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Flora 201 (2006) 108119

Morpho-anatomical differentiation of the balkan populations of the speciesTeucrium flavum L. (Lamiaceae)$

Branislava Lakusic a,, Dmitar Lakusic b, Radisa Janc ic a, Branka Stevanovic b

aFaculty of Pharmacy, Institute of Botany, University of Belgrade, Vojvode Stepe 450, 1100 Belgrade, Serbia and MontenegrobFaculty of Biology, Institute of Botany and Botanical Garden )Jevremovac*, University of Belgrade, Takovska 43,

11000 Belgrade, Serbia and Montenegro

Received 3 January 2005; accepted 26 May 2005

Abstract

Ecological plasticity, i.e., inter-population differentiation of the species Teucrium flavum was analyzed on the basis

of morpho-anatomical variability of its five populations from the maquis (Cisto-Ericetea and Cisto-Micromerietea),

rocky grounds (Festuco-Brometea) and rocky crevices (Asplenietea rupestris) in the Eumediterranean and sub-

Mediterranean region. Univariate statistic analysis included 22 quantitative characters related to the leaf and stem

anatomy and morphology. In order to establish the variability and significance of morpho-anatomical differentiation,

principal component analyses (PCA), multivariate analyses of variances (MANOVA), discriminant components

analysis (DCA) and clustering, according to the UPMGA method based on Mahalanobius distances, have been done.

The morpho-anatomical analysis of plants from the five distant populations confirmed that the species T. flavum

belongs to malacophyllous xeromorphic species. It was established that the plants from all the five populations

analyzed are distinguished by stable conservative xeromorphic characteristics. There is a difference between the

pronounced xeromorphic plants belonging to Eumediterranean populations and the subxeromorphic sub-

Mediterranean ones.

r 2005 Elsevier GmbH. All rights reserved.

Keywords: Teucrium flavum; Evergreen shrub; Morphology; Anatomy; Leaf; Indumentum

Introduction

The Mediterranean species Teucrium flavum L. belongsto Sect. Chamaedrys (Miller) Schreber (Tutin and Wood,

1972), which includes about 30 taxa, at the species and

subspecies rank, distributed mostly in the Mediterranean

Basin. The species range extends over the entireMediterranean Basin, from the eastern coasts of Spain

across France, Italy, Croatia, Serbia and Montenegro,

Albania and Greece, to Turkey in the east, and in the

north of Africa in Algeria, Tunisia and Morocco (Meusel

et al., 1978) (Fig. 1).

T. flavum is an evergreen, branchy, semi-woody shrub,

often over 50 cm tall, that belongs to the life form of

suffruticose chamaephytes. By such a habit T. flavum

markedly differs from other representatives of the sect.

ARTICLE IN PRESS

www.elsevier.de/flora

0367-2530/$- see front matter r 2005 Elsevier GmbH. All rights reserved.

doi:10.1016/j.flora.2005.05.001

$This paper represents a part of the Ph.D. thesis of B. Lakusic ,

entitled Morphological Variability and Ecological Differentiation of

Species of Genus Teucrium L. (Lamiaceae) in Yugoslavia defended at

the Faculty of Biology, University of Belgrade, in the year 2000.Corresponding author.

E-mail addresses: [email protected] (B. Lakusic ),

[email protected] (D. Lakusic ), [email protected]

(B. Stevanovic ).
http://www.elsevier.de/florahttp://www.elsevier.de/flora


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Chamaedrys which might indicate the relict character of

the species and its belonging to the ancient Mediterra-

nean flora (Tutin and Wood, 1972). On the basis of

investigation of flowers and inflorescenses of the genus

Teucrium, Ka stner (1978) introduced a new classifica-

tion of the genus, in which the species T. flavum is

included in Sect. Pollium Schreber.

In the Balkan Peninsula T. flavum is a strictly

calciphilous plant that inhabits limestone and dolomite,

at altitudes between 0 and 200 m. It is an important

element of maquis and garrigue vegetation as well as of

their degradation forms in the Mediterranean and sub-

Mediterranean floristic region (Lakusic , 2000).

The aim of the present study was to establish whether

there exists a morpho-anatomical differentiation be-

tween Eumediterranean and sub-Mediterranean popula-

tions of the xeromorphic species T. flavum, bearing in

mind the environmental, particularly climatic differ-

ences between their habitats. Three out of five popula-

tions analyzed here developed under conditions of the

Eumediterranean climate, on the coasts of the Adriatic

and Aegean Sea. Another two populations inhabit sub-

Mediterranean locations (the Montenegro hinterland, in

the canyons of Cijevna and Moraca rivers), character-

ized by the perhumid-sub-Mediterranean Adriatic cli-

mate (Table 1).

Material and methods

Plant material and morpho-anatomical analysis

A morpho-anatomical analysis was done on plant

samples from five populations of the species T. flavum

growing in the Adriatic (Montenegro) and Aegean

(Greece) part of the Mediterranean Basin. The collected

plant material was either placed in a herbarium or fixed

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Fig. 1. Map of distribution of Teucrium flavum L.

Table 1. Ecological characteristics of the habitats of the analyzed populations

Budva(Montenegro)

Lustica(Montenegro)

Peloponnesus(Greece)

Canyon of Cijevna(Montenegro)

Canyon of Moraca(Montenegro)

Biogeography Adriatic province

of Eumediterranean

region

Adriatic province

of Eumediterranean

region

Aegean province of

Eumediterranean

region

Adriatic province

of

Submediterranean

region

Adriatic province

of

Submediterranean

region

Vegetation Rocky crevices

(Asplenietea

rupestris)

Maquis (Cisto-

Ericetea)

Maquis (Cisto-

Micromerietea)

Rocky grounds

(Festuco-Brometea)

Rocky grounds

(Festuco-Brometea)

Substratum Limestone Limestone Limestone Limestone Limestone

Altitude 40 m 80 m 80 m 200 m

Average annual

temperature

1516 1C 1516 1C 1718.5 1C 1016 1C 1016 1C

Average Januarytemperature

78 1C 78 1C 8.510.5 1C 15 1C 15 1C

Annual

precipitation

13002300 mm 13002300 mm 350600 mm 15003100 mm 15003100 mm

B. Lakusic et al. / Flora 201 (2006) 108119 109


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in 50% alcohol and deposited, respectively in the

Herbarium of the Institute of Botany and Botanical

Garden Jevremovac, Faculty of Biology, University

of Belgrade (BEOU) and Herbarium of the Institute of

Botany, Faculty of Pharmacy, University of Belgrade

(HFF).

Voucher specimens:

1. Budva (Montenegro Eumediterranean): rocky

vegetation (class. Asplenietea rupestris), at the alti-

tude of 40m (Lakusic, D., 25 May 1995, HFF

Fix.no. Bu 01-02).

2. Lustica Stari Krasic i (Montenegro Eumediterra-

nean): maquis (class. Cisto-Ericetea), limestone, at

the altitude of 80 m (Lakusic, D. & B. 2225/96, 27

July 1996, BEOU, HFF Fix.no. TFS).

3. Peloponnesus (Greece, Peloponnesus Eumeditera-

nean: maquis (Stevanovic, V., May 1995, BEOU

Fix.no. TF).

4. Canyon Cijevna, village Dinosa (Montenegro sub-Mediterranean): rocky vegetation (class. Festuco-

Brometea), limestone (Lakusic, B., Jancic, R., Slav-

kovska, V., 09 July 1997, HFF Fix.no. 11).

5. Canyon of Moraca, Dromir (Montenegro sub-

Mediterranean): rocks above the river Moraca (class.

Festuco-Brometea) (Lakusic, B., Slavkovska, V.,

Jancic, R. 12 July 1997, HFF Fix.no. 67).

Anatomical analyses of leaves and stems were done

on permanent slides, prepared by the standard method

for light microscopy. Cross-sections of the leaves (150

samples) and stems (50 samples) were cut on a Reichertsliding microtome (up to 10 mm thick). The sections were

cleared in Parazone and thoroughly washed before

staining in safranin (1% w/v in 50% ethanol) and alcian

blue (1% w/v, aqueous).

Epidermal peels (150 samples), for surface structures

and stomata analyses, were prepared using Jeffreys

solution (10% nitric acid and 10% chromic acid, 1: 1)

and stained in safranin and alcian blue. All slides were

mounted in Canada balsam after dehydration.

Density and type of the leaf and stem hairs, as well as

the paradermal aspect of epidermal cells, were also

studied with SEM (JOEL JSM-6460), for which the

samples were covered by gold.

All morpho-anatomical measurements were done

with the Image Analyzer System Ozaria 2001 and the

data processed in the statistical package Statistica 4.5

for Windows. For each of the quantitative characters, 30

leaf samples and 10 stem samples were obtained from

different individuals belonging to each of the five

populations analyzed.

Twenty-two quantitative characters of the statistical

analysis were grouped in three categories: I, Leaf

anatomy characters (13); II, Leaf shape characters (4)

and III, Stem anatomy characters (5).

I. Leaf anatomy characters: (1) Height of adaxial

epidermal cells; (2) thickness of palisade tissue; (3)

thickness of spongy tissue; (4) height of abaxial

epidermal cells; (5) number of palisade layers; (6)

surface area of adaxial epidermal cells; (7) surface

area of abaxial epidermal cells; (8) surface area of

abaxial stomata; (9) number of abaxial stomata;(10) number of adaxial glandular hairs; (11)

number of abaxial glandular hairs; (12) number of

adaxial non-glandular hairs; (13) number of abaxial

non-glandular hair.

II. Leaf shape characters: (14) Leaf length; (15)

distance between the largest leaf width point and

the leaf top; (16) the largest width of the leaf; (17)

leaf surface area.

III. Stem anatomy characters: (18) Stem diameter; (19)

stem diagonal; (20) stem cortex thickness; (21)

thickness of the stem vascular cylinder; (22) stem

pith diameter.

Statistical analysis

For each of the quantitative characters a univariate

statistic analysis was done on the basis of the following

parameters: average value, minimum, maximum, stan-

dard deviation and standard error. The significance of

differences between the populations studied was estab-

lished by multivariate analyses of variances (MANO-

VA). The general structure of the sample variability

were established by Principal Component Analysis

(PCA). For checking the hypothesis that the analyzed

sample was composed of discrete groups, which are

morphologically differentiated one from the other, a

Discriminant Component Analysis (DCA) was done.

Overall differences between the compared groups are

presented by Mahalanobius distances, which are used

for clustering on the basis of UPGMA method.

Results

Leaf shape and anatomy

The leaves of T. flavum are elliptically oval, being the

widest at the basal part, and rounded at the tip. The leaf

margin is obtusely dentate. The leaf stalk is long. It

should be pointed out that the leaf shape was always the

same in all the populations studied.

In general, in all the populations studied the leaf

length was between 12 and 27 mm, whereas the leaf

width ranged between 11 and 21 mm. The leaf surface

area varied between 80 and 370 mm2.

The leaf indumentum of all the plants studied

was composed of glandular and non-glandular hairs

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(Fig. 2A). The glandular hairs were peltate and capitate.

Peltate hairs (Fig. 2B, D) consisted of a short unicellular

stalk and a multicellular secretory head with large

subcuticular space. Capitate hairs were small in size and

of three types on the basis of their structure: Type I

consisted of a short unicellular stalk and a rather large

secretory head of four cells with a small subcuticular

space (Fig. 2B, D); Type II consisted of a short

unicellular stalk and a secretory head of one or two

cells; Type III consisted of a two-cellular stalk and a

secretory head of one cell (Fig. 2C). The non-glandular

hairs are unicellular, basally widened, sharp on the top

(Fig. 3B) or multicellular, mostly having two to three

cells, uniseriate, branchless, the top cell having a sharp

edge, straight or bended (Fig. 3C). More or less wart-

like cuticular structures are observed on the surface of

the non-glandular hairs (Fig. 3D).

The glandular hairs are at the bottom of the complex

arrangement of the leaf indumentum, leaning against the

epidermal cells, while between them there are dispersed,

long non-glandular hairs that form its upper layer. Basal

cells of the glandular hairs are sunk under the level of

epidermal cells, and their large heads (composed of

several secretory cells) are in contact, leveling with theepidermis or being a bit above thus partially covering

the leaf blade (Fig. 3A).

The indumentum is particularly well developed on the

abaxial leaf side (Fig. 3A), which is a common feature of

plants from all five populations. Therefore, the abaxial

leaf side is grayish-green in color. The plants from the

Eumediterranean populations, namely from the local-

ities near Budva and Krasic i, as well as from Pelopon-

nesus in particular, are characterized by conspicuously

thick indumentum (Fig. 4). In contrast, the adaxial leaf

side is always covered with sparse hairs rendering a dark

green color to this side (Fig. 3E and Fig. 4).

The cuticle on the leaf adaxial epidermis is thicker

than that of the abaxial epidermis in plants of all the five

populations studied. Besides, the outer epidermal cell

walls are thickened, particularly in the adaxial epidermis

occupying 2/3 of the cell lumen. The plants of the sub-

Mediterranean populations (from the gorges of Cijevna

and Moraca) are characterized by larger adaxial

epidermal cells in respect to those of the plants of

Eumediterranean populations (Fig. 5).

Anticlinal walls of the adaxial and abaxial epidermal

cells are almost straight in the plants from the localities

near Budva and Krasic i (Fig. 6B), or slightly undulate,

as in the plants from Peloponnesus and from theMoraca and Cijevna canyons (Fig. 6A). On the outer

periclinal walls of the abaxial epidermal cells larger or

smaller cuticle wrinkles are formed.

The leaves are always hypostomatic; the stomata are

more or less raised (Fig. 7C) above the epidermal cells, of

diacytic and anomocytic type (Fig. 7A). Their frequency

varies from 129 to 300per mm2. The highest number of

stomata are present in the plants from Krasic i

(186300 permm2), and the lowest in those from the

Moraca canyon (129186 per mm2) (Fig. 8). The stomata

are usually encircled by the glandular hairs (either peltate

or capitate), thus being partially covered with the

subcuticular spaces of the secretory cells (Fig. 7BD).

Leaf thickness (Fig. 9) of all plants studied ranged

between 210 and 440 mm, being the thickest in the plants

from the canyon of Cijevna (267440 mm).

The mesophyll is clearly differentiated into palisade

parenchyma and spongy parenchyma; the ratio of these

two photosynthetically functional mesophyll tissues is

generally 1.4:1, except in the plants from the locality

near Budva, being 2:1 (Fig. 9).

The palisade parenchyma, just below the upper

epidermis, consists of 23 rows of elongated and densely

arranged cells, which gradually shorten going towards

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Fig. 2. Teucrium flavum A, indumentum of glandular (g) and

non-glandular (h) hairs on the lower leaf side. (SEM) B, peltate

(p) and capitate type I (k) hairs. C, capitate hair type III

(SEM). D, Paradermal view, peltate (p) and capitate type I (k)

hairs.



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the spongy parenchyma. The anticlinal walls of the

palisade cells are almost always undulate. The cells of

spongy parenchyma are usually irregularly shaped, but

with relatively small intercellular spaces (Fig. 10A, B).

Even in the leaves of the plants from Peloponnesus,

which are smaller and less thick, the palisade parench-

yma is the thinnest but still densely packed into 23

layers, which is always the case in the plants of all the

populations studied.

In the leaf cross-section, a large number of vascular

bundles, situated in the central region of the mesophyll,

and only one main vascular bundle, developed in the

leaf midrib, are observed. Large bundle sheath cells

enclose the vascular bundles.

Stem shape and anatomy

T. flavum is an evergreen, branchy, semi-ligneous

shrub. In general, the resemblance of the external

morphology of the stem of all different populations is

obvious. In all the populations studied, the stem height

was between 40 and 70 cm, and a basal ligneous part is

clearly developed and reaches the length of up to 30 cm.

However, slight differences could be observed between

the population groups growing in very different

ecological conditions. In the individuals from Eumedi-terranean populations the height of the shrubs usually

varies in between 40 and 45 cm. The internodia are very

short and dense, so that the leaves overlap each other.

Contrary to them, the shrubs of the sub-Mediterranean

populations reach a height of over 60 cm, having longer

internodia; therefore their leaves mostly do not overlap.

The herbaceous stem of T. flavum specimens is more

or less square-shaped (in the cross section), firm,

particularly in the plants from the localities near

Budva and Peloponnesus, as well as from the Cijevna

canyon (Fig. 11A). Seldom, as in the plants from the

localities from the Moraca canyon it is slightly rounded

(Fig. 11B). The stem is well covered with epidermis, and

the thick cuticle, permeated by wax deposits and

glandular (peltate and capitate) and non-glandular

hairs, is arranged in a similar way as in the leaves.

Scattered stomata are slightly raised above the level of

the surrounding epidermal cells.

The stem cortex is differentiated into two to three

layered subepidermal supporting tissues, collenchyma,

and several layers of thin-walled parenchymatous cells

with prominent intercellular spaces. The collenchyma is

discontinuously distributed in the peripheral part of the

stem, forming thick projecting strands particularly in the

stem corners.The vascular tissue commonly forms a cylinder

between the stem cortex and the pith, consisting of

collateral vascular bundles separated by interfascicular

parenchyma. Conspicuous cups of sclerenchymatous

fibres are present above the phloem, being particularly

large below the stem corners. These fibres are more

developed in the vascular cylinder of plants from the

localities of Moraca and Cijevna canyons as well

as in those from Peloponnesus. However, in the stem

of plants from the other two populations there are o

nly 23 sclerenchyma cells above the phloem elements.

The correlation coefficient of the cortex and the whole

stem diameter ranges from 0.226 (Krasic i) to 0.343

(Cijevna).

Multivariate analysis of the morpho-anatomical

characters

By PCA it could be shown that the structural

variability of the populations studied is extremely

complex, since the first three axes comprise only

47.58% of total variability. By MANOVA statistically

significant differences between all populations were

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Fig. 3. Teucrium flavum A, indumentum on the lower leaf side(SEM). B, three-cellular hair. C, bicellular hair. D, wart-like

structures on the surface of the non-glandular hairs (SEM).

E, indumentum on peeled upper epidermis.



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established. It should be pointed out that the most

important characters in structural differentiation are

those related to leaf shape, stem anatomy, indumentum,

and leaf anatomy features in this order of significance

(Table 2).

DCA of the populations studied of T. flavum

has shown that the Eumediterranean (Peloponnesus,

Krasic i, Budva) and sub-Mediterranean (Moraca,

Cijevna) populations represent two morphologically

almost completely separate groups. On the first two

axes, the populations from Peloponnesus and Budva

stand completely separated from the sub-Mediterranean

populations. The population from Krasic i shows

(Fig. 12) transitional characteristics between the

Peloponnesus and Montenegro sub-Mediterranean

populations, as it was the case also in the PCA analysis.

Morpho-anatomical separation between Mediterranean

and sub-Mediterranean populations is clearly observed

also on the basis of overall Mahalanobious distances

(Fig. 13).

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Fig. 4. Box and whisker plots of basic statistic parameters of indumentum.

Fig. 5. Box and whisker plots of basic statistic parameters of epidermis.



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Discussion

The analyzed populations of the species T. flavum

inhabit the Mediterranean area on terra-rossa (red

soil) substrate, which develops on porous limestone. The

species grows within the maquis-garrigue vegetation of

different stages of progression and regression, undervarious Mediterranean bio-climate conditions perhu-

mid Mediterranean Adriatic, arid Mediterranean Ae-

gean and perhumid sub-Mediterranean Adriatic climate.

The resemblance of plants from different populations is

obvious, even at first sight, due to the similar general

habit, i.e., of quite a similar external morphology of the

stem and evergreen leaves. It is rather important to

stress this uniformity of the species T. flavum that

contrastes to the extreme morphological heterogeneity

that is present within the whole genus Teucrium. A

detailed growthform analysis of Teucrium have shown

significant morphological differences between shrubs,

semi-shrubs and perennial and annual herbs, especially

in regard to the extension and volume of lignification, as

well as with respect to the existence or the lack of

sclerenchyma elements in the cortex. Some of these

features can be used taxonomically on the level of

sections and species groups (Ka stner, 1978, 1979,

1981, 1986).

The macromorphological similarity of the stems and

evergreen leaves of T. flavum populations might be

assumed as a strong indication of structural stability and

some kind of morpho-anatomical conservatism of this

ancient Mediterranean xerophyte. However, this phy-

siognomic uniformity obviously is combined with eco-anatomical differentiations of leaves and stems of T.

flavum populations which thrive both in sites with

summers not particularly dry, and in those with a

pronounced summer drought.

In general, the evergreen leaves of T. flavum are

xeromorphic, moderately to significantly thick, tough

but not flabby neither rigid nor hard. In the Mediterra-

nean vegetation there is a large number of xerophytes

with such leaves, commonly known as malakophyllous,

notably within the genera of Cistus, Rosmarinus,

Thymus, etc. (Breckle, 2002; Kummerow, 1973).

The prominent xeromorphic features of the T. flavum

leaves are: simple form and relatively small size, dense

indumentum, especially on the lower side where a high

number of stomata are also located. The smallest leaves,

having a reduced external surface and mesophyll

thickness, are found in plants from the Eumediterra-

nean, Peloponnesian locality. In contrast, the thickest

leaves with the largest lamina surface area have the

plants from the sub-Mediterranean locality in the

canyon of Cijevna.

A dense and complex indumentum, composed of

glandular and non-glandular hairs, covers the lower

leaf side, shielding stomata and thus advantageously

ARTICLE IN PRESS

Fig. 6. Teucrium flavum paradermal view A, undulate anticli-

nal walls of the upper epidermal cells of plants from Moraca.

B, straight anticlinal walls of the upper epidermal cells of

plants from Budva.

Fig. 7. Teucrium flavum A, anomocytic (a) and diacytic (d)

stomata. B, stomata encircling by the glandular hairs or

glandular hairs encircling stomata. (SEM). C, highly raised

stomata and cuticular striae. (SEM). D, peltate hair around

the stomata (SEM).



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reducing transpiration loss. Stomata and glandular

hairs are very closely related, meaning that the stomata

are surrounded by glandular hairs or glandular hairs

are surrounded by stomata. In any case, stomata are

partially or totally flanged by the large subcuticular

swellings of peltate hairs and/or secretory cells of the

capitate hairs. Since the protrusions of capitate secretory

cells have only a small storing space, there is a

continuous evaporation of essential oils (Werker et al.,

1985a, b). This renders the air near the leaf surface more

condensed thus providing a higher boundary layer

resistance to gas diffusion. Regardless of the small

quantity of essential oils (0.10.2%), which characterizes

the specimens of T. flavum, even their minimal presence

in the external secretory structures may be efficient in

reducing both transpiration and overheating (C orovic et

al., 1969; Todorovic and Stevanovic , 1994). Otherwise,

it is well known that all species of the genus Teucrium

are distinguished by only a low quantity of essential oils

(Kovacevic et al., 2001; Petric ic et al., 1993).

Beside essential oils, some other terpenoids, as well

as flavonoids and/or phenylcarbonic acids might be

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Fig. 9. Box and whisker plots of basic statistic parameters of mesophyll.

Fig. 8. Box and whisker plots of basic statistic parameters of stomata.



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produced by these glandular hairs (Wollenweber, 1984).

Terpene exudates are the resins that cover the surface of

the plant above-ground parts, while the flavonoids are

incorporated either into the resins or into the coating the

leaf surfaces of many plants from the semi-arid regions

(Kelsey et al., 1984; Wollenweber, 1984). It has been

reported previously that the resin content in T. flavum

leaves is about 1.03%, consisting of terpenes, another

phenolic compounds, and free flavonoids (Kovacevic et

al., 1998). All these mostly aromatic volatile compounds

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Fig. 10. Cross section of the leaf: A, from Krasic i. B, from Peloponnesus.

Fig. 11. Cross section of the stem: A, square-shaped stem. B, rounded stem.



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on the upper leaf side consisting of short and protruding

non-glandular hairs and of all the types of glandular

hairs mentioned, especially in plants from the Eumedi-

terranean populations, also have an important influence

on the spectral features of the leaves. Such structural

adaptations increase leaf reflectance, thus reducing solar

inception, heat load and therefore water deficit. This hasbeen reported for leaves of Mediterranean species from

the genus Cistus (Gausman and Quisenberry, 1990).

It is worth mentioning that the more dense indumen-

tum of leaves from the Peloponnesian population must

be regarded as a favorable adaptive modification which

helps in protecting the mesophyll from excessive water

loss and intense radiation in this particular hostile,

perarid Mediterranean environment.

More or less conspicuous xeromorphic characteristics

ofT. flavum, from different populations, are represented

by a relatively high number of stomata, ranging from

129 to 257 per mm2 in the plants from the sub-

Mediterranean sites to 143300 per mm2 in those from

the Adriatic coast and the Peloponnesus. A similar high

number of stomata was established also in the Apennine

populations of T. flavum, in which the number of

stomata varies from 168 to 258 per mm2 (Ka stner, 1979).

It is also a typical xeromorphism that the dense,

complex indumentum on the lower leaf side protects

stomata which, on the other side are somewhat raised

above the level of the epidermal cells.

Smaller and thick-walled epidermal cells on the upper

leaf side are a pronounced xeromorphic feature of the

Eumediterranean populations of the taxon, compared

with the two sub-Mediterranean ones. The anticlinalwalls of both adaxial and abaxial epidermal cells of

plant leaves from all populations studied are straight to

wavy, which is described as an other xeromorphic

feature (Fahn and Cutler, 1992).

A ratio between 1.4:1 and 2:1 of 24 layered palisade

parenchyma to 23 layered spongy parenchyma is

characteristic for plants from all the five populations.

The number of palisade layers is increased in the plants

from Eumediterranean populations, particularly in

those from the localities near Budva and Krasic i, but

also in those from Peloponnesus. Moreover, the palisade

cells of these plants are narrower and more compact. In

addition, in leaves of these groups of plants of spongy

cells can be found, which elongate in such a way that

they resemble palisade cells. A partial differentiation

into an isolateral mesophyll is asumed to be a strongly

xeromorphic character. Again, similar characteristics of

the palisade and spongy tissues were established also in

the Apennine populations of T. flavum (Ka stner, 1979).

The stems of the studied T. flavum populations are

also protected by a thick cuticle with waxy layers and

with a dense indumentum of the same structural pattern

as that of the leaves. The stem hairs are more protruding

and less intertwined than those on the leaves. The ratio

of the stem cortex to stem diameter ranges from 0.226 to

0.343, which is within the usual values found in

xeromorphic stems (Fahn and Cutler, 1992).

All the data obtained, particularly those subjected to

a comparative multivariant analysis of morpho-anato-

mical characteristics of the five populations from three

different climate variants, have shown that the speciesT. flavum has maintained quite a stable, conservative

morpho-anatomical structure. Such a substantial simi-

larity between different populations is also characteristic

of other ancient Mediterranean plants since their

adaptive structures evolved, in the first place, as the

consequence of severe summer drought and high

temperatures (Margaris, 1981). In all the localities, both

eu- and sub-Mediterranean ones (arid-Mediterranean

and perhumid-sub-Mediteranean), the plant popula-

tions of which have been studied, more or less

pronounced, longer or shorter intervals of summer

drought stress prevail. Inter-population differences refer

to small variations in leaf size, indumentum density,

number of stomata, thickness of cuticle and outer

epidermal cell walls, as well as to the number of the

mesophyll tissues layers. While all these anatomical

features are of the same pattern, they are clearly more

expressed in the Eumediterranean than in the sub-

Mediterranean populations.

Acknowledgements

The authors are grateful to Prof. Dr. Vladimir

Stevanovic , Institute of Botany and Botanical garden

Jevremovac University of Belgrade for useful advice

and valuable comments and to the Ministry for Science,

Technology and Development of Serbia (Project Nos.

1568 and 1505) for financial support.

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