). Shade leaves have
significantlythinnerdimensions than sun leaves. The
thickeranatomical dimensionspromotehigherefficiency
in wateruse and lowerevapotranspirationdemandsunder
high radiation.
Results supportfindingsfromanother studydone on
an assemblage of species thatoccur,and occupythesame
canopy stratumofthematurephase ofstanddevelopment
(Ashton and Berlyn, 1992). In that studywe examined
seedlings of four species of Shorea section Doona from
SriLanka. These
forestin southwestern
mixed-dipterocarp
species had closer and greaternumbers of correlations
betweenmeasured anatomical and physiologicalparametersthan the Quercus species in this study.This might
in degreeofhabitatspecialization
be relatedto differences
among species of Shorea section Doona as compared to
QuercussectionErythrobalanus.Based on thehypothesis
of Grubb (1977) concerningthe partitioningof the regenerationniche, we speculate that closer and greater
[Vol. 81
numbers of correlationswould be found between anatomicaland physiologicalmeasuresofrelatedspecies that
grow in environmentsthat provide a more predictable,
and more distinctvarietyof habitats. Our findingsfor
this study thereforesuggestthat the greateroverlap of
anatomical and physiologicalattributesforQuercusspp.,
as compared to Shorea spp., ensure theirsurvival in the
more unpredictableforestenvironmentof southernNew
England. It should be recognizedthatthese studies have
examined patternsin seedling anatomy and physiology
and did not investigatechanges in ontogenywith age.
Findingsformaturetreesmightbe verydifferent.
Furtherstudiesare investigatingtheserelationshipson
other generic assemblages. Patterns among individual
species that belong to a closely related assemblage, and
patternsamong the assemblages themselves,may prove
usefulto understandingspecies habitat specialization in
different
environments.With this knowledgeit may be
possible to use species assemblages as indicatorsof ecosystemadaptibilityand resilienceto change.
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