Leaf variations in Elaeagnus angustifolia related to ...directory.umm.ac.id/Data Elmu/jurnal/E... · Environmental and Experimental Botany 44 (2000) 171–183 Leaf variations in Elaeagnus

Environmental and Experimental Botany 44 (2000) 171–183

Leaf variations in Elaeagnus angustifolia related toenvironmental heterogeneity

Marıa Guadalupe Klich *Departamento de Agronomıa, Centro de Recursos Naturales Reno6ables de la Zona Semiarida (CERZOS),

Uni6ersidad Nacional del Sur, C.C. 738, 8000-Bahıa Blanca, Argentina

Received 3 August 1999; received in revised form 6 April 2000; accepted 10 April 2000

Abstract

Elaeagnus angustifolia (Russian olive) is a Eurasian tree that has become naturalized and has invaded zones alongwatercourses in many arid and semiarid regions of the world. These habitats are characterized by verticalenvironmental gradients, thus trees must develop some plasticity to adapt to the wide range of site conditions. Thisstudy was undertaken to test the hypothesis that variations in leaf anatomy and morphology of E. angustifolia reflecttheir adaptability to the differences in the microclimate that occur within the canopy of single trees. Foliararchitecture, blade and petiole epidermal and internal anatomy were examined in leaves at different canopy positionsand related to environmental conditions. Upper sun-leaves are exposed to higher solar irradiance and lower airhumidity and are smaller, more slender and thicker than the lower, half-exposed and shade-leaves. Color variesbetween the leaves at different levels, from silvery grey-green in the upper strata, to dark green in the lower one.Bicolor is more evident in half-exposed and shaded leaves. When compared with the lower half-exposed andshade-leaves, the upper leaves of E. angustifolia have a greater areole density, a higher mesophyll proportion andstomatal density. Trichomes are multicellular, pedestalled, stellate-branched or peltate and their form and density canbe associated with leaf color and appearance. The slender petioles of the upper leaves have proportionally moreepidermis, collenchyma and phloem and less parenchyma and xylem than those of lower leaves, when observed intransverse sections. Foliar morphological and anatomical variability in E. angustifolia may be considered an adaptiveadvantage that enables leaves to develop and function in habitats marked by strong variations of solar radiation, airtemperature and humidity. © 2000 Elsevier Science B.V. All rights reserved.

Keywords: Leaf heterogeneity; Leaf architecture; Phenotypic plasticity; Water stress; Xeromorphy; Canopy microclimate

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1. Introduction

Developmental responses to small-scale envi-ronmental heterogeneity can be important for

plant adaptation (Novoplansky, 1996). Leaves arethe plant organs most exposed to aerial conditionsand the changes in their characters have beeninterpreted as adaptations to specific environ-ments (Fahn and Cutler, 1992). Variations in themorphological and anatomical features of leavesdeveloped at different levels in the plants have

* Corresponding author. Fax: +54-291-4541224.E-mail address: [email protected] (M.G. Klich).

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M.G. Klich / En6ironmental and Experimental Botany 44 (2000) 171–183172

been reported for many species and related espe-cially to the amount of sun exposure or wateravailability. (Kaufmann and Troendle, 1981;Niinemets and Kull, 1994; Smith et al., 1997).

Elaeagnus angustifolia L. (Russian olive) is aEurasian tree that has become naturalized, form-ing monotypic stands along the watercourses inthe Rıo Negro valleys of Argentina. This speciesis known for its capacity to grow over a widerange of environmental conditions. For example,seedlings are tolerant of shade and mature treescan live exposed to high light intensities(Shafroth et al., 1995; Lucchesini and Mensuali-Sodi, 1996). E. angustifolia can displace nativewoody species and has been so successful incolonising disturbed areas and old fields, that itsuse is prohibited in some areas (Dawson, 1990).The ability of E. angustifolia to establish, growand invade new areas has led to investigations ofthe conditions that might favor its spread(Shafroth et al., 1995).

Visiting the invaded zone, I noticed that withinclustered individuals of E. angustifolia there werevariations in form and color between leavesgrowing at different levels in a tree. I evaluatedthe environmental heterogeneity within thecanopy of trees growing along the Rio Negrowatercourse in this dry-region. Anatomical andmorphological studies were performed in orderto prove if the externally observed leaf differ-ences were correlated with internal adaptations. Itested the hypothesis that variations in develop-mental responses of the E. angustifolia leaves tospatial heterogeneity are related to the ecologicalstrategies of this invasive species.

2. Material and methods

The study was conducted during three growthperiods (1995–1998), using leaf samples origi-nated from a stand of E. angustifolia growing atthe margin of the Rıo Negro, Argentina (39°30%S, 65°30% W) in an area where the expansion ofthis species has been notable in the last 20 years.The climate is temperate semiarid to cold arid.The average temperature during the coldestmonth (July) is 6.83°C and during the hottest

month (January) is 23.02°C. The average annualprecipitation is 300 mm, most falling during thespring and autumn. Average relative air humidityranges from 48% (January) to 70% (June). Theaverage annual evapotranspiration is \800 mm,with a negative water balance throughout theyear. The former regional climatic data were ob-tained from the Meteorological Station at FrayLuis Beltran, which is 30 km away from thestudy site. Soils are alluvial and occasionally sub-jected to flooding. During the study, the localdata of ambient air temperature and humiditywere recorded with an hygrothermograph andthose of solar radiation and rain with an auto-matic data recorder (KADEC-U, Kona System,Sapporo, Japan). Soil water content was deter-mined monthly by gravimetry.

Undamaged leaves of ten well-developed trees(8–9 m height) were collected from the uppersun-exposed crown (from 5 m up), the mediumhalf sun-exposed branches (between 1 and 3 mheight) and the lower shaded crown (B1 mheight).

Leaf water content (LWC) during the growingperiod was determined by collecting :100 g ofleaf material at each level of the ten trees. Thefresh weight was determined in recently cutleaves and the dry weight after heating them at60°C for 48 h. Sampling was made in Octoberafter the beginning of the growing period, inDecember, in February and finally in April, justbefore the initiation of the cold latency period.Leaf blade size was determined with a portablearea meter (LI-COR, LI 3000A) from ten leavesof each level of the ten trees.

Foliar architecture was defined according toHickey (Hickey, 1974; Dilcher, 1974) and in-cluded measurements of leaf morphology and ve-nation patterns. Cleared leaves — five leaves ofeach level of the ten trees — were obtained byboiling formol-acetic acid-alcohol (FAA)-fixedleaves in 5% sodium hydroxide, decolorized with10% sodium hypochlorite, cleared in saturatedchloral hydrate, rinsed thoroughly in water,dehydrated through an alcohol series and stainedin saturated safranin in alcohol 50%. After suc-cessive steps in an alcohol series to xylene, eachleaf was mounted with Canada balsam between

M.G. Klich / En6ironmental and Experimental Botany 44 (2000) 171–183 173

specially cut thin glasses. The mounted leaveswere photographed and the photographs en-hanced so that the determination of the vena-tion’s pattern could be easily performed.Drawings of the smaller veins, veinlets and are-oles were made using a Wild M 5 stereoscopicmicroscope and a Wild M 20 binocular micro-scope, both with drawing tubes. Microphoto-graphs were taken with a Zeiss PhotomicroscopeII. Drawings of each epidermis were made afterremoving the other epidermis and most of themesophyllic tissue. Means of measurements ofanatomical features were based on five measuresper leaf in five leaves of each of the three levelsof the ten trees.

The estimation of leaf volume, mesophyll vol-ume, proportion of mesophyll in the leaf andproportion of spongy and palisade parenchymawere made with data obtained, by stereologicalprocedures, from drawings of photographedtransverse sections of paraffin-embedded mate-rial, stained in safranin-fast green and mountedin balsam. The sampling of tissue blocks to beused for stereological measurements of leafanatomy and the estimation of the mentionedcharacters was made following the recommenda-tions of Kubınova (1993). Data were obtainedfrom five transverse sections per leaf in fiveleaves of each of the three levels of the ten trees.

Leaf material for scanning electron microscopy(SEM) was fixed in FAA. Samples were dehy-drated in a series of alcohol of increasingstrength to absolute alcohol and in a series ofalcohol–acetone to pure acetone, treated in aPolaroid critical point dryer and coated with afilm of gold with a sputter coater Pelco 91000.Both epidermis of each sample were examinedwith a JEOL 35 SEM operated at 7 KV.

The relation between the various tissues of thepetioles at the different level in the plants wasdetermined by drawings of the cross-section atthe basal and distal end of the petioles, usingUTHSCSA Image Tool (University of TexasHealth Science Center, San Antonio, TX). Freehand sections were made on five petioles of eachof the three levels of the ten trees.

The evaluation of the data was carried out bymeans of ANOVA and the mean values of thetreatments were compared using the Student–Newman–Keuls’ test.

3. Results

Table 1 shows the data of the environmentalconditions registered during the growth period1997–1998 in the sampling zone. Air tempera-ture outside the shaded understorey reachedhigher values, up to a maximum of 42°C in Jan-uary 1998. Air humidity in the lower protectedstrata reached a minimum of 36% and attained100% every night, but in the upper sun and windexposed zone, values ranged from 18% up to amaximum of 84%.

Fig. 1 represents the average monthly mea-sures of daily solar radiation as well as the maxi-mum hourly records in the upper canopy of theE. angustifolia trees. During spring and summertime, solar radiation is very high and the valuesclimb up to 927 calorie cm2/day in December.Light attenuation at the lower level reaches 90%and at the medium level ranges between 60 and80%.

Leaf water content decreased through the grow-ing period at all levels in the plants, but while inspring the higher values were those of half-ex-

Fig. 1. Mean daily solar radiation (cal. cm2/day) and maxi-mum hourly solar radiation (cal. cm2/h) registered during theperiod April 1997 to March 1998 in the upper canopy of the E.angustifolia trees.


Tab

le1

Env

iron

men

tal

cond

itio

nsof

the

sam

plin

gar

eadu

ring

the

grow

thpe

riod

(199

7–19

98)

ofE

.an

gust

ifol

iaa

%A

H(l

ower

heig

ht)

AT

(°C

)(l

ower

heig

ht)

%A

H(u

pper

heig

ht)

%SW

C(2

0,40

and

60cm

Rai

n(m

m)

(min

,m

ax)

(max

,m

in,

mea

n)(m

in,

max

)de

pth)

3081

4.5

33.6

27.8

9.3

Aug

ust

13.3

1.5

7.4

5310

0Se

ptem

ber

17.0

3073

26.3

16.5

15.9

5110

014

.31.

78.

028

.017

.614

.119

.717

.34.

811

.141

100

3069

Oct

ober

2863

16.0

20.6

8.1

14.3

Nov

embe

r37

100

33.8

30.9

29.0

5210

030

.025

6123

.910

.117

.3D

ecem

ber

16.1

15.9

13.7

3.5

7.0

11.3

11.8

25.4

11.4

18.4

3610

018

60Ja

nuar

y21

6947

.511

.414

.011

.0F

ebru

ary

22.3

10.5

16.4

5610

035

8022

.521

.66.

914

.2M

arch

4810

010

.014

.315

.334

8448

100

18.1

6.5

11.9

19.5

Apr

il13

.917

.418

.3

aA

vera

gem

onth

lyso

ilw

ater

cont

ent

(%SW

C)

atdi

ffer

ent

dept

h;av

erag

em

axim

um,

min

imum

and

mea

nm

onth

lyai

rte

mpe

ratu

re(A

T°C

);av

erag

em

inim

uman

dm

axim

umm

onth

lyai

rhu

mid

ity

(%A

H)

atlo

wer

(1m

)an

dup

per

(5m

)he

ight

;an

dm

onth

lyra

in(m

m).


Table 2Comparison of leaf water content (LWC%) of E. angustifolialeaves developed at different heights in a treea

MLLL UL

74.11bOctober 70.20a75.90bDecember 74.54b 73.27b 68.99a

57.90a 57.54aFebruary 62.07b51.10a 55.81b51.13aApril

a LL, lower shade leaves (B1 m height); ML, medium leaves( 1–3 m height); UL, upper sun leaves (\5 m height). Valuesare the mean for 30 measurements. For each row, valueswhich have the same letter are not significantly different at the0.05 level, as determined by Student–Newman–Keuls’ test.

the tree level increases but its course is generallystraight. The angles of divergence of secondaryveins were found to be always acute, althoughthey are wider in the upper leaves. The relativethickness of secondary veins is moderate and theircourse is mainly curved. The intersecondary veinsare simple and the intercostal areas are irregular.The pattern of tertiary veins is randomly reticu-late. The higher order of venation is quaternaryand a looped marginal ultimate venation is ob-served. The areoles are imperfect, pentagonal topolygonal and randomly arranged. In the upperleaves, the density of areoles is higher (17 areoles/mm2) than in the medium and lower ones (15 and14 areoles/mm2, respectively). Veinlets are mainlybranched. One to three veinlets generally entereach areole, but areoles lacking terminal veinletsare also common.

The thickness of the foliar blades increases withthe height and the degree of sun exposure, whiletheir area decreases, so that the mean volume ofthe leaves at the evaluated levels has no significantdifferences (Table 4).

Leaves are bifacial, with a biseriate palisade inthe two inferior levels, but a third poorly orga-nized stratum is observed in the upper leaves (Fig.2b,d,f). Spongy mesophyll cells are round or elon-gate, not lobed and randomly oriented. The pro-portion of mesophyll tissue is higher in the upperleaves (81.86%) than in the medium (74.93%) andlower (73.97%) leaves, but the ratio between pal-isade and spongy parenchyma remains constant(average 60 and 40%, respectively) at all leaflevels.

Leaves are hypostomatous, with anomocyticstomata (Fig. 3). Stomata are at the level of theneighboring ordinary epidermal cells. The pentag-onal or hexagonal epidermal cells are smaller inthe lower than upper epidermis. Adaxial epider-mis is thinner in the upper leaves but the outertangential walls are thicker than in the lowerleveled leaves. Stomata density is higher in theupper leaves, but there are no significant differ-ences in their length and width between the threeanalyzed leaf levels (Table 3). The abaxial surfaceof the leaves is always more pubescent than theadaxial one. Trichomes are multicellular,pedestalled, stellate-branched or peltate, and their

posed and shade-leaves, in April these were theleaves that bore the lower values (Table 2).

The leaves of E. angustifolia are annually decid-uous, however, many of the upper leaves maypersist when winters are wetter and warmer thannormal. New leaves are produced during late win-ter and early spring, along with the abscission ofthe old winter persistent leaves. Fully expandedleaves are simple and symmetrical, with entiremargins. Upper leaves of E. angustifolia are in-clined, especially at midday, while the mediumand lower leaves are nearly perpendicularly ori-ented to the incident light. Upper leaves upfoldthrough the midvein. Table 3 shows the foliarfeatures of the differently leveled leaves. By theirsize they are classified as microphyll, althoughsome of the medium leaves are mesophyll. Theform of the whole lamina is ovate in the inferiorlevels and oblong to elliptic in the upper level; theform of the base and the apex varies between theleaves in the inferior levels but is always acute inthe upper levels (Fig. 2a,c,d). The lamina textureis chartaceous but the color varies; adaxial sur-faces of leaves are dark green in the shadedinferior branches, light green in the half exposedand silvery grey–green in the sun exposed canopy.The abaxial surface always presents a lightercolor, a feature that is especially evident in thetwo lower levels of leaves. The type of venation ispinnate eucamptodromous (Fig. 2a,c,d). The sizeof the primary vein, calculated as the percent ofvein width to leaf width, is larger as the height of


form and density can be associated with leaf level,color and appearance. Lower leaves have

branched hairs and present a woolly appearanceabaxially (Fig. 4a,b). The abaxial epidermis of the

Table 3Comparison of morphological and anatomical features of E. angustifolia leaves developed at different heights in a treea

Medium leavesLower shade leaves Upper sun leaves(1–3 m height)(B1 m height) (\5 m height)

Microphyll from 7.5 to 18.7Lamina area (one side) cm2 Microphyll from 4.2 to 10.5Microphyll-mesophyll from4.6 to 23.7

Lamina length Upto 10 cm.Upto 10 cm. Upto 10 cm.Symmetrical SymmetricalShape: whole lamina Symmetrical

SymmetricalGenerally symmetricalShape: base only SymmetricalOblong: narrow-oblongOvate: ovate (l/w: 1.5:1) Ovate: lanceolate (l/w:3:1)Form: whole lamina (l/w:(l/w:3:1) Elliptic:length/width) narrow-ovate (l/w: 2:1)narrow-elliptic (l/w:3:1)lanceolate (l/w: 3:1)Acute normalAcute cuneate rounded to Acute cuneate obtuseForm: base only

decurrentcordateForm: apex only AcuteAcute or obtuseAcute, obtuse or obtuse

mucronateEntire EntireMargin Entire

Texture ChartaceousChartaceous ChartaceousSilvery grey–green (bicolor)Appearance Adaxial light green (notableAdaxial dark green (notable

bicolor)bicolor)Attachment (petiole) NormalNormal Normal

Pinnate eucamptodromousType of venation Pinnate eucamptodromous Pinnate eucamptodromousModerate (1.25–2%) to stout Stout (2–4%) to massiveSize of primary vein % vein Stout (2–4%)(2–4%) (\4%)width/leaf width

Course of primary vein Straight (some slightly Straight (some slightly curved) Straightcurved)

Acute: narrow (B45°) toAngle of divergence of Acute: moderate (45–65°) toAcute: narrow (B45°) towide (65–80°)moderate (45–65°)secondary veins moderate (45–65°)

Lower and upper secondary UniformVariation in angle of Lower and upper secondaryveins more obtuse than middledivergence of secondary veins more obtuse than

veins setsmiddle setsModerateModerateModerateRelative thickness of

secondary veinsCurvedCourse of secondary veins Straight to curvedCurved

Pattern of tertiary veins Random reticulateRandom reticulate Random reticulate42.90b 29.37a43.16bAdaxial epidermal thickness

(mm)Adaxial epidermal outer wall 5.02a5.36a 9.09b

thickness (mm)18.18aAbaxial epidermal thickness 20.31a 16.99a

(mm)2.49a2.72a 3.01aAbaxial epidermal outer wall

thickness (mm)312c247aStomata/mm2 270b

Guard cell length (mm) 16.94a16.96a 17.02aGuard cell width (mm) 10.10a 10.07a 10.11a

327bAbaxial indumentum height 341b 257a(mm)

a Morphological and data are the result of measurements conducted on 100 leaves per leaf type. Venation patterns weredetermined from measurements conducted on 50 leaves per height. Anatomical values are the mean for 250 measurements. For eachrow, values which have the same letter are not significantly different at the 0.05 level as determined by Student–Newman–Keuls’ test.


Fig. 2. Cleared leaves of E. angustifolia and drawings of transverse sections. (a,b) Lower shade leaves; (c,d) medium half sun-exposedleaves; (e,f) upper sun-leaves. (For a,c,e, bar: 1 cm; for b,d,f, bar: 50 mm).

light green leaves from half exposed brancheshave several hair layers, the external ones com-posed of hairs totally branched or stellate withcells arranged radially and joined near the tri-chome stalk and the internal layer formed bypeltate hairs with the cells of the shield partiallyjoined. The rays of adjacent trichomes interlockand form a dense cover over the abaxial leafsurface (Fig. 4d,e). The silvery highly sun exposedleaves from the upper branches have only peltatehairs that, in the abaxial leaf surface, are arrangedto form two or three layers of their flattenedmulticellular shields (Fig. 4g,h). Abaxial indumen-tum height is greater in the lower leaves (Table 3).All abaxial epidermal cells remain covered by the

indumentum. The same type of hairs are found inthe respective adaxial epidermis of each type ofanalyzed leaf, but they are too sparse and, al-though their rays have a greater length andspread, they do not form a canopy and manyepidermal cells remain exposed, especially in thetwo lower levels of leaves (Fig. 4c,f,i).

When the tissue distribution of the petioles ofthe differently leveled leaves is compared, it isfound that when height increases there is an en-largement of the proportion of epidermis, col-lenchyma and phloem while the relative amountof parenchyma and xylem diminishes (Table 5).Petioles are slender in the upper leaves. In trans-verse sections through the basal end, they exhibit


Table 4Comparison of leaf dimensions and tissue compositions of E.angustifolia leaves developed at different heights in a treea

ML ULLL

0.326a 0.382bThickness (mm) 0.474c(without hairs)

1132.00a,bArea (mm2) 955.91a1250.08bVolume (mm3) 407.53a 432.42a 450.82a% Mesophyll 73.97a 74.93a 81.86b

58.40a60.23a 62.62a% Palisade41.60a% Spongy 37.38a39.77a

a LL, lower shade leaves (B1 m height); ML, medium leaves(1–3 m height); UL, upper sun leaves (\5 m height). Valuesare the mean for 250 measurements. For each row, valueswhich have the same letter are not significantly different at the0.05 level as determined by Student–Newman–Keuls’ test.

4. Discussion

The environmental measurements made duringthe study demonstrate the great variation in thehabitat conditions to which the leaves at differentlevels are exposed. As the area is included in asemiarid to arid region, summer temperature out-side the shaded understorey reaches much highervalues than under the canopy. Differences are alsofound in air humidity; while in the lower strata itreaches saturation every night, at the upper ex-posed canopy the values are always lower. The highsolar radiation is greatly attenuated by the foliagein such a way that the lower leaves can really beconsidered as growing in the shade. As there is anexponential relationship between light absorptionand cumulative foliage area, the light gradientacross the canopy should be greater for highervalues of incident irradiance (Niinemets, 1996b).

If the climatic data are considered in a generalregional sense, it can be assumed that the scarcityof soil water resources and/or the high evaporativedemand of the atmosphere during the warmerseasons induce stress situations. The survival of

an open vascular arc and it becomes incurved tothe distal end. Though the vascular strand nearlyforms a cylinder in the petioles of the upperleaves, the vascular arc remains slightly open (Fig.5). Trichomes on petiole epidermis are in accordwith those of the corresponding leaf.

Fig. 3. Drawings of abaxial (a,c,e) and adaxial (b,d,f) epidermis (amidst trichomes) of E. agustifolia. (a,b) Lower shade leaves; (c,d)medium half sun-exposed leaves; (e,f) upper sun-leaves. (Bar: 10 mm).


Fig. 4. Scanning electron micrographs of the epidermis of E. angustifolia. (a,b,c) Lower shade leaves; (d,e,f) medium halfsun-exposed leaves; (g,h,i) upper sun-leaves. (a,b,d,e,g,h) Abaxial epidermis; (c,f,i) adaxial epidermis.

the plants to adverse conditions requires long-and short-term plasticity responses and trees maydevelop stress avoidance mechanisms by an ade-quate canopy architecture (Save et al., 1995), rootdevelopment (Fernandez et al., 1988) or leaf het-erogeneity (Niinemets, 1996a). When light is thelimiting factor, since trees have the potential toreach unshaded overstorey, the adaptability ofcrown architecture may be an important determi-nant of competitive strength than foliar plasticity(Niinemets, 1996b). However, when trees developat different strata, the canopy of the same plant isexposed to diverse natural environments. Thus,the leaf morphoanatomical plasticity with respectto the combined conditions of incident irradiance,air temperature and humidity may be one of the

Table 5Comparison of petiole tissue composition (%) of E. angustifo-lia leaves developed at different heights in a treea

ML ULLL

10.04a 16.97b 23.90cCollenchyma18.75b16.44aPhloem 16.30a

54.14c 48.58b 35.90aParenchyma7.20a8.82bXylem 9.42c

9.94a 9.32aEpidermis 14.30b

a LL, lower shade leaves (B1 m height); ML, medium leaves(1–3 m height); UL, upper sun leaves (\5 m height). Valuesare the mean for 100 measurements. For each row, valueswhich have the same letter are not significantly different at the0.05 level as determined by Student–Newman–Keuls’ test.


Fig. 5. Transverse sections through the basal (a,c,e) and distal (b,d,f) end of the petioles of E. angustifolia. (a,b) Lower shade leaves;(c,d) medium half sun-exposed leaves; (e,f) upper sun-leaves. (External white: epidermis; squared: collenchyma; internal white:parenchyma; dashed: xylem; dotted: phloem). (Bar: 150 mm).

features that confers the species success in theirpermanence and even in their competition withother species.

The changes in the dimensions — especially thewidth — of the leaves of E. angustifolia, can beconsidered to have a functional significance re-lated to the different natural conditions in whichthey developed. The shaded as well as the half-ex-posed branches, with wider ovate leaves, developin an environment of low irradiance, relativelyhigh air humidity content and are protected fromthe wind. The upper narrow oblong or ellipticleaves are exposed to high light, low air humidityand dry winds. The reduction of leaf dimensiongenerates an increase in convective heat dissipa-tion, that is important to counteract the negativeeffects of overheating and high transpiration rates(Gates, 1980) such as those to which the upperleaves of E. angustifolia are exposed.

Upper leaves of E. angustifolia are inclined,especially at midday, while the medium and lowerleaves are nearly perpendicularly oriented to theincident light. This characteristic may be relatedto the high values of irradiation registered in theregion and to which the upper leaves are exposed,for it has been determined that high light has adetrimental impact on photosynthetic perfor-mance (Smith et al., 1997) and leaf movementstending to avoid full exposition partially counter-act these harmful effects. Furthermore, during thehigher irradiation periods, upper leaves upfoldthrough the midvein. Lower shade leaves, onthe other hand, must capture as much light aspossible and their orientation helps to fulfillthis requirement. Although narrow blades andinclined leaves contribute to the avoidance ofmutual shading between leaves (Yamada andSuzuki, 1996), the solar radiation reaching the


under storey of E. angustifolia clusters is neverthe-less greatly attenuated.

Bicolor is a common phenomena among speciesthat occupy shaded habitats; the leaf side that facesaway from the sun is lighter in color than the leafsurface facing towards the sun. The lighter surfacemay act as a reflective surface and enhance theparticipation of the spongy mesophyll in leaf pho-tosynthesis. Smith et al. (1997) suggest that thepresence in shaded environments of thin, horizon-tal, bicolor laminar leaves that have stomata onlyin the abaxial epidermis may have evolved as aresult of a selective pressure to enhance lightcapture while avoiding the detrimental effect ofexposing the stomata directly to sunlight andminimizing transpirational water-loss. In E. angus-tifolia the difference in color between both leafsurfaces is especially evident in the two lowerlevels, but it also occurs in the upper level. As sunleaves have a silvery grey–green adaxial face anda brilliant silver colored abaxial one and as theyupfold through the medium vein under the highersolar radiation conditions, they mainly expose thishighly reflective surface.

Though there are some variations in the grossmorphology of the leaves of E. angustifolia atdifferent levels in a tree, the pattern of majorvenation is the same in all of them, which is logical,as the latter is a character considered of systematicvalue (Dilcher, 1974). Increased vein density ispositively correlated with water stress in the habi-tat (Pyykko, 1966) and the higher areole density inthe upper leaves of E. angustifolia may be aresponse to the dryer habitat to which they aresubmitted. The proportionally greater primaryvein size of upper leaves means an additionalmechanical advantage under those stress environ-mental conditions.

The use of only the size and morphology of theleaf as indicators for xeromorphy or plasticity isinsufficient and anatomical features, such as thevolume and organization of the mesophyll tissue,should be taken into consideration (Fahn andCutler, 1992). The greater thickness of the uppersun E. angustifolia leaves is related to a higherproportion of mesophyllic tissue. These character-istics are mentioned as structural mechanisms thatincrease photosynthesis per unit leaf area and

enable a greater water-use efficiency. Leaves in theupper part of the canopy or sun leaves have higherrates of carbon assimilation and water loss and arethus, physiologically more active (Boardman,1977). Leaves exposed to high irradiation condi-tions or sun leaves generally develop a well-definedpalisade parenchyma and those that grow underlow irradiation condition or shade leaves, arethinner and present a less defined palisade layerthan the former (Vogelmann, 1993). The tissuedistribution in the mesophyll remains constantamong the studied E. angustifolia leaves, but theaverage diameter and length of palisade cells aresmaller in the upper ones in which an incompletethird palisade stratum is a common feature. Ahigher number of palisade cells in the mesophyllvolume may imply an increase in photosyntheticefficiency. The columnar cells of the palisade tis-sue, beside their contribution in the CO2 exchange,may have also an optical function (Vogelman,1989). The directionality of light can affect lightgradients within leaves. Vogelman and Martin(1993) stated that palisade appears to facilitate thepenetration of directional but not diffuse light.This is particularly important in leaves exposed todirect sunlight, where the irradiance is highly colli-mated.

The epidermis and cuticle strengthen the leaf.The epidermal thickness of the upper, more-ex-posed leaves of E. angustifolia is smaller whencompared with the other leaves, but has a propor-tionally greater outer tangential wall (measured aswall plus cuticle) and this feature has been relatedto increased aridity and/or insolation (Pyykko,1966; Fahn and Cutler, 1992). No differences werefound in the size of stomata but their densityincrease from the lower to the upper leaves of E.angustifolia. Size and density of stomata have beenwidely studied and related to many environmentalfactors (Salibury, 1927; Shields, 1950; Klich et al.,1996a,b). Small stomata in large numbers seemedto be characteristics of xeromorphic leaves(Shields, 1950); however, Meidner and Mamsfield(1968) found a great stomatal frequency variationamong mesophytes, so that the efficiency of stom-ata in regulating water loss could not be directlyrelated to their size and frequency.


Pubescence is another characteristic that con-fers stress resistance (Ehleringer, 1980; Klich etal., 1996b) and the presence of hairs on the aerialparts of the plants is regarded as an adaptation toarid conditions (Fahn, 1986). Hairs may affecttranspiration by influencing the water diffusionboundary as an indumentum decreases air move-ments on the leaf surface, creates a zone of still airand reduces diffusion of water vapor from the leafinterior to the atmosphere. An indirect influenceof trichomes on plant water economy is throughtemperature regulation (Ehleringer, 1980). Themicroroughness caused by anatomical characteris-tics, as epidermal cell surface contours and densetrichome layers, substantially increases leaf reflec-tance and reduces radiation absorption which re-sults in the reduction of leaf temperature andconsequently of leaf transpiration rates(Premachandra et al., 1991, McWhorter, 1993;Karabourniotis et al., 1995; Klich et al., 1997).The abaxial epidermis of all the leaves of E.angustifolia is densely covered by hairs and al-though the indumentum height of the lower leavesis greater than that of the upper leaves, the tri-chomes of the latter, with their overlapping flat-tened shields, may constitute a stronger barrier togas diffusion.

The lower leaves of E. angustifolia are the mostsensitive to environmental changes and when soilwater content decreases or when these leaves be-come exposed because of the removal of neigh-boring plants, the trees shed the leaves of theinferior branches (personal observations, unpub-lished data). Lower strata are also the first to shedtheir leaves at the end of the growth period,initiated by a decrease in their water content.

The higher proportion of epidermis and col-lenchyma of the upper leaf petioles is not unex-pected, as Pyykko (1966) already confirmed acorrelation between strong development of me-chanical tissue and habitat aridity.

Leaf variability in E. angustifolia can be consid-ered an adaptive advantage of both upper andlower leaves in habitats marked by strong varia-tions of sun radiation, air humidity and tempera-ture and wind exposition. Upper leaves showmany xeromorphic characters that enables thetrees to maintain their canopy foliage even under

the unfavorable conditions — high solar radia-tion, high temperature, low humidity — duringthe summer. Lower leaves show many traits ofshaded leaves and allow the plant to compete forspace also in the understorey.

These data confirm the hypothesis that varia-tions in developmental responses of E. angustifolialeaves to spatial heterogeneity are related to itsecological strategies. This invasive species relies,at least partially, on its foliar plasticity to over-come the environmental gradient between thelower and upper parts of a developed tree andeven to compete against other species when itgrows in places where spatial environment hetero-geneity can easily manifest, as in a river valley ofa semiarid region.

Acknowledgements

I would like to thank Marıa Elena Garcıa andLucrecia Gallego for their technical assistance andtheir help with the drawings; Federico and LuisFresser for their help with field temperature andhumidity measurements and the technical assis-tance of the Electron Microscopy Laboratory ofthe Centro Regional de Investigaciones Basicas yAplicadas de Bahıa Blanca (CRIBABB), Ar-gentina. This research was supported by a grantfrom the Universidad Nacional del Sur, BahıaBlanca, Argentina

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