Research Article
Morphological Study of Salicornieae (Chenopodiaceae) Native to Iran
Department of Biology, Alzahra University, Vanak, Tehran, Iran
Maryam Keshavarzi
Department of Biology, Alzahra University, Vanak, Tehran, Iran
The tribe Salicornieae belongs to the subfamily Salicornioideae Kostel. (Chenopodiaceae Vent.), includes halophyte plants. These 5 genera and 6 species are distributed in different habitats of Iran (Hedge, 1997). Members of the tribe Salicornieae Dumort., are characterized by their distinctive reduced leaves, which may be modified to form an articulated, photosynthetic stem (de Frain, 1912). These specialized plants generally have spike-like compound inflorescences, comprised of paired cymules of tiny flowers that are sessile within succulent free or fused bracts (Kuhn et al., 1993). Each cymule has (1-) 3 (-12) flowers.
The Salicornieae are among the most salt-tolerant plant and frequently occur in saline areas associated with coast lines, tidal floodways and salt lakes (Wilson, 1980; Davy et al., 2001; Asri, 1998). These halophytes are globally distributed, being found on every continent with the exclusion of Antarctic (Kuhn et al., 1993). Reduced morphology of Salicornieae limits the availability of easily recognized diagnostic characters at the tribal and generic levels. Furthermore the Salicornieae exhibit considerable phenotypic variation at the population level (Wilson, 1980; Davy, 2001; Freitag et al., 2001) and taxonomic confusion is exaggerated by the occurrence of species complex (Wilson, 1980) and polyploids (Shepherd and Yan, 2003). The succulent vegetative morphology may also be modified when dried, limiting the use of herbarium material. As a result, the sub familial and inter-generic relationships of the Salicornioideae are not fully clarified (Shepherd et al., 2005).
Although few vegetative and floral features are diagnostic in the Salicornioideae, seed characters have been recognized as potentially useful at both the generic and specific levels (Wilson, 1980). In some respects mature fruits and seeds of the Salicornioideae are more convenient to use as taxonomic characters than vegetative and floral features. They are less inclined to exhibit variability in the field, are frequently retained on perennial plant for months or even years and are likely to remain relatively unmodified upon drying (Shepherd, 2005).
There have been few global taxonomic treatments of the Salicornieae (Kadereit et al., 2003) and to our knowledge there has been no detailed survey of examining morphological characters of the tribe in Iran. The populations of tribe Salicornieae in Iran are studied for the first time.
In this study 46 Accessions of different salty marshlands of Iran were collected (Fig. 1 and Table 1). At collecting site altitude from sea level were measured and soil sample were gathered. Stomata were taken from fresh material. We use methyl green for studying this part. Seeds were gathered from dried specimens. Seed length and width were measured by digital caliper for 50 seeds per species. Seed coat ornamentation was studied by SEM (JEOL model JXA-140).
Fig. 1: | Distribution map of accessions of the tribe Salicornieae in Iran |
Pollen grain gathered from fresh flowering taxa, were studied without acetolysis. Pollen diameter was measured for 100 grain of each accession (by light microscopy). Observed morphological characters and their states are shown at Table 2. Soil Electric conductivity was evaluated by Electrolytic Conductivity measuring set model MC-1-Marv. All collected samples are deposited at Herbarium of Alzahra University.
Ecological features: Members of tribe Salicornieae are found in soils with electric conductivity from 17 to 150 Mm cm-1 (Table 1). The highest electric conductivity (150) belongs to a population of Salicornia europaea from western coast of Uromiyeh Lake (Azerbaijan). The lowest electric conductivity (17) belongs to populations of Salicornia europaea and Halocnemum strobilaceum from Khajeh salt mine in Azerbaijan. As a whole Salicornieae populations of Iran are found in a wide range of soil EC.
Plants of this tribe are found in a wide range of altitude (0-1600) from sea level in Iran (Table 1). Except Arthrocnemum macrostachyum which is limited to Persian Gulf Coast, at south of Iran, other taxa of central parts of Iran and Azerbaijan are distributed at different altitude till 1600 m. Halocnemum strobilaceum are distributed in disturbed salt marshes, the coast of salty lakes and rivers and make a great patches of vegetation. There are no other plants, where Salicornieae members grow in Iran. In western coast of Uromiyeh Lake, Coast of Talkheroud River and Mighan desert we can visit large marshes of Halocnemum strobilaceum. Populations of Halostachys belangeriana are also take part in making large patches of vegetation in coast of salt marshes and salty rivers and in the rivers estuaries. Populations of genus Salicornia comprise the first band of vegetation near salty rivers and lakes. After this band there is a layer of Halconemum strobilaceum. Members of Salicornieae are found in different salty habitats of Iran (Fig. 2).
Macro morphology: We have studied all macro morphological characters for 64 accessions. We have put the average values of each taxon in Table 3. Some no variant characters as articulated stems, phyllotaxy, number of flowers, perianth parts and stamens were eliminated. The most variation is shown in length and diameter of inflorescence parts and bract shape.
Micromorphology: Pollen grains were studied by light microscopy. We found that all pollen grains are spherical (Fig. 3). Pollen grains of this tribe were all polypantoporate although they show some differences in their diameter (Table 4).
Seeds of members of tribe Salicornieae in Iran are very different from each other. Seeds are globular and elliptical. Their color is from pale yellow-brown to dark brown.
Table 1: | Character of sampled accessions of tribe Salicornieae native to Iran |
Studying seeds with stereo microscopy we found that they have some differences in their seed coat ornamentations so we use Scanning Electro Micrographs to study these differences. As it could be seen in Fig. 4 and 5 ornamentations of these taxa are in form of tuberculate (Arthrocnemum macrostachyum), Granular (Halocnemum strobilaceum) and smooth (Halostachys belangeriana). Two species of Salicornia show some differences in distribution patterns of seed coat hairs. These hairs are in form of hooked or smooth (Fig. 4 and 5). Seeds length and width and the ratio of these characters show differences through members of this tribe in Iran (Table 4).
Epidermis which covers the stems of taxa was studied. We found that Stomata distribution pattern is of anemocytic type. Some characters as Frequency of stomata per leaf area, Length and width of guard cells and features of epidermis cell walls show some differences (Table 5). The lowest stomata index is found in Microcnemum coralloides and the highest stomata Index is found in Holostachys belangerian. Different populations of Salicornia in Iran show the highest variation. There are some special papillae on the epidermis surface of Halostachys belangeriana, Arthrocnemum macrostachyum and Halocnemum strobilaceum. These papillae are absent in other Iranian members of this tribe (Fig. 6).
Fig. 2: | Members of tribe Salicornieae in different habitats of Iran A and B: Halocnemum strobilaceum, C and D: Salicornia europaea |
Fig. 3: | Pollen Grains of Salicornieae in Iran A; Salicornia europaea, B; Salicornia persica, C, D and E Halocnemum strobilaceum F; Halostachys belengeriana |
Table 2: | Evaluated morphological character of Salicornieae in Iran |
Table 3: | Micromorphological characters of the Iranian Salicornieae |
+: Present; -: Absent |
Table 4: | Results of studying pollen grains and seeds in members of tribe Salicornieae in Iran |
Table 5: | Stem epidermis characters in members of tribe Salicornieae in Iran |
Fig. 4: | Scanning electron micrograph of salicornieae seeds of Iran showing seed coat ornamentations. Arthrocnemum macrostachyum (A and B); Halocnemum strobilaceum (C and D); Halostachys belangeriana (E and F) |
Fig. 5: | Scanning electron micrograph of salicornieae seeds of Iran showing seed coat ornamentations of Salicornia europaea (A and B) and S. persica (C and D) |
Fig. 6: | Stomata distribution pattern in members of tribe salicornieae in Iran A and C; Salicornia persica, B; Salicornia europaea, D; Halocnemum strobilaceum, E; Halostachys belangeriana, F; Arthrocnemum macrostachyum |
In this project macro and micro morphological characters were studied. The values of characters in separating taxa of this tribe in Iran were evaluated. Results show that characters as vegetative form and duration of life, arrangements of flowers in inflorescence and bract shape are diagnostic. Seed coat ornamentation is also important and all these can be used in preparing an efficient identification key for members of this tribe in Iran:
1 | a. | Annual herb, woody at base or not2 |
b. | Perennial herb, woody at base4 | |
2 | a. | Small plants, not branching, 5-10 cm height, Flower with linear arrangement in inflorescence, Seed coat vesiculate Microcnemum coralloides. |
b. | small herb to large bushes, branching, 8-50 cm height, Flowers with triangular arrangement are immersed in inflorescence, Seed coat with Hooked hairs.3 | |
3 | a. | Inflorescence branches 3-5, middle flower doesnt exceed the upper segment, Rectangular, Seed length 0.7-1.2 mm. Salicornia europaea. |
b. | Inflorescence branches 5-8, middle flower attached to the upper segment, with truncate end, pentagonal shape, Seed length 0.7-1.6 mm.Salicornia persica. | |
4 | a. | Small branching shrubs, Having opposite globular buds, yellow to green, Inflorescence without pedicel, with peltate bracts, Seed coat ornamentations granular H. strobilaceum. |
b. | Big branching shrubs, without opposite globular buds, glucose, Inflorescence pedicelate, without peltate bracts, Seed coat ornamentations is not granular5 | |
5 | a. | Bracts ob-pyramidal, not attached to each other, Flower arrangement linear, free, Stamens are not exerted, Seed coat almost smooth H. belangeriana |
b. | Bracts cup shape, attached to each other, Flower are immersed in inflorescence axis, free, Stamens are exerted, Seed coat tuberculate A. macrostachyum |
Present study shows that there is a very low variation in populations of Halocnemum strobilaceum and Halostachys belangeriana in Iran where there is a very high variation in morphological features of populations of Salicornia especially S. europaea. It seems common and general methods of morphological studies are not capable of revealing this kind of variation, so it is better to use molecular approaches for evaluating the genetic variation in this taxon for future studies.
Vegetative characters are not sufficient to separate these taxa so the necessity of using features of reproductive parts is distinct. Seed characters which are less affected by climate and habitat conditions provide very useful characters in this tribe.
Our results of studying seed coat ornamentations are in congruence with Shepherd et al. (2005) although we have not such high species richness in this tribe in Iran. It seems Seed coat features are more efficient in separation of Genus in this tribe. Results of studying pollen grains of tribe Salicornieae are in congruence with Akhani (2003), he believes pollen grains of Salicornia persica is larger than S. europaea due to the polyploidy in this species.
Due to the wide distribution of steppe region and salty soils in Iran and the wide range of salt tolerance of members of Salicornieae, it seems that they are good choices for desert improving and management and also as fodder supply. In traditional medicine of Iran, Salicornia has also an edible and officinal importance.
We thank Prof. P.G. Wilson for his guidance on morphological features and Dr. Phil Davidson and Farzaneh Zoie for their helps and co-operations.