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DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
1826
Revue Agrobiologia
www.agrobiologia.net
ISSN (Print): 2170-1652
e-ISSN (Online): 2507-7627
COMPARATIVE ECO-BOTANICAL ANALYSIS OF PISTACIA LENTISCUS L. IN
ALGERIA THROUGH MORPHOLOGICAL AND ULTRA-STRUCTURAL MARKERS
RELATED TO LEAVES AND STOMATA
DOGHBAGE Abdelghafour 1, 2*, BELHADJ Safia 3, DERRIDJ Arrezki1, MEVY Jean Philippe4, GAUQUELIN
Thierry4, MERDAS Saifi2, TONETTO Alain4 and FOULLA HASSEN Feriel3
1 Faculty of Biological and Agronomic Sciences, Mouloud Mammeri University BP 17, Tizi-Ouzou, Algeria.
2 Center of Scientific and Technical Research on Arid Regions CRSTRA. BP 1682, Biskra, Algeria.
3 Institute of Agropastoralism, University of Djelfa, Cité Aïn Chih, B.P. 3117. Djelfa 17000. Algeria.
4 CNRS, IRD, Institut Méditerranéen de Biodiversité et d'Ecologie marine et continentale IMBE, Aix-Marseille Université, Avignon
Université, CS 80249, Case 4, 13 331 Marseille cedex 03.
Reçu le 07/12/2019, Révisé le 20/05/2020, Accepté le 28/05/2020
Abstract
Description of the subject: In this study, we compared the morphological and ultra-structural characters of Pistacia lentiscus
L. leaves (epidermis, stomata, trichome and wax) belonging to three populations from Northern Algeria ( Djelfa, Médea and
Tizi-Ouzou).
Objectifs: This study aims to establish an analysis of the inter-population variability of Pistacia lentiscus in the purpose of
identification and knowledge of this species. Despite the ecological and economic features of this species, it remains neglected
in the restoration of preforest and forest ecosystems. Besides, it is important to understand the strategies developed by this
species according to environmental drivers including altitude and aridity.
Methods: We assessed 14 quantitative and qualitative morphological characters: related to leaf size, number of leaflets, petiole,
stomata size, stomata density in abaxial and in adaxila face of the leaf. In addition, the leaf epidermis and stomata were observed
under the scanning electron microscope (SEM).
Results: The statistical analysis and scanning electron microscopy observations allowed the separation of the studied
populations according to the studied variables and the climatic conditions. The dimensions of the leaf and the terminal leaflet,
the number of pairs of leaflets, trichomes occurrence, the dimensions, density, shape, and distribution of the stomata are the
most discriminating characteristics.
Conclusion: This approach allowed highlighting new characteristics in species studied such as wax and glandular trichomes
occurrence on the leaflets, sunken stomata in the epidermis. These characteristics may afford an initial screening method for
classifying species of the genus Pistacia in Algeria.
Keywords: Pistacia lentiscus; variability; ultrastructure; epidermis; leaf; stomata; adaptation; aridity
ANALYSE ECO-BOTANIQUE COMPARATIVE DE PISTACIA LENTISCUS L. EN
ALGÉRIE PAR LE BIAIS DE MARQUEURS MORPHOLOGIQUES ET
ULTRASTRUCTURELS FOLIAIRES ET STOMATIQUES
Résumé
Description du sujet : Cette étude se propose d’identifier trois populations Algérienne de Pistacia lentiscus L. (Djelfa, Médéa
et Tizi-Ouzou) dans leur milieu naturel et ceci, en se basant sur des caractères morphologiques et ultra-structurels foliaires
(épiderme, stomates, trichomes et cire).
Objectifs : Cette étude vise à établir une analyse de la variabilité inter-population de Pistacia lentiscus dans le but d’identifier
et de mieux connaitre l’espèce qui reste méconnue en Algérie et par conséquent, très peu employée dans la préservation des
écosystèmes forestiers et pré-forestiers malgré ses intérêt, aussi bien écologique qu'économique. Elle permet également de
comprendre les stratégies développées par cette espèce dans des habitats aux conditions extrêmes, notamment l’altitude et
l’aridité.
Méthode : 14 caractères morphologiques quantitatifs et qualitatifs ont été mesurés pour les feuilles et les stomates. En plus de
ces caractères, d’autres observations ont été effectuées pour les surfaces foliaires et les stomates sous microscope électronique
à balayage (MEB).
Résultats : Les analyses statistiques et les observations au microscope électronique à balayage ont permis de séparer les
populations étudiées selon les variables étudiées et les conditions climatiques. Les dimensions des feuilles et des folioles
terminales, le nombre de folioles, la présence de trichomes, les dimensions, la densité, la forme ainsi que la répartition des
stomates sont les caractéristiques les plus discriminantes.
Conclusions : Cette approche nous a permis de mettre en évidence de nouvelles caractéristiques chez l’espèce étudiée, tel que
l’occurrence des cires et des poils glandulaires sur les folioles, de stomates enfoncés dans l'épiderme. Ces critères pourront être
ajoutés aux critères morphologiques utilisés dans la classification des espèces du genre Pistacia en Algérie qui peuvent donner
des résultats satisfaisants dans la lutte contre la désertification.
Mots-clés : Pistacia lentiscus ; variabilité ; ultrastructure ; épiderme ; feuille ; stomate ; adaptation ; aridité.
*Corresponding author: DOGHBAGE Abdelghafour, E-mail: doghbage_abdelghafour@yahoo.com.
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
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INTRODUCTION
The environmental conditions and their
variations directly affect plants, particularly
diversity, distribution and functional traits [1].
In response to these conditions, plants develop
adaptation mechanisms reflecting particular
morphological characters [2]. In general, water
stress is a limiting environmental factor for
plant development. This stress worsens in arid
semiarid and dry sub-humid areas. Furthermore,
individuals, populations do not passively suffer
the influence of environmental factors. They
present in varying degrees an ecological
plasticity allowing them to adapt to the temporal
and / or spatial fluctuations of the limiting
factors in the environments to which they are
attached. Hence, they develop regulatory
mechanisms that cause morphological and
physiological modifications that allow them to
maintain constant and optimal value their
internal conditions in the face of the variability
of the environment. Several studies have
initiated the relationship of environmental
conditions with plants using morphological
traits. Ait Said et al. (2011) showed in their
study that the aridity conditions affect the
variability of the morphometric traits of
Pistacia atlantica Desf. Many biometrics works
have been based on the study of leaf
characteristics.
Indeed, many authors explain the variation of
certain biometric characters by the influence of
the stationary conditions. We cite those of
Cedrus atlantica and Pistacia atlantica [3, 4].
Plants promote different functional traits in
order to minimize the impact of drought [5, 6].
In arid environments, the leaves of xeromorphic
plants are often smaller and covered with
trichomes and wax.
The density of waxes and trichomes is also a
characteristic influenced by ecological
conditions. Altitude and positive values of
minimum temperatures can play an important
role in their distribution and density on the
leaves [4]. On the other hand, little work has
been done on the leaf characteristics of Pistacia
lentiscus. Although, contributions have been
made to the description of the morphology of
the leaf epidermis, leaves.
Only a few species of the genus Pistacia have
been examined with the light microscope and
very little with the scanning electron
microscope (SEM).
The genus Pistacia remains poorly defined
systematically and ecologically [7].
Moreover, very little information is available on
the leaf morphological characters of P. lentiscus
occurring in different climatic regions in North
Africa.
In this context, it is important to use the
functional approach including foliar and
stomatal micro and macromorphological to
characterize Pistacia lentiscus. Pistacia
lentiscus. (lentisque pistachio) is a typical
Mediterranean thermophilic species; it is a
dioecious shrub with persistent paripinnate
leaves. This species is distinguished from the
two other spontaneous species of Algeria of the
same genus; P. atlantica Desf and P.
terebinthus L [7, 8, 9]. It can reach 3 m in
height, belonging to the family of
Anacardiaceae which consists of more than
eleven species [7] . The pollination is
anemophilous, the fruit is a drupe [8, 10]. P.
lentiscusis known in the Mediterranean
countries by its resin (putty) used since
antiquity for the manufacture of certain
products and the treatment of gastric diseases,
ulcers, bacterial infections and canker sores
[11]. The aqueous leaf extract of P. lentiscus is
widely used as a beverage in North African
countries and increasingly in the world for its
special health benefits [12]. In addition,
Pistatcia oil is widely recognized in the
Algerian traditional medicine[13]. These
species are adapted to climatic hazards and can
be used in the reforestation of eroded soils.
Pistacia lentiscus is one of those species with
great potential. Unfortunately, its use is often
hampered by insufficient or fragmentary
knowledge of its diversity, its ecology and the
techniques of its multiplication. P. lentiscus has
a wide geographical and bioclimatic
distribution, ranging from wetlands to arid
zones [14]. This elasticity is due to its capacity
to develop morphological and physiological
adaptation strategies with respect to different
degrees of water stress (reference). Particularly,
these adaptation strategies are related to
mechanisms based on stomatal control and
reduction of leaf area and size [15]. P. lentiscus
occurs in isolated stands or in association with
other species such as the Aleppo pine, the
Prickly Juniper, the carob tree, the olive tree, the
terebinth, the holm oak and the cork oak [16].
This species grows on different soil types in the
sub-humid and semi-arid climates [17].
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
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Our study is based on the morphological and
ultrastructural features of the leaf, which is the
most exposed organ of the plant to
environmental conditions; this study aims to
determine how the three populations of P.
lentiscus respond to climatic variations by their
micro and macromorphological traits.
Especially, the survey aims to elucidate the
effects of climatic variables on the
morphological and ultra-structural
characteristics of the leaves (epidermis,
stomata, trichome and wax) and the observation
of the leaf epidermis and stomata under the
(SEM) across a climatic gradient that includes
semi-arid climate, semi-humid climate and
humid climate.
MATERIAL AND METHODS
1. Sampling sites
The sampling sites of Pistacia lentiscus leaves
are situated according to a climatic gradient
south–northof Algeria (Fig. 1). We selected
three sites to assess the differences in
morphological and ultra-structural traits,
Taksebt (Tizi-Ouzou province), Cherrata
(Medea province) and Sidi Bayazid (Djelfa
province). We used the De Martonne aridity
climate index as an aridity gradient for the
choice of the sampling sites from semi-arid
climate to humid climate. - The site of Taksebt
(36.665° N, 4.116° E, altitude is 200 m a.s.l).
The climate data were obtained from the nearest
meteorological station of Tizi-Ouzou for the
period (1999- 2012), these data were provided
by the National Meteorological Office. The
climate of this site is humid with a temperate
winter. The average temperature is 18.30°C
with the highest value of 28.03°C recorded in
August and a minimum value of 10.11°C for
January. The rainy month was December with
127.55 mm, and the average rainfall was 780.13
mm. The climate is characterized by two
periods, a dry period between June and
September, and a humid period from October to
May.
- The site of Cherrata (36.177° N, 2.89° E,
altitude is 1040 m a.s.l). The climate data used
belongs to the nearest meteorological station of
Ben-Chicao. These data were issued from the
climate software New_Loc Clim: Local Climate
Estimator version 1.10 (http://www.
fao.org/nr/climpag/pub/en3_051002_en.asp).
The program includes the FAOCLIM database
of 28100 stations worldwide. The climate of this
site is humid with a hot winter. The average
rainfall was 615 mm, mostly occurring in
November, December and January. The average
temperature is 13.75°C.
Two periods characterize this site, a humid
period of 8 months from October to May, and a
dry period from June to September.
- The site of Sidi Bayazid (34.933° N, 3.383° E,
altitude is 1080 m a.s.l). The climate
information was obtained from the nearest
meteorological station of Djelfa for the period
(1984- 2013). The climate of this site is humid
with a temperate winter. The average rainfall
was 311.41 mm, with a maximum of 34.93 mm
recorded in May and a minimum of 9.59 mm
recorded in July. The average temperature is
14.73°C. The dry period extends from June to
October, and the humid period extends from
November to May. 2. Plant Materials
At each sampling site, ten trees were randomly
selected for each population. For each tree, 30
leaves were harvested; in total 300 leaves in
each sampling site and 900 leaves for the whole
study area. Sampling was performed between
June and September 2012.
The leaves were dried in the open air and kept
in paper bags in the laboratory for trait
measurements and analysis.
3. Traits measurement
We followed the method described in the
I.P.G.R.I [18], reference for biometric and
macromorphological measurements of the
leaves. Hence, seven quantitative
morphological characters were measured: (i)
leaf length (cm), (ii) leaf width (cm), (iii) leaflet
length (cm), (iv) leaflet width (cm), (v) petiole
length (cm), (vi) number of pairs of leaflets, and
(vii) ratio of the length to the width of the
terminal leaflet. We used the epidermal printing
method for biometric stomatal measurements.
This method involves printing or molding the
surface of the leaf epidermis on a colorless
adhesive tape. This adhesive tape is glued on a
microslide to count the number of stomata
under a light microscope (magnification × 40).
Stomatal size measurements (length and width)
were performed on the abaxial face of P.
lentiscus leaves. On the other hand, the stomatal
densities were evaluated on both sides. These
measurements were made using an optical
microscope equipped with a digital camera
connected to the computer, as well as the
software Motic Image Plus "version 2.0. For the
micromorphological study of leaf surfaces
(shape, distribution and position of stomata on
the epidermis, trichomes, waxes), we used a
scanning electron microscope (SEM) (PHILIPS
XL 30 ESEM) with a secondary electron
detector to characterize the microstructure of
our samples.
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
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Sample preparation for SEM observations was
carried out at the Mediterranean Institute of
Biodiversity and Marine and Continental
Ecology at Aix Marseille University.
4. Statistical analysis
Data were assessed with one-way ANOVA in
order to compare the differences between macro
and micromorphological traits in the three
populations. Tukey’s multiple comparisons
followed the analysis to separate means. We
retained statistical significant levels at p<0.05.
In addition, principal component analysis
(PCA) was performed to assess the
relationships between trait variables of different
populations. Statistical test and models were
performed using the SPSS software.
RESULTS
1. Macromorphological variability of the
leaves
1.1. The leaves
The dimensions of the leaves vary between 5 to
14.50 cm concerning the length (an average of
9.71 cm), and 2.2 to 12 cm for the width (an
average of 5.24 cm). The leaves are long (10.46
cm) and wide (5.33 cm) at Cherrata (C), shorter
(8.77 cm) and narrower (5.11 cm) at Taksept
(T). The leaves have between 4 and 16 leaflets
for all provenances, with an average of 9.92
leaflets (Table 1). ANOVA indicated that there
are significant differences between the three
populations of P. lentiscus in leaf length (F (2,
897)=163.9, p<0.001), and leaf width (F (2,
897)=4.52, p<0.05). The analysis of variance
showed that the number of leaflets was
significantly different for the three populations
(F (2, 897)=11.81, p<0.001). A Tukey post hoc test
revealed a statistically significant difference
between the three groups of sites concerning
leaf length. For leaf width and number of
leaflets, Tukey's test revealed two
homogeneous groups (Table 1). 1.2. The
terminal leaflet
32.77% of the leaves had the terminal
leaflet for the three populations studied,
20% in (T), 38.66% in (S) and 39% in (C).
Significant differences were recorded (F(2,
897)=6.41, p<0.01) for the terminal leaflet
length between the three population of P.
lentiscus. The same observation was
indicated by the ANOVA for the terminal
leaflet width (F(2, 897)=4.23, p<0.05), and
for the length/width ratio (F(2, 897)=13.65,
p<0.001). Tukey's post hoc test indicated
two homogeneous groups for three
mentioned traits (Table 1).
1.3. The petiole
The petiole length varied significantly
(F(2, 897)=34.7, p<0.001) between the three
stations. The mean value of petiole length
in (S) was 1.61 cm, whereas in (C) it was
1.65 cm, and 1.36 cm recorded in (T). The
comparison of the means with the Tukey
test reveals the presence of two distinct
groups (Table 1).
2. Comparative analysis of leaf epidermis
and stomatal characters
2.1. Density and size of stomata in the
epidermis
The mean of stomatal length recorded in (C) is
25.93 μm, and 29.46 μmin (S), and 26.14 μm
in (T). ANOVA indicated significant
differences for this parameter (F(2, 746)=87.87,
p<0.001), and Tukey's post hoc test showed two
groups. Whereas the mean value of stomatal
width reveiled significant differences between
the three stations (F(2, 746)=114.29, p<0.001), the
stomatal width was 19.71 μmin (T) and 23.27
μmin (S) and 20.80 μm in (C) (Table 2). For the
density, the values vary between 105.09 st/mm2
in (T) and 197.83 st/mm2 in (C), on the abaxial
face, and 0.33 st/mm2 in (S) and 3.97st/mm2 (T)
on the adaxial face (Table 2). ANOVA analysis
indicated significant differences (P< 0.001)
between the different populations of Pistacia
lentiscus concerning these variables (Table 2).
2.2. Distribution, position, form of stomata
The leaves are amphistomatic for the three
studied populations (the stomata are present on
the abaxial and the adaxial face of the leaf). The
numberof stomata on the abaxial face is higher
than to the adaxial face. Our results show that
the stomata are distributed over all abaxial leaf
surfaces for the three populations, while the rare
stomata of the adaxial face are distributed near
the main and secondary veins (Fig. 2). In this
study, the stomata are embedded in the
epidermis (S) while they are at the same level to
slightly embedded in the epidermis for the other
populations (C), (T) (Fig. 3). The stomata have
different shapes; they are elliptical in (S) and
(T) and sub-rounded in (C) (Fig. 3).
Principal component analysis (PCA) (Fig.
4A) separated the populations into three
distinct groups based on stomatal sizes
and densities. Axis 1 is determined by the
size of the stomata and explains 44.68 %
of the total variance, and axis 2 represents
the stomatal density and explains 29.38%
of the total variance (74.06%).
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
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The figure revealed a negative correlation
between leaf stomata dimensions, while
the number of stomata on the abaxial face
is positively correlated.
The projection of the variables related to
stomata traits (Fig. 4B) reveals an
association between traits of the same
population characterized by the
environmental conditions. The stomat
traits of Cherrata (C) are correlated
positively to the first axis. However, those
of Taksebt (T) are negatively correlated to
the same axis. The stomata traits of the
population sampled in Sidi Bayazid (S)
are correlated negatively to the second
axis.
2.3. Trichomes and waxes
Trichomes were observed in P. lentiscus with
low intensity, especially for the population (T),
SEM observations show the presence of two
types of trichomes on the abaxial and the
adaxial face of the leaves for all populations.
Glandular hairs scattered throughout the leaf
surface (abaxial and adaxial) and rarely at the
level of the midrib. On the other hand, the non-
glandular hairs are elongated and distributed
along the main vein (nerve hair), they are absent
on the leaf margin (Fig. 5). SEM observation
also allowed us to notice wax deposits on all
samples (Fig. 5). This observation was not
possible under the binocular microscope or
optical microscope.
Figure 1: The location of sampling sites (○) according to a climatic gradient, Taksebt (Tizi-Ouzou province)
humid climate, Cherrata (Medea province) semi-humid climate and Sidi Bayazid (Djelfa province) semi-arid
climate. The diagrams represent climate conditions for each sampling site (precipitation in a blue bar chart and
mean temperatures in orange squares).
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
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Table 1: Morphological characteristics of Pistacia lentiscus leaves from different sampling sites (M ± SD,R,CV)
Characters
Sidi bayzid (S)
Cherrata (C)
Taksept (T)
Leaf length (cm)
9.9±0.85 a***
7.8–12.10 (8.61)
10.46±0.76 b***
8.7–12.6 (7.27)
8.77±1.66 c***
5–14.5 (18.99)
Leaf width(cm)
5.27±0.82 ab*
3.5–10.1 (15.56)
5.33±0.89 a*
3.3–12 (16.75)
5.11±1.06 b*
2.20–8.6 (20.77)
Number of leaflets
10.32±2.03 a***
4–16 (19.7)
9.70±1.54 b***
5–14 (15.94)
9.75±1.61 b***
5–15 (16.56)
Terminal leaflet length (cm)
2.31±0.66 a*
0.7–4.4 (28.82)
2.37±0.58 a*
1,1–4,6 (24,56)
2.66±0.63 b*
1.1–4 (23.91)
Terminal leaflet width (cm)
1.02±0.44 a*
0.2–2,10 (43.38)
0.98±0.39 a*
0.5–1.9 (39.9)
0.84±0.28 b*
0.2–1.6 (33.89)
length / width ration of terminal leaflet
2.58±1.04 a**
1.16–8.5 (40.49)
2.66±0.85 a**
0.88–5.20 (31.95)
3.32±0.89 b**
1.5–6 (27.01)
Petiole length (cm)
1.61±0.44 a***
0.7–3.3 (27.30)
1.56±0.37 a***
0.8–2.7 (23.91)
1.36±0.37 b***
0.5–2.8 (27.49)
a,b, c Separation of groups of populations by the Tukey test (p< 0.05). Values marked with the same letter are not significantly
different. Mean: M; Standard deviation: SD.; Range: Min-Max; Coefficient of variation (%) CV.
Table 2: Stomata characteristics of Pistacia lentiscus leaves from different sampling sites (M ± SD, R, CV)
Characters Sidi bayzid (S) Cherrata (C) Taksept (T)
Length of stomata on the abaxial face (µm) 29.46±4.15 a***
12.71–42.67 25.93±3.17 b***
15.49–39.44 26.14±2.47 b***
17.49–31.21
Width of stomata on the abaxial face (µm) 23.27±2.76 a***
14.98–31.09 20.80±3.05 b***
14.40–37.74 19.71±2.23 c***
13.22–29.15
Number of stomata on the abaxial face
(st/mm2) 194.86±48.62 a***
78.95–321.05 197.83±50.67 a***
78.95–352.63 105.09±35.09 b***
47.36–236.84
Number of stomata on the adaxial face
(st/mm2) 0.33±1.53 a***
0–10.53 0.48±1.73 a***
0–10.53 3.97±4.67 b***
0–15.78
a,b, c Separation of groups of populations by the Tukey test (p < 0.05). Values marked with the same letter are not significantly
different. Mean: M; Standard deviation: SD.; Range: Min-Max; Coefficient of variation (%) CV.
Figure. 2: Scanning electronmicrographs of abaxial and adaxialleaf surfaces showing stomata
distribution: (A) and (B) midrib on the adaxial surface, (C) et (D) midrib on the abaxial surface.
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
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Figure. 3: Scanning electronmicrographs of adaxial leaf surfaces showing stomata position and shape
(A) (B) Sidi bayzid, (C) (D) Cherrata and (E) (F) Taksept.
Figure 4: Principal Components Analysis (PCA) of the investigated P. lentiscus populations and theirs
tomatal characteristics (SDAb: stomatal density in the abaxial face, SDAd: stomatal density on the adaxial face, SW:
stomata width, SL: stomata length).
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Figure 5: Scanning electronmicrographs of wax and different types of trichomes on leaf surface of P.
lentiscus (A) (B) ciliated hair, (C) (D) glandularhair and (E) (F) wax.
DISCUSSION
For the Macromorphological variability of the
leaves, we recorded a large interpopulation
variability between (T) on the one hand and (S),
(C) on the other hand for the majority of
quantitative variables measured. Barazini et al.
[19], in their study of three populations of
Pistacia lentiscus in Cyprus, Tunisia,
and Spain, reported a smaller leaf length (3-7.8
cm) compared to our results (5- 14.5 cm).
However, the work of Al-Saghir [10] reported
very similar values compared to our results
concerning the dimensions of the leaf and
terminal leaflet as well as the number of leaflets.
This heterogeneity can be justified by the
different environmental drivers especially
climatic conditions of the sampling sites.
Reduced leaf size is correlated with reduced
transpiration [20] , as aridity increases and leaf
size decreases.
This finding is contradicted by our results
where we recorded higher values in semi-
arid and semi-humid stations (S, 311.41
mm) (C, 615 mm) and lower values in (T,
780.13 mm) on the dimensional plan. We
find that climate is a determining factor
since the large values recorded for the size
of the leaves, number of leaflets as well as
for the length of the petiole. Other factors,
such as edaphic conditions, can decisively
influence leaf morphology. The presence
or absence of the terminal leaflet is
important in distinguishing species of the
genus Pistacia. According to our study,
the presence of the terminal leaflet was
recorded for all the studied populations.
Kafkas et al. [21], reported the presence
of a mixture of paripinnate and
imparipinnate leaves on the same tree.
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In addition, it is also possible to add the
difference of sexes between subjects
(trees). Most authors state that the length
of the leaves and leaflets of female
subjects is slightly higher than that of
males, this is consistent and demonstrated
for P. vera [22], P. terebinthus [21] and P.
lentiscus [19, 23]. Nevertheless, the
influence of the genetic factor is not to be
omitted [24]. For the leaf epidermis and
stomatal characters, Generally, little work
has been done on the comparative study of
species of the genus Pistacia
micromorphologically.Nevertheless, we
can mention the comparative study of the
micromorphology of the leaf epidermis of
eight populations of Pistacia atlantica
from Algeria [4, 25, 26]. The study of the
variability of leaf characteristics and
stomata of four species of the genus
Pistacia in Algeria [23], and the study
conducted by Ait Said et al. [27] on the
morpho-anatomical variability and the
terpene composition contained in the
leaves of Pistacia atlantica. The last study
demonstrated that the studied populations
exhibited very great macro and
micromorphological morphological
variability in the response of the aridity
gradient, both in the leaves and in the
stomata. Al-Saghir and Porter [28]
suggested that the distribution of stomata
could be related to the ecological
plasticity of Pistacia species on a wide
range of environmental conditions. In fact,
our samples were taken from different
bioclimatic stages, from semi-arid (S) to
humid (T), with annual rainfall ranging
from 311.41 mm (S) to 780.13 mm (T). In
addition, the altitude varies from 1211 m
(S) to 182 m (C). It should be noted that
Calamassi [29], indicated that forest
species of different origins are
characterized by high stomatal density and
have a better ability to withstand drought.
Indeed, Scuiller [30], reported that plant
species from dry habitats generally had
higher stomatal densities than species
from humid habitats.
Our study confirms this hypothesis, where
the two stations (S) and (C) with an
average rainfall of between 311.41 mm/ yr
and 615 mm / yr, have a high density of
194.86 st / mm2 and 197.83 st / mm2. On
the other hand, the station (T) which is
characterized by average precipitation
exceeding 780.13 mm/ year had the
lowest density of 105.09 st / mm2. This
characteristic seems to be one of the
features of Pistacia lentiscus under the
conditions of increasing aridity. Few data
are available regarding the position of
stomata in the epidermis, and our results
are the among the first data reporting this
feature for the studied species. Other
criteria, such as pubescence and the
presence of wax are commonly used in the
classification in the genus Pistacia are
also unstable [25], some families can be
easily identified by the presence of a
particular type of hairs. In other cases, the
hairs are important in the classification of
genera and species [31, 20]. In this study,
the leaves of P. lentiscus are pubescent at
the level of the main vein, the abaxial and
adaxial leaf surface. However, their
margins are not ciliate, which is consistent
with the results of Doghbage [23], where
the results showed the presence of
trichomes in P. lentiscus with a low
intensity unlike the leaves of other species
of the genus Pistacia.
CONCLUSION
The functional approach is suitable in providing
solutions on the distribution of organisms along
environmental gradients. This implies many
aspects as; the identification of the patterning
drivers of the assembly of communities, the
understanding of how those functioning are
reflected in ecosystems and how controls some
of the goods and services they provide to human
societies. This approach allowed us to highlight
new characteristics of the species studied, such
as the occurrence of waxes and glandular hairs
of the leaflets, stomata sunk into the epidermis.
These criteria may be added to the
morphological criteria used in the classification
of species of the genus Pistacia in Algeria.
DOGHBAGE et al. Revue Agrobiologia (2020) 10(1): 1826-36
1835
Acknowledgments
Our thanks go to the anonymous reviewers
for their corrections, and relevant
comments.
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