Acta Ecologica Sinica 36 (2016) 246251

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Acta Ecologica Sinica

journal homepage: www.elsevier.com/locate/chnaes

Studies on some anatomical features of selected plant species grown in

sand dune areas of North Sinai, Egypt
Anwar A. Elkharbotly
Desert Research Center, Sand dunes Dept., Environment and Arid Lands Cultivation Division, Matariya, P.O. Box 11753, Cairo, Egypt

a r t i c l e

i n f o

Article history:
Received 17 August 2015
Received in revised form 17 March 2016
Accepted 18 March 2016
Keywords:
Anatomical adaptations
Palisade layer
multiepidermal layers
Cuticle
Spongy mesophyll
Periderm
Water storage cells
Arid environments
Native plants to sand dunes

a b s t r a c t
The present investigation aims at studying some anatomical features of some selected native plant species in arid
environments of sand dunes at North Sinai, Egypt. Plant samples were collected from three localities; Coastal
sand dunes of Balouza (Zygophyllum album, Zygophyllaceae; root, stem and leaf); sand sheets of El-Arish city
(stems of Anabasis articulata, Amaranthaceae and Salsola tetrandra, Chenopodiaceae) and El-Owga interdune
areas (Fagonia indica, Zygophyllaceae; stem and root, Zygophyllum album, stem). Anatomical adaptations in
leaves of Zygophyllum album include the presence of palisade layers on the adaxial and abaxial surfaces, thick cuticle layer cover the epidermis, spongy mesophyll and the presence of water storage cells. Stem anatomical adaptations in different plant species as general observations were the presence of thick cuticle, multiepidermal
layers, palisade shape chlorenchyma, patches of sclerenchymatous ber in the cortex and the precipitation of
raphid and druse crystals of different sizes in plant tissues. Root adaptations in Zygophyllum album and Fagonia
indica include the presence of periderm layers composed of compacted and elongated cells of different origins
and increase the number of small xylem vessels which can guarantee the continuity of water uptake from soil
in the case of xylem embolism.
2016 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

1. Introduction
Native plants to arid environments in sand dune areas are very important for sand dune stabilization and reducing wind and water erosion resulting from severe oods. Such plants have different
anatomical and physiological adaptations to maintain survive under adverse conditions of limited water resources and active sand encroachment. Hence plants can exhibit a quick growth development to
overcome being buried by sand accumulation. Substantial leaf loss and
more developed vascular are also noticeable and the presence of
water storage tissues in mesophyll cells to withstand drought, this is
consider as a prevalent character of xeromorphic leaves [31,33]. Plants
in such circumstances tend to reduce it by transpiring surface area by
means of substantial leaf loss. Therefore, plants with small leaves are
more common in dry habitats [8,2224]. A very common characteristic
of xeromorphic leaves is a lower surface area to volume ratio, thick cuticle and sunken stomata, thus reducing water loss [19,20,30]. The presence of a palisade layer on both leaf surface, together with a mesophyll
composed of smaller cells and reduced intracellular spaces is reported
to be a characteristic of xerophytic species [9,25]. The increase of mesophyll thickness enhances the photosynthetic capacity if it is

E-mail address: anwar_online@yahoo.com.

http://dx.doi.org/10.1016/j.chnaes.2016.03.004
1872-2032/ 2016 Ecological Society of China. Published by Elsevier B.V. All rights reserved.

accompanied by an increase in the number of chloroplasts exposed

near the surface area facing the intercellular spacing [21].
The presence of additional layers of palisade parenchyma at the expense of spongy tissue is also considered a way to increase the path of
water through intercellular spaces to reach stomata; this would be a
strategy to increase water use efciency (ratio of carbon dioxide xed
to water lost) [17]. Many plants in desert environments produce different shapes and volumes of crystals in plant tissues. Calcium (Ca) oxalates are among the most abundant crystals present in different plant
tissues, it is found as crystalline deposits [2,7,12,32]. The formation of
calcium (Ca) oxalate crystal is considered to be a high capacity mechanism for regulating Ca in many plants. Needle shaped raphides and multifaceted druse crystals are the two common types of crystals formed in
the plant tissues. [18]. In a study on four genera of the tribe Salsoleae,
Chenopodiaceae, crystals of calcium (Ca) oxalate are formed in Anabasis
articulata, they precipitated in epidermis, palisade shape chlorenchyma,
cortex and in the vascular cylinder and also they found bers in the cortex and in the vascular bundles [10].
Fibers are found in many plant tissues and in various organs of the
plant and vary in position, they are sclerenchymatous (thick-walled)
cells that form the bulk of mechanical or supporting tissue in the plants,
[29]. The chief function of the bers to the plant is to give it mechanical
strength and save the plant from the various stresses and strains of the
environmental factors e.g., strong winds. Their presence in the leaf gives

A.A. Elkharbotly / Acta Ecologica Sinica 36 (2016) 246251

it rigidity and prevents it from collapsing. Their presence on the surface

of seeds and fruits may help in dispersal by wind.
Another kind of a protective tissue called periderm, is highly developed in perennial roots [11]. Generally, it is not produced in the leaves
and in most of the monocot stems and roots, but it develops in majority
of woody dicots, gymnosperms and some herbaceous dicots called periderm which is developed by the activity of a secondary lateral meristem
and replaces the epidermis which is ruptured and destroyed by the
pressure of the increasing secondary vascular tissue and form phelloderm or cork layers. Phelloderm may arise from the permanent living
cells of the epidermis, hypoderms, cortex and the phloem cells (including the phloem ray cells). Its activity adds to the diameter of the stem
and root because cells divide in a tangential plane cutting of cells towards its inner as well as outer face consists of compactly arranged
thin or thick-walled cells, [29]. The present study aims at studying
some anatomical features of some selected native plant species, which
are promising in sand dune stabilization at three different geomorphological areas (Balouza, El Arish and El-Owga) at North Sinai, Egypt.

247

green then slides were mounted in Canada balsam and were examined
under light microscope then photographs were taken with camera xed
(MC 80) in the microscope (Zeiss, Germany, Standard 20).
3. Results
The examination of the native perennials anatomy yielded more interesting results about stem, leaf and roots of these plant species.
3.1. Stem anatomy
3.1.1. Anabasis articulata, Amaranthaceae
It is clear that the multilayered epidermis is covered by thin cuticle
layer then hypodermis is found and palisade shape chlorenchyma
ended by short cell chlorenchyma layer. It is obvious that there are
many small druse crystals in the epidermal cells, hypodermis and in palisade shape chlorenchyma. However, bigger druse crystals and tannin
cells are found in the cortex cells, (Fig. 1AB). Cortical and vascular bers are also presented, (Fig. 1CD).

2. Materials and methods

Plant samples for the anatomical study were collected in October
2010 from three localities; Coastal sand dunes of Balouza (Zygophyllum
album, Zygophyllaceae; root, stem and leaf), sand sheets of El-Arish city
(stems of Anabasis articulata, Amaranthaceae and Salsola tetrandra;
Chenopodiaceae), and El-Owga interdune areas (Fagonia indica,
Zygophyllaceae; stem and root; Zygophyllum album, stem).
2.1. Study area
Sinai peninsula is located in the far northeast of Egypt. It represents
about 6% of Egypt's area (61,000 Km2). It is characterized by the distribution of active sand dunes in the north coastal and the middle areas,
they elongated and directed from NNW to SSE with migration rate
ranged from 1.6 to 8.4 m/year [5,6]. Natural vegetation of different
plant species has an important role in stabilizing dune sand. Their survival and distribution depend upon their ability to withstand the
harsh environments through morphological, physiological and anatomical traits of these plant species and the amount of rainfall. Rainfall and
oods are the only sources of renewable water resources in Sinai Peninsula. Mediterranean climate is prevail in the northern parts of Sinai to be
close to the desert and semi desert climate to the south. Temperature is
hot in the northern areas or very hot with a higher temperature degrees
inland. During May/June to September/ October, the mean daily maximum temperature is 28 C to 37 C in the north, 31 C to 42 C near
the south coast and 35 C to 41 C inland. Minimum temperature degrees average between 20 C to 25 C in the summer. The amount of
rainfall in Sinai decreases from the northeast towards the southwest.
Highest amount was 304 mm at Rafah. The annual rainfall average is
about 120 mm/year along the Mediterranean Coast, it decreases in the
uplands to the south to about 32 mm/ year, [4].
Three localities were selected for the study area, two of them their
natural plant species are subjected to severe wind erosion and sand
drift processes in Balouza (31 1 49.70 N, 32 35 27.81 E) and El
Arish sand sheets (31 4 30.77 N, 33 50 21.86 E) and the third location at El-Owga (30 58 01.05 N, 33 56 25.09 E) in the path of oods
especially the severe ash ood of January 18, 2010, natural plants here
are subjected to severe water erosion.
2.2. Microtechniques
Johansen [16] method was used to prepare permanent slides. Plant
samples were immediately immersed in FAA and transferred to the histology laboratory of Desert Research Center (DRC), samples were
dehydrated in a graded ethanol series, inltrated, embedded in parafn
wax and microtome sectioned, and stained with safranin and light

3.1.2. Zygophyllum album, Zygophyllaceae

It is a common xerophyte belonging to family Zygophyllaceae, a
transverse section of the stem (Fig. 1EF) reveals the following structures; epidermis, it made up of a single layer of compactly arranged
cells. The cells are radially elongated and are covered with a thick cuticle.
Cortical parenchyma shrunk lead to irregular epidermis surface obtain ridges and furrows (Fig. 1E), which may be an anatomical adaptation to aridity and adverse conditions prevailed in the interdune of ElOwga region, this anatomical adaptation is not found in Balouza coastal
sand dunes may be due to high rainfall in the Coastal area.
Cortex is 1520 layers thick. Cortical and phloem bers are found. In
Balouza sand dunes, the same structures are found in the transverse section of the stem, except that the regular epidermal surface without shrunk
of Cortical parenchyma and the cortex is 810 layers thick (Fig. 1F).
3.1.3. Fagonia indica, Zygophyllaceae
It is clear that cross section of stem of Fagonia showed that the epidermis is covered with cuticle, and then cortex is 810 layer thick. Separated longitudinal patches of bers are found as a ring around the
vascular cylinder. Modularly rays are long and enclosed small vessels.
Pith occupies the center of the stem and consists of thin walled oval or
rounded cells with small intracellular spaces. Raphid crystals are
found in the cortex, (Fig. 1GH).
3.1.4. Salsola tetrandra, Chenopodiaceae
A transverse section of stem reveals the following structures; epidermis is consists of single layers of cells and is covered with thin cuticle
layer. Cortex is distinguished to collenchymatous cells 58 layer thick
and chlorenchymatous cells of 48 thick layer. Sclerenchymatous
patches of bers are spread in the cortex. Complete rings of external
and intraxylary phloem or internal phloem are present and the modularly xylem is found in-between (Fig. 1IJ).
3.2. Root anatomy
In Zygophyllum album, it is clear that a phelloderm (periderm) layers
comprised of are 1021 thick layers of compacted and elongated cells
arise from sub-epidermal cells, then the cortex parenchyma occupied
large area and is composed of large elongated cells contains many starch
grains (Fig. 2A). Fibers and raphid crystals are found in the cortex and
phloem (Fig. 2A). Many xylem vessels in different diameters are observed (Fig. 2CE). In Fagonia indica, It is obvious that the phelloderm
layers originate from bast bers obtained from the phloem. Successive
layers of suberized periderm of compacted cells are recognizable outside the stele (Fig. 2EF). Different xylem vessels are also observed
with tendency to more narrow vessels.

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A.A. Elkharbotly / Acta Ecologica Sinica 36 (2016) 246251

Fig. 1. (AJ), Stem cross sections of some plant species grown at sand dunes of north Sinai AD, Anabasis articulata, Amaranthaceae at sand sheets of El-Arish city(A and B sections show
multilayered epiderms and portion of cortex & C show portion of cortex and vascular bers, D show the elongated ray parenchyma (ERP), note stomatal canal (ST.C), hypodermis (HYP),
palisade shape chlorenchyma (PAL), cortex (COR), druse crystals (DC) with different size (small in the epidermal layers but big sizes in the cortex), raphid crystals, short chlorenchymatous
layer (SCL) ended the palisade, tanin cells (TC) and nally the vascular bers (VF); EF, Zygophyllum album (Zygophyllaceae) E; at El-Owga inland interdunes and F at coastal sand dunes of
Balouza. Note thick cuticle and suberized lower side of epidermal layer and cortex cell wall (arrows) also note the shrunked cortex in El-Owga due to dryness, GH Fagonia indica, IJ Salsola
tetrandra, p; pith. Bars correspond to 200 m.

3.3. Leaf anatomy

In Zygophyllum album, a transverse section of the leaf (Fig. 3AD) reveals that it is a typical xeromorphic leaf characterized by the presence
of a thick cuticle cover the epiderms cells and the presences of highly

organized palisade mesophyll which are arranged next to the upper

and lower epidermis leading to isobilateral anatomical structure enhancing photosynthetic capacity as it is accompanied by an increase in
chloroplasts, Lewis [17]. Next to the palisade layer, there are large
thin-walled colorless water storage cells (spongy cells) arranged to

A.A. Elkharbotly / Acta Ecologica Sinica 36 (2016) 246251

249

Fig. 2. AF root cross sections, AD; portion of cross section of root of Zygophyllum album at coastal sand dunes of Balouza, A; periderm (P) and cortex (COR), note that the periderm
originate from subepidermal cells and it is composed of compacted and elongated walled cells of 1522 thick layer. B; magnier of cortex cells shows starch grains (ST.G). C, xylem
vessels of different diameters; D, lignied vessel walls (LVW), xylem vessels (XV). EF cross section and portion of cross section of root of Fagonia indica at Elowga inland interdunes.
Note that the periderm (P) originates from the inner part of the bast bers (BF) near phloem. Bars correspond to 200 m.

form water storage tissue, which is a prevalent character of typical

xeromorphic leaf. Central and lateral vascular bundles are presented
in (Fig. 3A), small druse crystals are found near the lateral vascular bundles (Fig. 3D).
4. Discussion
The results obtained from this study showed that in Z. album, a typical xeromorphic leaf characterized by highly organized palisade mesophyll and thick cuticle covers the epiderms, thus reducing water loss
[19,30]. The presence of well-developed palisade tissue containing chloroplasts below the adaxial and abaxial epidermis improves photosynthetic efciency [9,13,15,21,27,34].

Large water storage cells with a sinuous cell wall form the water
storage tissue (spongy tissue) in the leaf, this is a prevalent character
of typical xeromorphic leaf, it improves plant water retention, water absorption and preserves wet-micro-environment for surrounding photosynthetic cells [28]. Storing large volumes of water in mesophyll cells
helps in restraining drought [31].
The presence of multilayered epidermis, hypodermis and palisade
shape chlorenchyma in stem of A. articulata may enhance photosynthetic capacity [13,27].
Anatomical traits in the stem of Z. album are thick cuticle layers covering the epidermis cells, thus reducing water loss [19,30]. Fibers are
form in the bulk of mechanical or supporting tissue in the plant, thus
it provides good support and avoids damage from high temperature,

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A.A. Elkharbotly / Acta Ecologica Sinica 36 (2016) 246251

Fig. 3. AD, T.S. and portions of T.S. of leaf of Zygophyllum album. A, the palisade layers in the adaxial and abaxial surface; UPAL; upper palisade, LPAL; lower palisade, central bundle sheath
(CBS) and lateral bundles sheath (LBS), water storage cells (WSC) and spongy mesophyll cells (SP.M) and thick cuticle layer (CU); B, abaxial leaf surface low density of palisade layers; C,
adaxial leaf surface show high density of Palisade layers (PAL), EP; epidermis, small druse crystals (DC); D, the central bundle sheath and surrounded cells, water storage cells (WSC) note
the sinuous cell walls (arrows) of the water storage cells. Bars correspond to 200 m.

intense radiation, mechanical damage of sandstorms, and water erosion

following to oods and increases drought resistance [14,29,34].
In El-Owga interdune elds, stem of Z. album exhibited cortical parenchyma shrunk lead to irregular epidermis surface have ridges and
furrows which is an anatomical responses water decit, thus reducing
water loss.
In stem of S. tetrandra complete rings of external and intraxylary
phloem exist in addition to the modularly xylem in-between. The internal phloem develops from the provascular tissue and is part of the vascular cylinder, this is primary in origin [29].
Anatomical traits in roots of Z. album and F. indica exhibit periderm
of different origins and are in agreement with that illustrated by [26].
The well-developed phellem layer prevents mechanical damage that resulted from windstorms, water erosion in the case of oods and high
temperature and water loss by reverse osmotic pressure [1]. Different
xylem vessels exist in Z. album and F. indica with tendency to more narrow vessels which can allow slow water rate, however, narrow vessels
are valuable for safety since they guarantee water transport and also
when larger vessels are embolised [3].
5. Conclusion
In North Sinai adverse environments, plant species grown in sand
dune area, have many anatomical traits in different plant organs to
withstand drought, dryness, sand accumulation and sand drift attack.
Anatomical traits in stems are the occurrence of thick cuticle and

thick-walled epidermis cell as well as on the presence of suberized

sub-epidermal layers, also patches of sclerenchymatous bers as
supporting and protective source, parenchyma cortex shrunk as response to drought resistance, and multiepidermal layer (hypodermis).
Anatomical traits in Z. album leaf is the presence of highly organized
palisade mesophyll lead to isobilateral anatomical structure and the occurrence of water storage tissues (spongy cells). Anatomical traits in
roots of F. indica and Z. album are the occurrence of periderm of different
origins; from sub-epidermal cells as in Z. album or from cortical bast
bers as in F. indica. The periderm is a wonderful protective layer from
either wounds or drought.
Many narrow xylem vessels are found in both of F. indica and
Z. album which are consider xeromorphic traits.
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