Correlation between leaf age and other leaf traits in ...directory.umm.ac.id/Data Elmu/jurnal/E... · PII: S0098-8472(99)00052-0. 142 L. Gratani, A. Bombelli:En6ironmental and Experimental

Environmental and Experimental Botany 43 (2000) 141–153

Correlation between leaf age and other leaf traits in threeMediterranean maquis shrub species: Quercus ilex, Phillyrea

latifolia and Cistus incanus

Loretta Gratani *, Antonio BombelliDipartimento di Biologia Vegetale, Uni6ersità di Roma ‘La Sapienza’, P.le A. Moro, 5, 00185 Rome, Italy

Received 12 February 1999; received in revised form 29 September 1999; accepted 9 October 1999

Abstract

The anatomical and morphological leaf traits as well as leaf inclination and orientation per different leaf age cohortof Quercus ilex, Phillyrea latifolia and Cistus incanus growing in the Mediterranean maquis along Rome’s coast-line(Italy) were investigated. Specific leaf weight (SLW), total leaf thickness (L), leaf density index and leaf inclination(a) changed according to leaf age. The maximum values were measured at full leaf expansion, underlining the stronginfluence of a on the reduction of solar radiation incident on leaf surface and the importance of the received solarradiation by leaf structure during leaf age. C. incanus summer leaves had the lowest surface area, the highest SLW(1592 mg cm−2) and L (244915 mm) with respect to winter leaves, reducing the evaporative leaf surface duringdrought. Older leaves of 2–4 years Q. ilex and P. latifolia, shaded by new leaves had lower a than 1 year old leaves.a is a linear function of SLW. By the seasonal leaf dimorphism and the characteristic leaf folding the adjustment ofleaf inclination angle from −37° in winter leaves to +44° in summer leaves increased reduction of incident solarradiation during drought. Leaf folding may be related to the less xeromorphic leaf structure of C. incanus. The indexof xeromorphism, measured at full leaf expansion and resulting from the surface area of the polygon plotted joiningthe value of the seven considered xeromorphic leaf traits in the radar graph, is the highest in P. latifolia (0.88), andthe lowest in C. incanus (0.44). © 2000 Elsevier Science B.V. All rights reserved.

Keywords: Evergreen Mediterranean shrubs; Leaf age; Leaf inclination angle; Specific leaf weight; Leaf thickness; Leaf density;Xeromorphic index

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1. Introduction

Evergreen sclerophylls and drought semi-decid-uous species which prevail in regions with Med-iterranean climate represent different adaptive

strategies (Christodoulakis, 1989; Kutbay andKilinç, 1994). Evergreen sclerophyllous specieswhich have high construction cost of leaf protec-tive structures (Chabot and Hicks, 1982; Williamset al., 1989) are long-lived (Miller and Stoner,1979; Mooney, 1981), while semi-deciduous areshort-lived and their adaptations include leafanatomical differences between summer and win-

* Corresponding author. Fax: +39-6-4991-2358.E-mail address: [email protected] (L. Gratani)

S0098-8472/00/$ - see front matter © 2000 Elsevier Science B.V. All rights reserved.

PII: S0098 -8472 (99 )00052 -0

L. Gratani, A. Bombelli / En6ironmental and Experimental Botany 43 (2000) 141–153142

ter leaves (Orshan, 1963; Westman, 1981;Christodoulakis, 1989; Correia et al., 1992;Gratani and Crescente, 1997). Seasonal and leafage changes may be a source of variation in therelationship between the different leaf traits (Re-ich et al., 1991). Although there are numerousstudies dealing with leaf morphological trends ofMediterranean evergreen species in response toenvironmental changes, their functional interpre-tation should be carefully considered (Reich,1993; Smith et al., 1998).

Increasing drought stress may determine ashortening of leaf life-span (Field and Mooney,1983; Jordan, 1983; Wolfe et al., 1988). We ad-vanced the hypothesis that real evergreen sclero-phyllous shrub species, by their long leaf life-spanand the high degree of xeromorphism, will be at acompetitive advantage in respect to semi-decidu-ous species, considering the forecasted increase ofair temperatures and drought in the Mediter-ranean climate. The high degree of xeromorphismmay permit evergreen sclerophyllous species toadapt to a changing environment maintainingtheir position in the community. The approachwas to measure the relative importance of thoseleaf traits which are important life-history traits ofplants with respect to their environment (leaflife-span, leaf inclination, leaf orientation) andthose which reflect the species adaptation (specificleaf weight (SLW), total leaf thickness (L), leafdensity, plasticity index) during leaf age. To ob-tain evidence supporting this hypothesis Quercusilex, Phillyrea latifolia, typical evergreen sclero-phyllous shrubs, and Cistus incanus, a drought-semi-deciduous shrub were compared; these arespecies largely represented in the Mediterraneanmaquis.

In a Mediteranean climate water stress duringsummer is often accompanied by high air temper-atures, high irradiance and high leaf to watervapour deficit. It has been demonstrated that thecombination of these factors favour leaf photoin-hibition (Björkman and Powles, 1984; Valladaresand Pearcy, 1997). Since leaves of most evergreenmaquis species cannot effectively utilize the fullirradiance, leaf inclination in all probability, pro-vides the most powerful means of regulating lightinterception (De Lucia et al., 1991; Poulson and

De Lucia, 1993; Ryel et al., 1993; Björkman andDemming-Adams, 1995; Myers et al., 1997; Kaoand Tsai, 1998). Plants with steeper a may notonly utilise more efficiently the reduced incidentflux, but also reduce the potential for photoinhibi-tion (Powles and Björkman, 1981; Ludlow andBjörkman, 1984; Werner et al., 1999). The evolu-tion of leaf structure is assumed to have occurredin concert with the evolution of leaf orientationproperties (Smith et al., 1998), therefore the au-thors would like to analyse how leaf inclination ofthe examined species is associated with leafstructure.

2. Materials and methods

2.1. Study area

The study was conducted in the Mediterraneanmaquis developing along the coast near Rome, inthe Castelporziano Estate (41°45% N; 12°26% E).The area’s climate is of Mediterranean type andmost of its annual rainfall is distributed in au-tumn–winter (Table 1). The average minimum airtemperature of the coldest month (February) was4.1°C and the average maximum air temperatureof the hottest month (August) was 30.8°C (databy the Castelporziano Meteorological Station,1987–1998, Table 1). Detailed descriptions of veg-etation is available in Gratani and Marinucci(1985).

All field measurements were made on randomlychosen Q. ilex L., P. latifolia L. and C. incanus L.plants (three per species), representative of thepopulation.

2.2. Leaf age

Leaf age was analysed in situ monitoring thenumber of nodes, according to Reich et al. (1992),since flushing patterns and C. incanus leaf dimor-phism were known (Gratani and Crescente, 1997).In order to determine whether leaf traits differedin function of leaf age, different leaf age cohortswere collected in the field from February 1998 toMay 1999. Particularly 2 and 4 month old leaves(summer leaves) and 3, 5 and 8 month old leaves

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Table 1Monthly average maximum air temperature (Tmax), monthly average minimum air temperarture (Tmin), monthly average air temperature (Tm) and total monthlyrainfall (R) for the period 1987–1998 and for the study period (from February 1998 to May 1999)a

Average 1987–1998 Study period

19991998

R (mm) Tmax (°C) Tmin (°C) Tm (°C) R (mm) Tmax (°C) Tmin (°C) Tm (°C) R (mm)Tmax (°C) Tmin (°C) Tm (°C)

5.0 9.4 101.6 13.7 3.852.5 8.813.8 33.49.04.413.6Jan50.7 15.4 4.9 10.2 100.0 11.8 1.6 6.7 30.0Feb 14.1 4.1 9.1

4.6 10.1 66.6 14.9 6.0 10.515.6 56.443.1Mar 15.9 5.8 10.89.5 14.0 81.4 18.3 9.0 13.7Apr 63.817.8 7.9 12.8 78.8 18.5

12.3 17.6 48.8 23.6 13.5 18.622.8 23.0May 33.716.911.722.236.0 27.3 15.5 21.4 6.626.2Jun 14.6 20.4

17.7 24.1 12.230.4Jul 11.923.817.730.018.8 25.3 17.2Aug 30.8 18.5 24.6 19.6 31.715.0 20.4 57.225.8Sep 57.621.215.626.912.3 17.0 127.8Oct 22.6 12.8 17.7 151.2 21.6

7.2 11.3 26.415.4105.1Nov 17.1 8.4 12.83.4 8.0 67.0Dec 13.6 5.4 9.5 86.5 12.5

713Total annual precipitation 727

a Data of the Meteorological Station of Castelporziano, Rome.


(winter leaves) of C. incanus ; 8 month, 1, 2 and 3year old Q. ilex leaves; 8 month, 1, 2, 3 and 4 yearold P. latifolia leaves were examined. In eachsampling occasion forty leaves were collected perdifferent leaf age cohort. These data were chosento include both expanding and fully expandedleaves.

2.3. Photosynthetic acti6e radiation (PAR)

PAR was measured on 02/02/98, 06/03/98, 06/07/98 and 03/08/98, using a Li-COR 190SB Quan-tum Sensor. The reduction of PAR incident on asloping leaf surface (RI) was calculated, per spe-cies and per different leaf age cohort by: RI=100(1−Is/I0), where I0 was the fraction of PARintercepted by a horizontal surface and Is thefraction of PAR incident on a sloping leaf surface(Ehleringer, 1989).

2.4. Leaf orientation and leaf inclination

Leaf movement analysis was determined by di-urnal measurements of leaf orientation (or az-imuth, h) and leaf inclination (a) (Nobel et al.,1993) and were conducted in the morning (09:30 hin winter, 07:30 h in summer), at midday (12:00 hin winter and in summer) and in the afternoon(14:30 h in winter, 16:30 h in summer) (Prichardand Forseth, 1988), during the coldest (02/02/98and 06/03/98) and the hottest (06/07/98 and 03/08/98) months of the year, in order to observeplant behaviour in response to severe environmen-tal conditions (low temperatures and PAR inwinter; high temperatures, PAR and drought insummer). Forty randomly chosen sun leaves rep-resentative of the population of each species werelabelled, with nylon tape at the base of the peti-oles, and monitored in each sampling occasion. hand a for the different leaf age cohorts wererecorded from February 1998 to May 1999.

Leaf inclination and leaf orientation were ob-tained by measuring the angle from the horizontaland azimuth (0°=N, 90°=E, 180°=S, 270°=W) of the adaxial leaf surface (Prichard andForseth, 1988). Angle measurements were madeby a hand-held clinometer (Suunto Co. ModelPM-5/360PC); azimuth was measured by a com-

pass (Suunto Co. Model KB-14/360R), accordingto Prichard and Forseth (1988). The repeatabilityof both measurements was 95°. Leaf orientationmodified the angle of incidence (i) between thedirect solar beam and the leaf lamina. The cosineof the angle of incidence was a measure of thefraction of the direct solar radiation beam thatstruck a planar surface.

C. incanus leaves were characteristically foldedalong the midrib. The degree of concavity wasmeasured by a goniometer on prints of ink-dippedleaf cross sections (n=120) (Begg, 1980,modified).

2.5. Leaf morphology

Leaf samples (40 observations per species andper different leaf age cohort) were dried at 90°Cfor 3 days to constant weight. Leaf surface area(SA), excluding petiole, was measured using theImage Analysis System (Delta-T Devices, LTD).SLW was calculated as the ratio of leaf dry weightto unifacial leaf area (Reich et al., 1992). Leafdensity index (LDI) was calculated by the ratio ofleaf dry weight and leaf volume (g cm−3), inorder to express leaf compactness (Christodou-lakis and Mitrakos, 1987).

2.6. Leaf anatomy

Leaf sections were hand-cut from fresh fullyexpanded leaves (4 month old summer leaves and8 month old winter leaves of C. incanus ; 1 yearold leaves of Q. ilex and P. latifolia), dehydratedin 90% ethanol and analysed by light microscopy(Bolhàr-Nordenkampf and Draxler, 1993). Thefollowing parameters were measured (40 observa-tions per species): total leaf thickness (L), palisadeand spongy layer thickness, thickness of the adax-ial and abaxial epidermis, thickness of the adaxialand abaxial cuticle. Total leaf thickness was alsomeasured per different leaf age cohort.

The ratio of palisade parenchyma thickness tothe mesophyll thickness, that reveals xeromorphychabitus (Xh), was calculated according to Pyykkö(1966) and Christodoulakis and Mitrakos (1987).

Plasticity index (Pi) at full leaf expansion wascalculated according to Carpenter and Smith

L. Gratani, A. Bombelli / En6ironmental and Experimental Botany 43 (2000) 141–153 145

(1981) by (sun leaf thickness−shade leaf thick-ness)/sun leaf thickness.

2.7. Statistics

All statistical tests were performed using astatistical software package (Statistica, StatsoftUSA). The distribution of h1 and a were com-pared to a uniform distribution by x2 test. Thedifferences of hl and a during the day and be-tween winter and summer were tested by one-wayanalysis of variance (ANOVA) and Tukey test formultiple comparison. Diurnal trend of cos(i ) wascompared to the cos(i ) of a horizontal plane(depending only on solar movement) by x2 test.Differences in mean morphological and anatomi-cal leaf traits were determined by t-test, ANOVAand Tukey test for multiple comparison. Linear,quadratic and logarithmic regression relationshipsfor all analysed leaf traits were tested.

3. Results

3.1. Leaf age

The typical evergreen sclerophyllous species, Q.ilex and P. latifolia, had a leaf life-span (LLS) of2–4 years: 84 and 16% leaves of Q. ilex are shedrespectively after 2 and 3 years; 41, 54 and 5%leaves of P. latifolia are shed respectively after 2,3 and 4 years. The seasonal leaf dimorphic shrubC. incanus produced smaller leaves (summerleaves) at the beginning of May, persistingthrough summer and falling mostly in autumn(leaf life-span of 4 months); full leaf expansionwas reached at 4 months. Larger leaves (winterleaves) were produced at the middle of September,persisting through winter and falling in spring(leaf life-span of 8 months). P. latifolia and Q. ilexfull leaf expansion was reached at 1 year oldleaves.

3.2. Leaf orientation, leaf inclination and incidentPAR

hl depended strictly on phyllotaxy: C. incanusand P. latifolia had opposite pattern and Q. ilex a

whorled pattern of leaf attachment. Oppositeleaves of C. incanus and P. latifolia were at 90°,from one to the other on the azimuthal projec-tion, while Q. ilex leaves were about 72°. Tocompare these patterns, leaves were monitored inall four cardinal directions. Azimuth was randomwith respect to sun and did not change daily,seasonally (Fig. 1) or per different leaf age cohort(the deviation from randomness and the differ-ences of means were not significant).

C. incanus, P. latifolia and Q. ilex leavesshowed a constant a throughout the day (Fig. 2)(the differences of means were not significant).

a changed per different leaf age cohort (PB0.01) (Table 2). One year old leaves of P. latifoliashowed the steepest leaf inclination (5997°) insummer, decreasing with increasing leaf age (PB0.01) and Q. ilex showed the same trend. C.incanus showed a different a trend (PB0.01) ofwinter and summer leaves: a was negative (−37912°) in winter leaves while it was positive(44913°) in summer leaves. a was significantlycorrelated with leaf age (PB0.01) (Table 3): aincreased until full leaf expansion, then it de-creased. RI showed the same trend, in particularP. latifolia had the highest RI in summer (47%). awas a linear function of SLW (PB0.05). C. in-canus showed, moreover, a particular trend of leafmargin: winter leaves had a marginal leaf foldingalong the midrib axis (2999°) higher in summerleaves (76911°) (PB0.01) (Fig. 3).

Diurnal trends of cos(i ) was similar for thethree species and per different leaf age cohort,depending solely on solar movement (PB0.01),therefore no form of heliotropism was present.

3.3. Leaf morphology

The average leaf traits of the analysed speciesper different leaf age cohort are shown in Tables2 and 4.

SLW varied significantly (PB0.01) among thespecies and it increased until full leaf expansionwas reached (maximum SA), decreasing with theincrease of leaf age. Fully expanded summerleaves of C. incanus were 20% smaller than winterleaves (PB0.05). SLW at full leaf expansion wassignificantly higher (PB0.01) in Q. ilex and P.


latifolia compared to that of C. incanus. Leaves ofP. latifolia were characterised by the smallest SA,almost three times lower than Q. ilex. SLW sig-

nificantly correlated with leaf age (PB0.01), L(PB0.01), LDI (PB0.01) and a (PB0.05), confi-rming the dependence among the leaf traits (Table

Fig. 1. Distribution of leaf orientation (hl) frequency of Cistus incanus, Phillyrea latifolia and Quercus ilex sun leaves during the dayin winter (02/02/98 and 06/03/98) and in summer (06/07/98 and 03/08/98). In winter: morning=09:30 h (hs=135°), midday=12:00h (hs=174°), afternoon=14:30 h (hs=212°). In summer: morning=07:30 h (hs=85°), midday=12:00 h (hs=177°), afternoon=16:30 h (hs=269°). hs=sun azimuth. The distribution of leaf orientation was random. Standard error is shown.


Fig. 2. Distribution of leaf inclination (a) frequency of Cistus incanus, Phillyrea latifolia and Quercus ilex sun leaves during the dayin winter (02/02/98 and 06/03/98) and in summer (06/07/98 and 03/08/98). In winter: morning=09:30 h (as=26°), midday=12:00h (as=37°), afternoon=14:30 h (as=28°). In summer: morning=07:30 h (as=30°), midday=12:00 h (as=72°), afternoon=16:30 h (as=35°). as=sun zenith. P. latifolia a was steeper in summer than in winter (PB0.01). Standard error is shown.

3). LDI showed the same SLW trend increasinguntil full leaf expansion. In essence, longer leaflife-span combined with higher SLW, L, LDI andsteeper a.

3.4. Leaf anatomy

The microscopical analysis of fully expandedleaves revealed significant variations among the


Table 2a (°), RI (%), SA (cm2), DW (mg), SLW (mg cm−2), LDI (g cm−3) and L (mm) per different leaf age (months) of Cistus incanusa

C. incanus

RI SA DWLA SLWa L LDI

13 2.990.3 2595 8.590.92b 2359162998 0.3690.0132 4.090.7 5991144913 14.791.54b 244915 0.6090.0217 3.591.0 419123c 11.991.7−34910 201914 0.5890.0318 4.790.8 63913−35910 13.391.65c 216913 0.6290.0220 5.090.58c 70916−37912 14.091.3 220914 0.6490.03

a LA, leaf age; a, leaf inclination; RI, reduction of PAR (mmol m2 s−1) incident on the sloping leaf surface; SA, surface area; DW,dry weight; SLW, specific leaf weight; LDI, leaf density index; L, total leaf thickness. Standard error is shown.

b Summer leaves.c Winter leaves.

species (Table 5). P. latifolia showed a particularlythick adaxial cuticle, more than two time higerthan C. incanus. Q. ilex leaves showed hairs onthe abaxial surface while C. incanus on both theadaxial and the abaxial surfaces (data not shown).On the average Q. ilex and P. latifolia showed adensely packed mesophyll with few air spaces; onthe contrary C. incanus showed well developedintercellular spaces (data not shown). P. latifoliahad the highest total leaf thickness (Table 4). Xhof the three species was on the average 0.55(Table 5). Total leaf thickness increased until fullleaf expansion was reached, decreasingprogressively with leaf age increase (PB0.01). Lsignificantly correlated with SLW (PB0.01)(Table 3).

The plasticity index (Pi), calculated on sun andshade fully expanded leaves was the highest in Q.ilex (0.65) and the lowest in C. incanus (0.29).

4. Discussion

Evergreen sclerophyllous shrub species growingin the Mediterranean climate are basically xero-phytes; their leaves are steeply inclined and pos-sess similar basic anatomical organization (Walterand Kreeb, 1970; Kummerow, 1973; Catarino etal., 1981; Mitrakos and Christodoulakis, 1981;Turner, 1994; Karabourniotis, 1998). The resultsare in accordance with this general trend: a higherxeromorphic habitus, according to Pyykkö (1966)

and Christodoulakis and Mitrakos (1987) steeperleaf inclination in summer in response to drought,according to Mooney (1982) and Comstock andMahall (1985) thicker leaf cuticle according toMitrakos and Christodoulakis (1981). Generallythere is a great difference in sun and shade leaf

Table 3Summary of regression relationships between all the analysedleaf traits (n=14)a

Relationshipx–y (leaf traits) R

y=−0.1348x2+8.3684x+213.55 0.78LA–L**y=0.0213x+5.1227LA–SA ns

0.78LA–SLW** y=3.4096 Ln(x)+9.6506y=0.0014x+0.5889LA–LDI nsy=−0.0298x2+1.2224x+34.996LA–a** 0.62y=0.0104x+2.4849L–SA ns

L–SLW** y=0.0623x 0.90y=0.0006x+0.4449L–LDI ns

L–a y=0.0868x+16.108 nsSA–SLW nsy=0.5436x+14.776

y=0.0905 Ln(x)+0.4686SA–LDI* 0.57SA–a y=0.4935x+38.321 nsSLW–LDI** y=0.2115 Ln(x)+0.0102 0.78

y=1.2507x+18.821SLW–a* 0.60nsy=55.329x+7.1915LDI–a

a LA, leaf age (months); L, total leaf thickness (mm); SLW,specific leaf weight (mg cm−2); SA, leaf surface area (cm2);LDI, leaf density index (g cm−3); a, leaf inclination (°).

** The relationships were significant at PB0.01; and* at PB0.05, unless noted ns (not significant, P\0.05).


Fig. 3. Leaf folding along midrib in Cistus incanus winterleaves (average of 02/02/98 and 06/03/98) and summer leaves(average of 06/07/98 and 03/08/98). Standard error is shown.

Table 5Anatomical leaf traits at full leaf expansion of Cistus incanus,Phillyrea latifolia and Quercus ilexa

C. incanus P. latifolia Q. ilex

7.290.7aCab (mm) 16.891.7b 9.791.8c22.393.5aEab (mm) 19.993.1a 14.191.4b

P (mm) 107.299.1a 141.2915.7b 163.2916.0cS (mm) 106.4915.5c93.1912.1a 138.0916.6b

10.891.0a 15.891.8bEad (mm) 9.390.8a6.790.7b3.391aCad (mm) 7.290.9b

0.5490.04aXh 0.5190.05a 0.6190.06b

0.6590.04a 0.5590.04bPi 0.2990.02c

a Cad, adaxial cuticle thickness; Ead, adaxial epidermis thick-ness; P, palisade parenchyma thickness; S, spongy parenchymathickness; Eab, abaxial epidermis thickness; Cab, abaxial cuticlethickness; Xh, palisade parenchyma thickness/mesophyll thick-ness; Pi, plasticity index. Means with the same letter are notsignificantly different (P\0.05). Standard error is shown.

morphological traits in xeric species (Carpenterand Smith, 1981), and consequently in plasticityindex. The latter character may in part explainspecies differences in growth, shade tolerance andphotosynthesis (Carpenter and Smith, 1981) con-tributing mostly to the broad ecological toleranceat air temperature and light energy (Chabot et al.,1979; Williams and Black, 1993). High phenotypicplasticity increases the species fitness and adap-tiveness (Bradshaw, 1965; Osmond, 1987; Fitterand Hay, 1993; Murchie and Horton, 1997). Theanalysed species have a high plasticity index incomparison to other woody species (Carpenterand Smith, 1981) and Q. ilex has the absolutehighest Pi.

Nevertheless the analysis of morphological andanatomical leaf traits reveal different adaptive

strategies. Q. ilex and P. latifolia maintain theirleaves until 3–4 years while C. incanus has a LLSof 4 (summer leaves) to 8 months (winter leaves).Therefore the evergreenness character of C. in-canus is maintained by sequentially formed leafage cohorts rather than by extended leaflongevity. Leaf life-span is an important life-his-tory trait of plants with respect to their develop-ment and response to light, nutrient availability,drought and herbivory (Chapin, 1980; Gray andSchlesinger, 1983; Reich et al., 1987; Codey, 1988;

Table 4a (°), RI (%), SA (cm2), DW (mg), SLW (mg cm−2), LDI (g cm−3) and L (mm) per different leaf age (months) of Phillyrea latifolia,and Quercus ilexa

a RI SA DW SLWLA L LDI

P. latifolia4598 29 3.090.6 61912 20.992.5 3309158 0.6190.025997 47 3.690.612 77914 21.392.2 0.6390.03338918

749133.590.733489924 0.6390.0333891721.292.03995 22 3.590.536 72913 20.691.8 332915 0.6290.043196 14 3.390.5 66915 19.992.048 328914 0.6190.04

Q. ilex51911 358 9.992.6 209966 20.991.7 305918 0.6890.02

310921 0.6990.0537 10.092.812 21397752911 21.391.924 38910 21 9.992.7 205969 20.791.6 309919 0.6790.0336 16 0.6590.0330891819.991.61939583399 9.792.5

a LA, leaf age; a, leaf inclination; RI, reduction of PAR (mmol m2 s−1) incident on the sloping leaf surface; SA, surface area; DW,dry weight; SLW, specific leaf weight; LDI, leaf density index; L, total leaf thickness. Standard error is shown.


Reich et al., 1992). Even when growing in thesame site, different plant species show adaptivedifferences in LLS and related plant traits (Reichet al., 1992; Gower et al., 1993). The highest LLSof the examined evergreen sclerophyllous specieswith respect to the semi-deciduous species may benecessary to cover the higher leaf production costsand achieve a net profit in carbon gain (Mooney,1981). SLW is considered a useful index of xero-morphism (Witkowski and Lamont, 1991). Theresults show that SLW significantly correlateswith total leaf thickness, particularly in palisadeparenchyma thickness. Many authors havedemonstrated that reflectance increases and trans-mittance decreases with an increase in leaf thick-ness (Gausman et al., 1973; Knapp and Carter,1998). Palisade layers may act more as ‘lightconducting pipes’ into the leaf, whereas spongy

mesophyll layers may scatter light more efficiently(Vogelmann, 1993). The thickness of the cuticleoften corresponds with the degree of leaf xero-morphism (Bolhàr-Nordenkampf and Draxler1993), and it is considered part of the leaf con-struction cost (Koike 1988). In the examined spe-cies SLW changes according to leaf age and themaximum SLW is reached at full leaf expansion,generally corresponding with the maximum pho-tosynthetic rates (Gratani, unpublished; Wool-house, 1967). SLW decreases during senescence.An adaptive feature of evergreen leaves may bethat older leaves provide a sink for nutrient stor-age during nutrient uptake (Kutbay and Kilinç,1994). C. incanus summer leaves have the lowestSA and the highest SLW with respect to winterleaves, reducing the evaporative leaf surface dur-ing summer. Moreover the maximum litter-fall inMay–June, just before summer drought, reducesthe system’s nutrient loss due to a lack of leachingby rainwater, according to Nùñez-Olivera et al.(1993).

Q. ilex and P. latifolia have steeper a than C.incanus. The higher a reduces the leaf amount ofsolar radiation (Ludlow and Björkman, 1984;Kao and Forseth, 1991, 1992) in the evergreensclerophyllous species that maintain their leavesthroughout the year. The higher a may be also ameans of preventing photoinhibition of water-stressed leaves and it may provide a mechanismfor reducing transpiration rates during drought bylowering leaf temperatures (Comstock and Ma-hall, 1985). Older leaves are shaded by new andconsequently have a lower a.

C. incanus leaf folding may be related to theless xeromorphic structure of leaves. Water stressmay induce leaf folding as a means of improvingwater use efficiency and avoiding photoinhibition(Chiarello et al., 1987; Werner et al., 1999). By theseasonal leaf dimorphism and leaf folding, theadjustment of leaf inclination angle from −37° inwinter to +44° in summer leaves increases RIduring drought.

The examined species at full leaf expansionwere compared by analysing the degree of xero-morphism, expressed by calculating the surfacearea of the polygon plotted joining the value ofthe considered leaf xeromorphic traits (Fig. 4).

Fig. 4. Radar graph realised utilising LLS, LDI, a, SLW, L,Xh and Pi for Cistus incanus, Phillyrea latifolia and Quercusilex. The degree of xeromorphism of the examined species isexpressed by calculating the surface area of the polygon plot-ted joining the values of the seven considered leaf xeromorphictraits. It was considered that the maximum value of each leaftraits was 1. The ratio between the area of each species and themaximum area give the degree of xeromorphism (P. latifolia=0.88, Q. ilex=0.87, C. incanus=0.44). LLS, leaf life-span;LDI, leaf density index; a, leaf inclination; SLW, specific leafweight; L, total leaf thickness; Xh, xeromorphic habitus; Pi,plasticity index.


The area of the polygon in the radar graph inte-grates many xeromorphic leaf traits, resulting inan integrative index of xeromorphism. Consider-ing all the analysed leaf traits (LLS, SLW, LDI,L, a, Xh, Pi) the two sclerophyllous shrub, whichshow the larger area (0.88 and 0.87, respectively,for P. latifolia and Q. ilex) are the more xeromor-phic species and the semi-deciduous which has thelowest (0.44) is the less xeromorphic species.

The results on the whole enable one to under-line the strong influence of leaf inclination on thereceived solar radiation and the influence of inci-dent light level on leaf structure during leaf age.Moreover it is possible to define adaptive strate-gies of Q. ilex, P. latifolia and C. incanus : thetypical evergreen sclerophyllous species showlonger LLS, steeper a, and higher SLW, LDI, L,that is the opposite in the semi-deciduous species.As global change effects on Mediterranean cli-mate are likely to provide an increase of airtemperature and drought (Houghton et al., 1990;Peñuelas, 1996), it is important to understand themorphological and physiological responses ofthese species in order to predict possible changesin species dominance and in landscape structure(Filella et al., 1998). The results indicate that Q.ilex and P. latifolia will be at a competitive advan-tage on C. incanus, considering that drought stressincrease may determine a shortening of leaf life-span and that C. incanus is the species with thelower LLS, the lower SLW and the lower Pi(lower adaptativness). A high degree of xeromor-phism may be more advantageous to increasingaridity in the regions with Mediterranean climate.

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