Next Article in Journal
The Phyloperiodic Approach Removes the “Cryptic Species” and Puts forward Multilevel Organismal Diversity
Previous Article in Journal
Mycorrhizal Fungi of Phalaenopsis japonica (Orchidaceae) and Their Role in Seed Germination and Seedling Development
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Current Status and Resources of Alhagi pseudalhagi (Fabaceae) in the Atyrau Region, Western Kazakhstan

by
Meruert Sagyndykova
1,*,
Akzhunis Imanbayeva
1,*,
Gulnara Gassanova
1 and
Margarita Ishmuratova
1,2
1
Laboratory of Natural Flora, Mangyshlak Experimental Botanical Garden, Aktau 010004, Kazakhstan
2
Department of Botany, Faculty of Biology and Geography, Karaganda Buketov University, Karaganda 100024, Kazakhstan
*
Authors to whom correspondence should be addressed.
Diversity 2024, 16(4), 219; https://doi.org/10.3390/d16040219
Submission received: 14 February 2024 / Revised: 3 April 2024 / Accepted: 4 April 2024 / Published: 5 April 2024

Abstract

:
Alhagi pseudalhagi, which grows in the arid zone of the Atyrau region, and an assessment of the current state of its raw material reserves were studied. Botanical characteristics, ontogenetic spectra, morphological indicators, productivity, areas of thickets, and reserves of raw materials of above-ground organs were assessed. The structural parameters of these populations in the Zhangyr and Coneu Rivers valleys, in the vicinity of Imankara Mountain, and on the Taisoigan sands were studied. It was established that the species composition of the populations includes 63 species from 54 genera and 30 families. The most common species include 49 species, which, according to their occurrence in populations of A. pseudalhagi, are distributed in the following classes: 17 species—class II (0–20%); 7 species—class III (41–60%); and 2 species—classes IV (61–80%) and V (81–100%). The maximum similarity in species composition was noted between populations in the Zhangyr and Coneu Rivers valleys. The highest morphometric indicators were observed among the population of the Coneu river valley, and the lowest are located on the Taisoigan sands. Analysis of the age spectra made it possible to determine that the populations in the Zhangyr and Coneu River valleys are characterized as young and those in the area of Imankara Mountain and on the Taisoigan sands as stable and middle-aged.

1. Introduction

Alhagi pseudalhagi (M. Bieb.) Desv. ex Wangerin (camel thorn or manna tree) is one of four representatives of the genus Alhagi Tourn. ex Gagnebin of the family Fabaceae Lindl. This herbaceous perennial has the particularly thorny characteristics of a subshrub, in addition to having a root system that penetrates deeply into arid soils. The main feature of its morphological difference is the high variation in plant height from 30 to 100 cm, which directly depends on the habitat [1,2].
A. pseudalhagi is used in clinical and folk medicine to treat diseases of the gastrointestinal tract, genito-urinary system, and liver, as well as colds and rheumatism, and is used as a choleretic, diuretic, and cleansing agent in the treatment of liver diseases and peptic ulcers. When applied externally, the decoction heals wounds [3,4]. The decoction and infusion of the leaves have bacteriostatic, astringent, hemostatic, choleretic, and wound-healing effects [5,6,7,8,9]. The decoction and tincture are used to treat inflammation of the colon and duodenum and the gall bladder, gastritis, and peptic ulcers, and are sometimes prescribed for colds and severe coughs, as well as for the prevention of dysentery. These medicinal properties make it possible for this plant to become the basis for the production of local domestic herbal medicines [10,11]. Based on the above-ground organs of A. pseudalhagi, a syrup has been developed for the treatment of colds and upper respiratory tract infections [12,13,14].
The four species of this genus are widely distributed from North Africa to Greece, through Western and Central Asia, to India and Northern China. In Central Asia, including on the territory of Kazakhstan in the arid zone, A. pseudalhagi is widely found [15].
A. pseudalhagi grows in most arid territories of Kazakhstan and forms extensive thickets in semi-deserts, deserts, dry foothills, and river valleys on clay, salt marsh, and sandy soils. Significant reserves have been formed in Almaty, Zhambyl, South Kazakhstan, Aktobe, and Atyrau regions [16,17,18,19,20,21].
Earlier, about 177 species of medicinal plants belonging to 118 genera and 46 families were found in this territory of the Atyrau region. These identified species are suitable for potential procurement of medicinal raw materials and include such species as Althaea officinalis L., Nitraria schoberi L. Artemisia terrae-albae Krasch., Glycyrrhiza glabra L., Anabasis aphylla L., Anabasis salsa (Ledeb.) Benth. ex Volkens, and others. One promising medicinal species is Alhagi pseudalhagi (M. Bieb.) Desv. ex Wangerin [22,23,24,25].
The environmental distribution of this species mainly includes dry steppes; clayey and gravelly semi-deserts and deserts; along the banks of rivers and canals; and in wastelands and fallow lands. Plant raw materials in the arid zone in Kazakhstan can be obtained both by growing industrial plantations and by organizing harvests from natural arid conditions [26,27]. However, similar work studying A. pseudalhagi in the Atyrau region and Kazakhstan has not previously been carried out [28,29,30].
Significant thicket areas are noted for A. pseudalhagi, and the range of this species is confined to steppe, semi-desert, and desert territories [31]. Preliminary field studies revealed the presence of thickets of A. pseudalhagi in the Mangystau region; large thickets were also identified in the Atyrau region in the vicinity of Mount Imankara; the floodplain of the Zhangir, Uter, Koneu, Krasny Yarik, and Aktolkyn rivers; in Aktailak; and on the sands of Toysaigan and Naryn [32].
However, there is a need for additional research to assess the suitability of A. pseudalhagi populations for exploitation, as well as to identify potential volumes of procurable raw materials. The aerial part of the plant contains phenolic compounds (phenolic carboxylic acids, flavonoids, proanthocyanidins, xanthones, coumarins, tannins, α-pyrones, diphenyl ethers, and naphthoquinones), alkaloids, terpenoids (mono-, sesqui-, and triterpenoids and polyterpenoids), fatty acids and their aldehydes, carbohydrates, and organic acids [33]. However, raw material reserves and procurement possibilities in the arid region of Kazakhstan have not been sufficiently studied. There is research on various environmental factors affecting the biological mass of plants and their genetic characteristics [34].
The study of the current state of a natural population of economically valuable A. pseudalhagi specimens with an assessment of the possibility of their practical application is motivated by priorities for preserving biological diversity in arid zones, thus expanding the use of traditional herbal medicines [35].
The purpose of this study is to analyze the current state of the A. pseudalhagi population in four locations on the territory of the Atyrau arid zone according to various parameters, to estimate the quantity of resources, identify the properties of the plant and the density of its distribution, and determine the composition of related species for obtaining medicinal raw materials. In addition, the morphological features of A. pseudalhagi population and distribution areas in the arid zone are studied, along with the age composition of vegetative and generative individuals located within various plant species communities.

2. Materials and Methods

2.1. Research Areas

The studied area belongs to the western part of Kazakhstan, which is a special territory with a relatively high concentration of biological diversity of various arid plant species, including those with medicinal properties. The arid Atyrau region is located in the extreme western part of Kazakhstan on the Caspian Lowland, northeast of the Caspian Sea. The surface of the region is flat; in the north of the region, there are small mountains. The climate is sharply continental, and extremely dry, with hot summers and moderately cold winters. This territory can be classified as an arid zone with unfavorable conditions for most species of medicinal plants, which in turn increases interest in this territory and its natural plant species [36,37].

2.2. Floristic and Population Analyses

The population analysis of the morphological properties of plants in ontogenesis was studied using the methodology of O. V. Smirnova et al. [38]. At the same time, the names of the plant species were verified according to the “Flora of Kazakhstan” [39], the “Illustrated Determinant” [40], the “Determinant of Plants of Central Asia” [41], and the International Index of Names of Electronic Databases [42]. The classification of life forms of species included in the population was estimated according to the method of I.G. Serebriakov [43]. Traditional methods of geobotanical survey using ecological and morphological indicators were used to describe populations. A. pseudalhagi individuals were counted by age groups, and floristic composition was described within 1 m recording sites [44]. Nomenclature of plants was determined according to POWO [45]. The similarity in floristic composition was estimated according to the Jaccard similarity index [46].
The frequency of occurrence of individual species in populations with A. pseudalhagi was estimated according to 5 classes: I—0–20%; II—21–40%; III—41–60%; IV—61–80%; and V—81–100%. When describing ontogenesis, we used the method of Komarov et al. [47]. The population type was determined according to the method of S.V. Fedorova [48]. The following age groups were considered: juvenile plants (j), immature plants (im), adult vegetative plants (v), young generative plants (g1), middle-aged generative plants (g2), and old generative plants (g3). Sprouts and senile individuals were not identified in the natural population at the time of the study.
During the study, four main comparative populations were selected from different geographical regions (mountains, coastal waters, and sands) in the Atyrau region: in the vicinity of Mount Imankara (population 1), in the valley of the Zhangyr River (population 2), in the valley of the Coneu River (population 3), and on the Taisoigan Sands (population 4). Details on these locations are presented in Table 1.
The locations of the studied population of A. pseudalhagi and the conditions of their existence in the arid conditions of the Atyrau region are presented in Figure 1.

2.3. Assessment of Plant Resources

Evaluation of above-ground organ resources was performed according to the method of Elzinga et al. [49]. In the study area, 10–15 survey plots with an area of 1 m2 were laid out, from which above-ground organs of A. pseudalhagi were cut at a height of 5–8 cm from the soil. The raw materials were air-dried and weighed. The areas of the thickets were calculated by multiplying the length and width of the thickets. Average yield data from 1 survey plot were recalculated per hectare (kg/ha). The exploitable stock was calculated as the product of yield per total area, and the volume of possible raw material collection was set as 40–50% of the exploitable stock.

2.4. Statistical Processing

Statistical processing of the results was carried out using the Statistics 10 program (StatSoft STATISTICA 10.2011) and the capabilities of the Microsoft Excel 10.1 program. Statistical processing was carried out by calculating the non-parametric Mann–Whitney test to determine the reliability of differences between the indicators of the floristic composition between populations, as well as between morphological indicators of the populations of the species under study.
Mathematical processing was performed according to the methods of Kuziev R.K. and Yuldashev G. et al. [50,51]. Statistical analysis of population dynamics varies depending on the constraints, which vary according to the standard deviation of the coefficient of variation, the mean value of the error, the degree of confidence, and the degree of precision.
A dendrogram was constructed using the PAST 4.03 program and unweighted pair group method with arithmetic mean (UPGMA) algorithm and Boot N:1000 [52].
To compare the results, a one-way analysis of variance (ANOVA) was used with a significant correlation found between the soil type and the main plant parameters in the population. When analyzing primary data, correlation coefficients were calculated using the statistics program R Studio (IDE) for Windows (R version 3.6.0, 2019). The average values of the main quantitative traits (plant height, cm; plant diameter, cm; number of generative shoots, pieces; number of individuals per 1 m2, pieces) of the four populations were grouped according to PCoA (principal component analysis). PCoA was performed using the Numerical Taxonomy and Multivariate Analysis System Version 2.1. (NTSYS-pc) program [53].

3. Results

3.1. Structure of the Populations of Alhagi pseudalhagi

For the first time, a comprehensive description is given of the structure of the population, species composition, and resources of A. pseudalhagi depending on the position of the relief. Data on the distribution of species according to ecological groups showed that in the population of plants with A. pseudalhagi, xerophytes (53.9%), mesoxerophytes (15.8%), and mesophytes (14.3%) dominate. This fact is also confirmed by the ratio of ecological groups of plants according to humidification conditions. For example, the largest number of species belongs to xerophytes, accounting for more than half of the species found, while other ecological groups occupy smaller proportions of the studied populations.
Population 1 (Limonium suffruticosum (L.) Kuntze—Alhagi pseudalhagi (M. Bieb.) Desv. ex Wangerin—Herbaxerophytica) is located in the vicinity of Imankara Mountain. The total projective cover (hereinafter referred to as the TCC) of vegetation is 40–50%. The relief is plain with slight differences in elevation, and soils are loamy and brown, with numerous outcrops of chalky rocks. The surveyed area is used for cattle grazing in spring. Vegetation consists of two tiers: shrub, 40–55 cm (Atraphaxis spinosa L.), and herbaceous, 15–35 cm. The basic summarized species in this population are Limonium suffruticosum, Alhagi pseudalhagi, Ephedra distachya L., Anabasis salsa (C.A. Mey.) Benth. ex Volkens, Atraphaxis spinosa L., Ferula nuda Spreng., Centaurea scabiosa L., Scabiosa isetensis L., Tanacetum santolina C. Winkl., Kochia prostrata (L.) Schrad., and others. In the described population, all age groups of A. pseudalhagi are present, with middle-aged generative plants being dominant. The status of population 1 can be characterized as stable and capable of self-renewal. Soil type: flat area in front of the chalk mountains of Imankara, with loamy, dry, grey-earth soils that are heavily gravelly and of a basic nature.
Population 2 (Alhagi pseudalhagiSalsola foliosa (L.) Schrad.—Limonium gmelinii (Willd.) Kuntze) is located in the Zhangyr River valley. The TCC is 75%. The soils are chestnut and loamy. The vegetation forms three tiers: woody, 120–150 cm (Elaeagnus angustifolia L.); shrub, 70–90 cm (Tamarix laxa Willd.); and herbaceous, up to 50 cm high. The following species are part of the population: Cynodon dactylon (L.) Pers., Salsola orientalis S.G. Gmel., Plantago major L., Trifolium fragiferum L., Polygonum aviculare L., Limonium gmelinii (Willd.) Kuntze, Echinochloa crus-galli (L.) Beauv., Xanthium strumarium L., Solanum dulcamara L., Potentilla spuria A. Kern., etc. The area is actively exploited for livestock grazing, which leads to the degradation of the vegetation cover; the degree of degradation is 50–55%. The population is normal, young, and dominated by pre-generative and young generative individuals. Soil type: the soil is light chestnut, loamy, and moist, without the presence of rocky elements. This area is flooded in the spring.
Population 3 (Alhagi pseudalhagiHerba varia) is located in the Coneu River valley. The TCC is 75%. Soils are light chestnut, loamy, and, in some places, salty. The vegetation is degraded by 25–30% due to active cattle grazing. The vegetation is composed of three tiers (one shrub, 60–70 cm high, and two herbaceous, 30–50 and up to 20 cm high). The following species were found in the population: Alhagi pseudalhagi, Tamarix laxa Willd., Salsola foliosa (L.) Schrad., S. orientalis S.G. Gmel., Persicaria amphibia (L.) Delarbre, Butomus umbellatus L., Plantago major L., Mentha arvensis L., Trifolium fragiferum L., Zygophyllum fabago L., Limonium gmelinii (Willd.) Kuntze, etc. Population 3 is composed of A. pseudalhagi of the young, normal type, with a predominance of young generative individuals. Soil type: the soil is light chestnut, loamy, and moist, without the presence of rocky elements. This area is flooded in the spring.
Population 4 (Alhagi pseudalhagiGlycyrrhiza glabra L.—Herbaxerophytica) is described on the Taisoigan sands. The TCC is 50–55%. The relief is flat; the soils are sandy, with clay outcrops in some places. There are traces of cattle grazing. Vegetation degradation of 10–15% is observed. The cover is composed of two tiers: high grass, 40–65 cm, and low grass, 15–25 cm. The species composition includes the following species: Euphorbia seguieriana Neck., Melica taurica K. Koch, Agropyron fragile (Roth) P. Candargy, Achillea micrantha Willd., Kochia prostrata (L.) Schrad., Glycyrrhiza glabra L., Carex physodes M. Bieb., Arnebia decumbens (Vent.) Coss. & Kralik, Limonium suffruticosum (L.) Kuntze, etc. Population 4 is normal, stable, and medium-aged, dominated by medium-aged generative plants. Soil type: typical sandy massifs, with wet loams at a depth of 40 cm.
When describing the population structure, we also considered the age spectra of A. pseudalhagi individuals. In populations of perennial plants, all individuals are characterized by a set of biomorphic traits that determine their age differentiation (Figure 2).
Thus, the analysis of age spectra showed that population 1 and population 4 have a middle-aged and stable status, and population 2 and population 3 are normal and young. These characteristics make it possible to recommend all studied populations for the procurement of raw above-ground materials.
Age structure is one of the most important traits of the population. It reflects the vital state of the species in the cenosis, as well as such important processes as the intensity of reproduction and the rate of generational change. It shows the ability of the population to maintain itself and the degree of its resistance to the influence of negative environmental factors, including anthropogenic impacts.

3.2. Floristic Composition of A. pseudalhagi Populations

As a result of the analysis of herbarium material collected during field studies, 63 species from 54 genera and 26 families were observed growing as part of populations with A. pseudalhagi. Systematic analysis showed that the leading families by species composition are Poaceae (12.7%), Asteraceae (12.7%), Chenopodiaceae (9.5%), and Fabaceae (9.5%) (Table S1). The four leading families include 28 species and 23 genera, representing 44.4 and 42.6% of the total floral composition, respectively.
A comparison of the species composition of the populations showed that the greatest number of species was recorded for population 1 (25), the minimum for population 4 (21), while populations 2 and 3 have the same quantitative composition (24 species each).
Significant degradation of vegetation cover in the valleys of the Zhangyr and Coneu Rivers due to anthropogenic pressure is noted, which is confirmed by a significant number of weeds and ruderal elements (Onopordum acanthium L., Xanthium strumarium L., Cynodon dactylon (L.) Pers., Polygonum aviculare L., Convolvulus arvensis L., Echinochloa crus-galli (L.) P. Beauv., etc.). However, grazing has no depressing effect on A. pseudalhagi, as this species is not typically eaten by domestic animals. The analysis of species according to occurrence showed that classes IV and V were noted only for Alhagi kirghisorum Schrenk and Limonium suffruticosum (L.) Kuntze (3.2% of the total number of species). Class III was assigned for 7 species or 11.1% (Artemisia terrae-albae Krasch., Salsola foliosa (L.) Schrad., Carex physodes M. Bieb., Euphorbia seguieriana Neck., etc.), and class II comprised 17 species or 26.9% (Artemisia arenaria D.C., Peganum harmala L., Xanthium strumarium L., Tamarix laxa Willd., etc.). The greatest number of species were in class I—49 taxa or 77.8% (Allium sabulosum Steven ex Bunge, Atriplex cana C.A. Mey., Salsola orientalis S.G. Gmel., Arnebia decumbens (Vent.) Coss. & Kralik, Onosma stamineum Ledeb., Alyssum lenense Adams, Trifolium fragiferum L., etc.). The analysis of life forms showed the predominance of herbaceous perennials (33 species or 52.4%), with the second position occupied by minor shrubs (15 species or 23.8%) and the third by semi-shrubs (9 species or 14.3%). Shrubs account for five species (7.9%) and trees for one species (1.5%).

3.3. Morphological Differences between Populations and Resource Potential of A. pseudalhagi

Morphological studies of various populations made it possible to determine that the range of A. pseudalhagi in the Zhylyoysky, Kzylkoginsky, and Kurmangazinsky districts of the Atyrau region differ in their systematic structure, morphometric indicators, and age spectra. It is noted that previous studies of the natural populations of A. pseudalhagi in both the Atyrau region and in Kazakhstan as a whole have not been carried out.
The morphometric indicators of individuals from the four populations differed in the number of individuals per 1 m2, the height of generative shoots, and the number of shoots per individual. Table 2 presents the morphometric parameters of A. pseudalhagi in the studied populations of the Atyrau region. According to the data obtained, the greatest number of individuals per 1 m2 was noted for population 2 (2.6 pieces) and population 3 (2.2 pieces), and the lowest growth density was noted for population 4 (0.5 pieces).
The main morphological difference between individuals of the four populations of A. pseudalhagi is the height of the plants. In terms of growth indicators, the highest values were noted in population 3 (30.5 cm) and the lowest in population 1 (24.4 cm) (Figure 3).
Accordingly, individuals in population 3 which had the greatest generative shoot heights had the largest number of generative shoots per individual (6.1 pieces) by far, while population 4 had the largest number of generative shoots (2.9 pieces). Population 1 occupies an intermediate position between population 2 and population 4 in terms of morphometric parameters. Probably, the differences between the populations are due to differences in climatic conditions and the degree of anthropogenic load at the growing points.
The principle of basic coordinates showed the presence of similar basic population parameters between populations 2 and 3 and between populations 1 and 4 (Figure 4). This group association is related to the geographical proximities of these two groups. The most significant difference in the morphological parameters of individuals between different populations was observed for population 1 and population 4, while population 2 and population 3 have similar parameters.
The dendrogram shows that there is a small overlap of individuals between populations 2, 3, and 4, comprising a special group that does not climb up to the mountainous territory. A low degree of overlap characterizes the mountainous population. All populations differed significantly from each other in the number of individuals and in the growth of significant differences (Figure 5).
Moreover, differences between populations 2 and 4 were pointed out. There were significant differences in the number of generative shoots between populations 1 and 4 and between populations 2 and 3. Probably, the differences between the populations were due to the difference in the climatic conditions of the arid zone and the various natural conditions influencing the growth of the species.
The following indicators were correlated: the plant height, in cm (PH); the plant diameter, in cm (PD); the number of generative shoots (GS), in pieces; the number of individuals per 1 m2, in pieces (NI); the soil type (ST); the and population (CP). These correlations show the positive influence of the main factors for identifying and assessing the state of A. pseudalhagi populations (Figure 6).
The one-way factor analysis (ANOVA) showed the significance (p < 0.05) of the influence of the soil type (ST) on the following plant indicators in the different populations: plant height (PH), with a value of 4.16 × 10−6; plant diameter (PD), with a value of 6.55 × 10−13; number of generative shoots (GS), in pieces, with a value of 3.79 × 10−10; and number of individuals per 1 m2, in pieces (NI), with a value of 3.59 × 10−6.
A canonical correspondence analysis (CCA) was also performed for the four populations to determine correspondence between the parameters of height above sea level (altitude) and type of land and the following parameters: plant height, cm (PH), plant diameter, cm (PD); number of generative shoots, pieces (GS); number of individuals per 1 m2, pieces (NI). Also, the presence and absence of such geographical factors as mountainous terrain, riverbanks, and empty sands were considered. The results are presented graphically in Figure 7.

3.4. Resource Potential of the Populations A. pseudalhagi

A study of the resources of A. pseudalhagi made it possible to determine that the yield of raw materials varied from 850 to 2847 kg/ha (Table 3). The maximum harvest was found in the vicinity of Imankara Mountain, and the minimum harvest was in the Zhangyr River valley.
The total area of the thickets is estimated to be 240.3 ha. The operational reserve amounts to 418.52 tons, while the annual possible collection of above-ground organs was estimated at 209.26 tons. Sufficient thicket areas and the volume of potential plant raw materials of A. pseudalhagi on the territory of the Atyrau region make it possible to recommend this species for industrial procurement.

4. Discussion

Research studying the state of wild populations of A. pseudalhagi in the Atyrau region is scarce, and there is practically no scientific research on the study of the resource reserves of A. pseudalhagi. To conduct a comparative analysis, results from studies of closely related species were reviewed.
Significant differences in the species composition of A. pseudalhagi populations were noted. Thus, the maximum index of similarity in floristic composition was found between populations 2 and 3—0.122; the minimum index was between populations 1 and 2—0.042.
The obtained data can be explained by the fact that in the Zhangyr and Coneu River valleys, similar soil and climatic conditions and degrees of anthropogenic pressure are observed, while populations 1 and populations 4 are located in significantly different conditions. Thus, in the vicinity of Imankara Mountain, 25 species grow; in the valley of the rivers Zhangyr and Coneu, 24 species grow each; and on the Taisoigan sands, 21 species grow. This statement about the complex relationships of A. pseudalhagi populations with various plant and animal species is confirmed in other studies [54].
One of the main indicators of a plant’s resource reserves is the average height of the plants in the population. The tallest plants were recorded in populations 2 (Zhangyr) and 3 (Coneu) at 28.3 ± 1.3 and 30.5 ± 1.5 cm; in addition, the dry mass indicators are 976 ± 42 and 850 ± 94 kg/ha, which are among the lowest figures. Comparing the recorded dry weights of plants in this study, it can be seen that the same positive trends are shown in other parameters. This indicator is associated with the presence of the coastal–aquatic location factor, which is confirmed in Figure 7 (canonical correspondence analysis CCA). The same pattern has been scientifically confirmed in studies of A. sparsifolia populations in China [55]. The complex morphological structure of individual organs is also preserved for the root system of A. pseudalhagi [56]. A CCA of A. pseudalhagi populations showed a direct impact on the environment, namely rocky and soil characteristics showed differences between populations. This judgment is also confirmed in populations of A. maurorum, which may also be a growth strategy in arid and semi-arid conditions [57].
The one-way factor analysis (ANOVA) showed the significance (p < 0.05) of the influence of the soil type (ST) factor on the plant indicators in different populations: plant height (PH), with a value of 4.16 × 10−6; plant diameter (PD), with a value of 6.55 × 10−13; the number of generative shoots (GS), in pieces, with a value of 3.79 × 10−10; and the number of individuals per 1 m2, in pieces (NI), with the value 3.59 × 10−6. These results show the great importance of soil type. The populations growing in non-mountainous zones are depleted into one diseased group, which is presented in the dendrogram in Figure 5 (UPGMA). Similar results were obtained in some populations of A. graecorum and confirmed by genetic studies. It can be noted that the main morphological characteristics correlate positively with each other, as well as with such indicators as plant height and shoot diameter, which, in turn, are observed in populations of A. maurorum [58].
These results highlight the need for further investigation into the specific drivers of unexplained variations and the role of A. pseudalhagi in shaping plant community relationships under arid conditions. This study not only expands our understanding of the structure and community composition of A. pseudalhagi populations but also highlights the significant biodiversity and abundance of plant species in this arid habitat. These studies may also be of interest in environmental assessment and population management [59].

5. Conclusions

In general, the study of four populations of the medicinal plant A. pseudalhagi (in the arid zone of the Zhangyr and Coneu Rivers, the vicinity of Imankara Mountain, and on the Taisoigan sands) showed that they are in satisfactory conditions and can be used for organizing the procurement of medicinal herbs in compliance with the correct regime and frequency of harvesting. All populations of A. pseudalhagi differ from each other in terms of their floristic compositions and main significant morphological indicators. Analysis of the age spectra made it possible to determine that the populations in the valleys of the Zhangyr and Coneu Rivers are characterized as young and those in the vicinity of Imankara Mountain and on the Taisoigan sands as stable and middle-aged. The annual harvestable volume of above-ground organs is estimated at 209.26 tons in the catchments of the arid zone of the Atyrau region. To preserve natural populations of this medicinal species, it is necessary to regularly monitor the state of populations and develop recommendations for the procurement of these raw herbal medicinal materials.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/d16040219/s1, Table S1: Floristic composition of populations with Alhagi pseudalhagi.

Author Contributions

Data curation, A.I., M.S. and M.I.; investigation, M.S. and M.I.; methodology, G.G. and M.I.; project administration, A.I. and M.S.; resources, M.S. and A.I.; software, M.I. and G.G.; visualization, M.I.; writing—original draft, A.I.; writing—review and editing, M.I. All authors have read and agreed to the published version of the manuscript.

Funding

The research was carried out and funded within the framework of the BR18574125 program and the grant project of the Science Committee of the Ministry of Science and Higher Education of the Republic of Kazakhstan.

Institutional Review Board Statement

Not applicable.

Data Availability Statement

The original contributions presented in the study are included in the article and supplementary material.

Acknowledgments

The authors are most grateful to S.A. Kubentayev (Astana Botanical Garden—the branch of the Institute of Botany and PhytoIntroduction) for their help in identifying plant species.

Conflicts of Interest

The authors declare no conflicts of interest.

References

  1. Amirkhosravi, A.; Asri, Y.; Assadi, M.; Mehregan, I. Systematics of Alhagi: Molecular phylogeny and morphology revisited. Rostaniha 2020, 21, 174–184. [Google Scholar] [CrossRef]
  2. Ye, Z.; Li, T.; Qing, D.; Sun, Y.; Chen, H.; Yu, Q.; Yan, C. Structural elucidation and osteogenic activity of a novel heteropolysaccharide from Alhagi pseudalhagi. Int. J. Biol. Macromol. 2021, 171, 185–197. [Google Scholar] [CrossRef]
  3. Svetlana, Z.Y.; Nadezhda, G.G.; Mihaela, B.I. Northern Tien Shan medicinal herbs. J. Lucr. Științifice Manag. Agricol. 2019, 20, 399. [Google Scholar]
  4. Patsaev, A.K.; Makhatov, B.K.; Kucherbaev, K.D.; Bukharbaeva, A.E.; Anes, A.T. The study of medicinal plants of southern Kazakhstan. Bull. Kyrg. State Med. Acad. Named I.K. Akhunbaev 2017, 5, 96–97. [Google Scholar]
  5. Amini, M.H.; Ahmady, A.; Zhakfar, A.M.; Sediqi, M.N.; Babak, G. Preliminary Phytochemical Profile, in vitro Antioxidant and Sun Protective Activities of Alhagi pseudalhagi and Elaeagnus angustifolia L. J. Pharm. Res. Int. 2019, 12, 1–13. [Google Scholar] [CrossRef]
  6. Srivastava, B.; Sharma, H.; Dey, Y.N.; Wanjari, M.M.; Jadhav, A.D. Alhagi pseudalhagi: A review of its phytochemistry, pharmacology, folklore claims and Ayurvedic studies. Int. J. Herb. Med. 2014, 2, 47–51. [Google Scholar]
  7. Myrzagalieva, A.B. Comparative analysis of the species composition and resources of medicinal plants of the Kazakhstan Altai. Bull. Kaznu Biol. Ser. 2013, 2, 3–9. [Google Scholar]
  8. Xu, X.; Zhang, J.; Chen, L.; Sun, Y.; Qing, D.; Xin, X.; Yan, C. Alhagi pseudalhagiExtract Exerts Protective Effects Against Intestinal Inflammation in Ulcerative Colitis by Affecting TLR4-Dependent NF-κB Signaling Pathways. Front. Pharmacol. 2021, 12, 764602. [Google Scholar] [CrossRef]
  9. Mutailifu, P.; Nuerxiati, R.; Lu, C.; Huojiaaihemaiti, H.; Abuduwaili, A.; Yili, A. Extraction, purification, and characterization of polysaccharides from Alhagy pseudalhagi with antioxidant and hypoglycemic activities. Process Biochem. 2022, 121, 339–348. [Google Scholar] [CrossRef]
  10. Tavassoli, A.P.; Anushiravani, M.; Hoseini, S.M.; Nikakhtar, Z.; Baghdar, H.N.; Ramezani, M.; Ayati, Z.; Amiri, M.S.; Sahebkar, A.; Emami, S.A. Phytochemistry and therapeutic effects of Alhagi spp. and Taganda bin in traditional and modern medicine: A review. J. Herbmed Pharm. 2020, 9, 86–104. [Google Scholar] [CrossRef]
  11. Zeinullina, A.; Zargar, M.; Dyussibayeva, E.; Orazov, A.; Zhirnova, I.; Yessenbekova, G.; Zotova, L.; Rysbekova, A.; Hu, Y.-G. Agro-Morphological Traits and Molecular Diversity of Proso Millet (Panicum miliaceum L.) Affected by Various Colchicine Treatments. Agronomy 2023, 13, 2973. [Google Scholar] [CrossRef]
  12. Ishmuratova, M.Y.; Murzalieva, G.T.; Kraschanovskaya, T.R.; Sivolobova, O.A.; Kaldybaeva, A.K.; Temireeva, K.S.; Tukubaeva, G.N.; Isina, J.A.; Amanzhan, A. Wild Medicinal Plants of Karaganda Region; Monograph; Bolashak-Baspa: Karaganda, Kazakhstan, 2016; 205p. (In Russian) [Google Scholar]
  13. Ishmuratova, M.Y.; Zhunussova, M.A.; Tyrzhanova, S.S.; Silant’eva, M.M. Study of spreading and plant resources of herbs Scabiosa ochroleuca L. and Scabiosa isetensis L. on the territory of Karaganda region. Bull. Karaganda Univ. 2020, 97, 47–53. [Google Scholar] [CrossRef]
  14. Li, N.; Zhang, G.; Xiong, Y.; Makhabel, B.; Li, X.; Jia, X. New isoflavonolignan with quinone reductase inducing activity from Alhagi pseudalhagi (MB). Fitoterapia 2010, 81, 1058–1061. [Google Scholar] [CrossRef]
  15. Karshibaev, K.K. Reproduction characteristics of some species Alhagi Gagnev. in the arid zones of Uzbekistan. Arid. Ecosyst. 2014, 4, 127–133. [Google Scholar] [CrossRef]
  16. Kubentayev, S.A.; Suleimenov, A.N.; Kotukhov, J.A.; Danilova, A.N.; Sumbembayev, A.A. Phytocenotic characteristics and stock of the main medicinal plants of the South-Western Altai (East Kazakhstan). Eurasian J. BioScience 2018, 12, 355–368. [Google Scholar]
  17. Zhivotovsky, L.A. Typification of plant populations on the basis of their ontogenetic spectra. Contemp. Probl. Ecol. 2023, 16, 265–273. [Google Scholar] [CrossRef]
  18. Kuanbay, Z.I.; Abiyev, S.A.; Ishmuratova, M.Y.; Admanova, G.B.; Kukenov, Z.Z.; Maksutbekova, G.T. The analysis of the Dongyztau chink flora (Aktobe region). EurAsian J. BioSciences 2020, 14, 249–254. [Google Scholar]
  19. Aidarkhanova, G.S.; Novak, A.P.; Imasheva, B.S.; Tashev, A. Evaluation of resources of medicinal plants in the forests of the Kazakhstan part of the Altai and their ecological state. Bull. Karaganda Univ. Ser. Biol. Med. Geogr. 2019, 95, 73–79. [Google Scholar]
  20. Ishmuratova, M.Y.; Imanbayeva, A.A.; Tuyakova, A.T.; Kopbaeva, G.B. Study of common licorice (Glycyrrhiza glabra) reserves in Atyrau and Western-Kazakhstan regions. Biosci. Biotechnol. Res. Asia 2016, 13, 1429. [Google Scholar] [CrossRef]
  21. Orazov, A.; Tustubayeva, S.; Alemseytova, J.; Mukhitdinov, N.; Myrzagaliyeva, A.; Turuspekov, Y.; Sramko, G. Flora accompanying Prunus ledebouriana (Schltdl.) YY Yao in the Tarbagatai State National Park in Kazakhstan. Int. J. Biol. Chem. 2021, 14, 21–34. [Google Scholar] [CrossRef]
  22. Kubentayev, S.A.; Zhumagul, M.Z.; Kurmanbayeva, M.S.; Alibekov, D.T.; Kotukhov, Y.A.; Sitpayeva, G.T.; Mukhtubayeva, S.K.; Izbastina, K.S. Current state of population of Rhodiola rosea L. (Crassulaceae) in East Kazakhstan. Bot. Stud. 2021, 62, 19. [Google Scholar] [CrossRef] [PubMed]
  23. Zargar, M.; Dyussibayeva, E.; Orazov, A.; Zeinullina, A.; Zhirnova, I.; Yessenbekova, G.; Rysbekova, A. Microsatellite-based genetic diversity analysis and population structure of Proso Millet (Panicum miliaceum L.) in Kazakhstan. Agronomy 2023, 13, 2514. [Google Scholar] [CrossRef]
  24. Galaktionova, E.V. Medicinal plants included in the flora of the North Kazakhstan region. Stud. Nat. Sci. 2012, 5. (In Russian) [Google Scholar]
  25. Orazov, A.; Myrzagaliyeva, A.; Mukhitdinov, N.; Tustubayeva, S. Callus induction with 6-BAP and IBA as a way to preserve Prunus ledebouriana (Rosaceae), and endemic plant of Altai and Tarbagatai, East Kazakhstan. Biodiversitas J. Biol. Divers. 2022, 23, 3178–3184. [Google Scholar] [CrossRef]
  26. Chen, X.; Jiang, F.Q.; Wang, Y.J.; Li, Y.M.; Hu, R.J. Characteristics of the Eco-geographical pattern in the arid land of central Asia. Arid Zone Res. 2013, 30, 385–390. [Google Scholar]
  27. Grudzinskaya, L.M.; Gemedjieva, N.G.; Nelina, N.V.; Karzhaubekova, Z. Annotated List of Medicinal Plants of Kazakhstan: A Reference Edition; MEDA-Alliance Publishing House: Willis, TX, USA, 2010; 200p. [Google Scholar]
  28. Wei, F.; Yang, X.; Pang, K.; Tang, H. Traditional uses, chemistry, pharmacology, toxicology and quality control of Alhagi sparsifolia Shap.: A review. Front. Pharmacol. 2021, 1214, 761811. [Google Scholar] [CrossRef]
  29. Kotukhov, Y.A.; Danilova, A.N.; Kubentaev, S.A. List of Medicinal Plants Kazakhstan Altai; MEDA-Alliance Publishing House: Ridder, Kazakhstan, 2015; 70p. (In Russian) [Google Scholar]
  30. Abduraimov, O.S.; Li, W.; Shomurodov, H.F.; Feng, Y. The main medicinal plants in arid regions of Uzbekistan and their traditional use in folk medicine. Plants 2023, 12, 2950. [Google Scholar] [CrossRef]
  31. Roberson, E. Nature’s Pharmacy, Our Treasure Chest: Why We Must Conserve Our Natural Heritage. A Native Plant Conservation Campaign Report; Center for Biological Diversity: Tuczon, AZ, USA, 2008; 19p. [Google Scholar]
  32. Imanbaeva, A.A.; Ishmuratova, M.Y.; Tuyakova, A.T. Screening of Mangystau flora for wild relatives of cultivated plants. Cent. Eur. J. Bot. 2015, 1, 12–20. [Google Scholar] [CrossRef]
  33. Nishanbaev, S.Z.; Shamyanov, I.J.; Bobakulov, K.M.; Sagidullaev, S. Chemical composition and biological activity of metabolites of the genus Alhagi (review). Chem. Plant Raw Mater. 2019, 4, 5–28. [Google Scholar] [CrossRef]
  34. Orazov, A.; Yermagambetova, M.; Myrzagaliyeva, A.; Mukhitdinov, N.; Tustubayeva, S.; Turuspekov, Y.; Almerekova, S. Plant height variation and genetic diversity between Prunus ledebouriana (Schlecht.) YY Yao and Prunus tenella Batsch based on using SSR markers in East Kazakhstan. PeerJ 2024, 12, e16735. [Google Scholar] [CrossRef]
  35. UNCTAD. Convention on Biological Diversity and the Nagoya Protocol: Intellectual Property Implications; UNCTAD: Geneva, Switzerland, 2014; 215p. [Google Scholar]
  36. Janalieva, K.M.; Budnikova, T.I.; Veselov, E.N. Physical Geography of the Republic of Kazakhstan; Al-Farabi Kazak National University: Almaty, Kazakhstan, 1998; 266p. (In Russian) [Google Scholar]
  37. Zhang, M. A review on the floristic phytogeography in arid northwestern China and Central Asia. Biodivers. Sci. 2017, 25, 147–155. [Google Scholar] [CrossRef]
  38. Smirnova, O.V.; Zaugolnova, L.B.; Ermakova, I.M. Cenopopulation of Plants; Science Publishing House: Moscow, Russia, 1976; p. 217. [Google Scholar]
  39. Pavlov, N.B. Flora Kazahstana [Flora of Kazakhstan]; Publishing House of the Kazakh Academy of Sciences: Almaty, Kazakhstan, 1956; Volume 1, 347p. [Google Scholar]
  40. Goloskokov, V.P. (Ed.) Illiustrirovannyi Opredelitel Rastenii Kazakhstana [Illustrated Determinant of Plants of Kazakhstan]; Nauka: Almaty, Kazakhstan, 1972; Volume 2. (In Russian) [Google Scholar]
  41. Kamelin, R.V. Key to Plants of Central Asia. A Critical Abstract of Flora; Science Publishing House: Leningrad, Russia, 2015; Volume 11. [Google Scholar]
  42. International Plant Names Index. Available online: www.ipni.org (accessed on 30 January 2024).
  43. Serebryakov, I.G. Ecological Morphology of Plants. Life Forms of the Overgrowths and Conifers; High School: Moscow, Russia, 1982; 380p. (In Russian) [Google Scholar]
  44. Shay, J.E.; Pennington, L.K.; Mandussi Montiel-Molina, J.A.; Toews, D.J.; Hendrickson, B.T.; Sexton, J.P. Rules of plant species ranges: Application for conservation strategies. Front. Ecol. Evol. 2021, 9, 700962. [Google Scholar] [CrossRef]
  45. Kew Royal Botanical Garden. Plants of the World Online. Available online: www.powo.science.kew.org (accessed on 30 January 2024).
  46. Kalacska, M.; Sanchez-Azofeifa, G.A.; Calvo-Alvarado, J.C.; Quesada, M.; Rivard, B.; Janzen, D.H. Species composition, similarity and diversity in three successional stages of a seasonally dry tropical forest. For. Ecol. Manag. 2004, 200, 227–247. [Google Scholar] [CrossRef]
  47. Komarov, A.S.; Palenova, M.M.; Smirnova, O.V. The concept of discrete description of plant ontogenesis and cellular automata models of plant populations. Ecol. Model. 2003, 170, 427–439. [Google Scholar] [CrossRef]
  48. Fedorova, S.V. Methodological approaches in population botany and plant ecology. Am. J. BioScience 2020, 8, 73–90. [Google Scholar] [CrossRef]
  49. Elzinga, C.L.; Salzer, D.W.; Willoughby, J.W. Measuring & Monitoring Plant Populations; Bureau of Land Management, US Department of the Interior: Washington, DC, USA, 2019; 497p. [Google Scholar]
  50. Kuziev, R.K.; Sektimenko, V.E. Soils of Uzbekistan; Extremum Press Publishing House: Tashkent, Uzbekistan, 2009; p. 351. (In Russian) [Google Scholar]
  51. Kuziev, R.K.; Yuldashev, G.Y.U.; Akramov, I.A. Bonitization of Soils; The Way of Science Publishing House: Tashkent, Uzbekistan, 2004; p. 127. [Google Scholar]
  52. Joshi, S.P.; Gupta, V.S.; Aggarwal, R.K.; Ranjekar, P.K.; Brar, D.S. Genetic diversity and phylogenetic relationship revealed by inter simple sequence repeat (ISSR) polymorphism in the genus Oryza. Theor. Appl. Genet. 2000, 100, 1311–1320. [Google Scholar] [CrossRef]
  53. Rohlf, F. NTSYSpc: Numerical Taxonomy and Multivariate Analysis System, Version 2.02; Exeter Software: Setauket, NY, USA, 1998. [Google Scholar]
  54. Yaghmaee, F. Evaluation of biological activity of meadow spittlebug Philaenus spumarius (L.) (Cercopide: Homoptera) on Alhagi pseudalhagi (M. Bieb.) Desv. camel thorn plant in Mashhad region, Khorasan Razavi province, Iran. Res. J. Biol. Sci. 2008, 3, 845–849. [Google Scholar]
  55. Zeng, F.; Zhang, X.; Foetzki, A.; Li, X.; Li, X.; Runge, M. Water relation characteristics of Alhagi sparsifolia and consequences for a sustainable management. Sci. China Ser. D Earth Sci. 2002, 45, 125–131. [Google Scholar] [CrossRef]
  56. Yan, F.; Wenyong, W.; Zhongwei, H.; Tianyi, Z. Notice of Retraction: An alhagi pseudalhagi roots model based on l-systems in virtual plant research. In Proceedings of the 2010 International Conference on Computer Application and System Modeling (ICCASM 2010), Taiyuan, China, 22–24 October 2010; Volume 14. [Google Scholar]
  57. Iqbal, U.; Ali, A.; Daad, A.; Aslam, M.U.; Rehman, F.U.; Farooq, U.; Gul, M.F. Unraveling the defensive strategies of camel thorn Alhagi maurorum medik. For thriving in arid and semi-arid environments. J. Arid. Environ. 2023, 219, 105076. [Google Scholar] [CrossRef]
  58. El-Hak, A.; Hassan, H.Z. Genetic variation within and among the wild populations of Alhagi graecorum using ISSR markers. Taeckholmia 2019, 39, 67–85. [Google Scholar] [CrossRef]
  59. Brock, J.H. Ecology and management of Alhagi maurorum in a pine-oak forest in north-central Arizona, USA. In Plant Invasions: Human Perception, Ecological Impacts and Management; Backhuys Publishers: Leiden, The Netherlands, 2008; pp. 93–100. [Google Scholar]
Figure 1. Locations of the populations of A. pseudalhagi.
Figure 1. Locations of the populations of A. pseudalhagi.
Diversity 16 00219 g001
Figure 2. Age composition of the populations of A. pseudalhagi.
Figure 2. Age composition of the populations of A. pseudalhagi.
Diversity 16 00219 g002
Figure 3. Column diagram of plant heights in populations of A. pseudalhagi.
Figure 3. Column diagram of plant heights in populations of A. pseudalhagi.
Diversity 16 00219 g003
Figure 4. Principal coordinate analysis (PCoA) for populations of A. pseudalhagi.
Figure 4. Principal coordinate analysis (PCoA) for populations of A. pseudalhagi.
Diversity 16 00219 g004
Figure 5. Unweighted pair group method with arithmetic mean (UPGMA) dendrogram populations of A. pseudalhagi.
Figure 5. Unweighted pair group method with arithmetic mean (UPGMA) dendrogram populations of A. pseudalhagi.
Diversity 16 00219 g005
Figure 6. Correlation of the main significant parameters of populations of A. pseudalhagi: plant height, cm (PH); population (CP); plant diameter, cm (PD); number of generative shoots (GS), pieces; number of individuals per 1 m2, pieces (NI); soil type (ST).
Figure 6. Correlation of the main significant parameters of populations of A. pseudalhagi: plant height, cm (PH); population (CP); plant diameter, cm (PD); number of generative shoots (GS), pieces; number of individuals per 1 m2, pieces (NI); soil type (ST).
Diversity 16 00219 g006
Figure 7. Canonical correspondence analysis (CCA) of populations of A. pseudalhagi (The black dot indicates: plant height, cm (PH); plant diameter, cm (PD); number of generative shoots, pieces (GS); number of individuals per 1 m2, pieces (NI).
Figure 7. Canonical correspondence analysis (CCA) of populations of A. pseudalhagi (The black dot indicates: plant height, cm (PH); plant diameter, cm (PD); number of generative shoots, pieces (GS); number of individuals per 1 m2, pieces (NI).
Diversity 16 00219 g007
Table 1. Geographical locations of A. pseudalhagi populations in Atyrau region.
Table 1. Geographical locations of A. pseudalhagi populations in Atyrau region.
NameGeographical LocationCoordinatesHeight Above Sea LevelAdministrative Location
Population 1The vicinity of Imankara Mountain47°19′49″ N 54°22′12″ E370 m above sea levelAtyrau region, Zhylyoysky district
Population 2Zhangyr River valley46°40′05″ N 49°23′50″ E281 m below sea levelAtyrau region, Kurmangazinsky district
Population 3Coneu River valley46°40′00″ N 49°23′50″ E284 m below sea levelAtyrau region, Kurmangazinsky district
Population 4Taisoigan sands48°49′23″ N 53°44′36″ E225 m above sea levelAtyrau region, Kzylkoginsky district
Table 2. Quantitative and morphological indicators of generative individuals of A. pseudalhagi in the studied populations (M ± m).
Table 2. Quantitative and morphological indicators of generative individuals of A. pseudalhagi in the studied populations (M ± m).
NameGenerative Plant Height, cmNumber of Generative Individuals
per 1 m2, Pcs.
Number of Generative Shoots per Individual, Pcs.
Populations 124.4 ± 1.20.8 ± 0.023.2 ± 0.5
Populations 228.3 ± 1.32.6 ± 0.035.6 ± 0.8
Populations 330.5 ± 1.52.2 ± 0.016.1 ± 0.03
Populations 426.2 ± 1.40.5 ± 0.022.9 ± 0.4
Table 3. Areas of thickets and raw materials of above-ground organs of A. pseudalhagi in the studied populations in the Atyrau region (in air-dry weight).
Table 3. Areas of thickets and raw materials of above-ground organs of A. pseudalhagi in the studied populations in the Atyrau region (in air-dry weight).
PopulationsArea, haYield, kg/haOperational Reserve, tonsThe Volume
of Possible Harvested Raw Materials, tons
Population 196.02847 ± 180273.30136.65
Population 252.0976 ± 4250.7625.38
Population 380.0850 ± 9468.0434.02
Population 412.32148 ± 12226.4213.21
Total240.3-418.52209.26
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Sagyndykova, M.; Imanbayeva, A.; Gassanova, G.; Ishmuratova, M. Current Status and Resources of Alhagi pseudalhagi (Fabaceae) in the Atyrau Region, Western Kazakhstan. Diversity 2024, 16, 219. https://doi.org/10.3390/d16040219

AMA Style

Sagyndykova M, Imanbayeva A, Gassanova G, Ishmuratova M. Current Status and Resources of Alhagi pseudalhagi (Fabaceae) in the Atyrau Region, Western Kazakhstan. Diversity. 2024; 16(4):219. https://doi.org/10.3390/d16040219

Chicago/Turabian Style

Sagyndykova, Meruert, Akzhunis Imanbayeva, Gulnara Gassanova, and Margarita Ishmuratova. 2024. "Current Status and Resources of Alhagi pseudalhagi (Fabaceae) in the Atyrau Region, Western Kazakhstan" Diversity 16, no. 4: 219. https://doi.org/10.3390/d16040219

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop