The Current State of Populations of Rhaponticum altaicum (Asteraceae) in the Northern and Central Kazakhstan

Abstract

The article presented the results of the assessment of the current state of Rhaponticum altaicum populations in the Karaganda and Akmola regions (Central and Northern Kazakhstan). The research provided the phytocenotic characteristics of habitats, biological features, and ontogenetic structure of populations, as well as data on the morphological variability of the species. The floristic composition of plant communities with Rh. altaicum was analyzed for the first time. In the plant communities with Rh. altaicum, 67 species from 38 genera and 23 families were identified. Most species were herbaceous perennials (92.5%) or hemicryptophytes (68.7%). Among the ecological groups, mesophytes (32.8%) dominated, and other groups were represented by transitional species: mesoxerophytes, xeromesophytes, mesogyrophytes, and hygromesophytes (49.2%). Therefore, in nature, Rh. altaicum occupied an intermediate place between meadow-bog and meadow communities. The species preferred moist meadows on slightly and moderately saline soils. In the ontogeny of Rh. altaicum, eight age-related states were identified, from seedlings to senile plants. The analysis of morphological indices allowed estimating that Rh. altaicum stem height was the most important; so, under unfavorable growing conditions, the stem height decreased. In the majority of populations, the upper leaf width was a highly variable trait, and the length and width of the lower leaf had low or moderate morphological variability. The highest positive correlation (significant at p = 0.05) was between plant height and lower leaf length, suggesting that taller plants had longer lower leaf blades. The studied populations were mainly dominated by virgin and medium-age generative plants. Sub-senile and senile plants were not detected, which is due to the difficulty of diagnosis as well as to the increasing anthropogenic load and narrow ecological amplitude of Rh. altaicum. Our study provided new insights into Rh. altaicum biology and ecology, thereby contributing to biodiversity conservation at a regional level.

1. Introduction

The plant world of Kazakhstan is characterized by exceptional diversity and richness of flora with more than 1400 species of medicinal plants belonging to 134 families [1]. The study of medicinal plant populations is important to assess their current state and the possibility of using.

In this regard, the genus Rhaponticum Vaill is extremely interesting and promising for study. Plants of this genus are characterized by a rich chemical composition and possess valuable medicinal properties. Their main active substances are ecdysteroids, sesquiterpene lactones, flavonoids, and essential oils [2].

There are six species of Rhaponticum native to Kazakhstan, including Rhaponticum carthamoides (Wllld.) lljin, Rh. aulieatense Iljin, Rh. karatavicum Regel et Schmalh, Rh. altaicum (Fisch. ex Spreng.) Soskov, Rh. nitidum Fisch. and Rh. namanganicum Iljin [3]. Rh. karatavicum is endemic to Kazakhstan [4].

The most studied representative of this genus is Rhaponticum carthamoides (Wiild.) Iljin, the chemical composition of the roots of which began to be studied in the middle of the XX century, and now this plant is widely used in medicine [5]. Extracts and preparations from Rh. carthamoides are characterized by low toxicity; they exhibit tonic, stimulating, and adaptogenic properties, and provide antioxidant, immunomodulatory, hemorheological, antibacterial, and anabolic effects [6,7,8,9,10,11,12,13]. The first in Kazakhstan tonic preparation “Ecdistene” was based on ecdysterone isolated from the roots of Rh. carthamoides [14]. Some other members of the genus Rhaponticum, including Rh. uniflorum (L.) DC., Rh. coniferum (L.) Greuter, Rh. acaule (L.) DC. and Rh. karatavicum, are also characterized by a wide range of biological activity and are used in traditional medicine. Their pharmacological action is due to the presence of ecdysteroids, sesquiterpene lactones, phenolic compounds, and essential oils [15,16,17,18,19,20,21,22,23,24,25,26,27,28].

At present, the medicinal potential of other species of the genus Rhaponticum growing in Kazakhstan remains insufficiently studied. One of such species is Rhaponticum altaicum (Fisch. ex Spreng.) Soskov, widely distributed in Northern and Central Kazakhstan [3]. Data on the chemical composition and pharmacological activity of Rh. altaicum are limited. According to A.G. Berdin [29], the aerial part of this plant can be used as an additional source of medicinal plant raw material with antiviral, cytotoxic, and antiprotozoal activities due to the presence of ecdysterone and sesquiterpene lactones. Centaurepsin and raposerine proved to inhibit the reproduction of influenza virus [29,30]. The potential of Rh. altaicum as an alternative source of ecdysterone was confirmed by S.O. Volodin [31]. According to their data, in the fruiting phase, the content of 20-hydroxyecdysone in young leaves was 1.43%, which is significantly higher than in roots of Rh. carthamoides (0.14%).

Rh. altaicum (synonyms: Leuzea altaica Link., Rh. serratuloides Georgi (Bobr.), Stemmacantha serratuloides (Georgi) M. Dittrich)) is a perennial herbaceous plant with a low rhizome, 40 to 100 cm high [32,33]. The species is widespread in Kazakhstan, growing in 13 floristic areas, mainly in the steppe and semi-desert zones [3]. Globally, its distribution range extends across the steppe zone of Eastern Europe and includes Romania, Moldova, Ukraine [34], and the south and center of the European part of Russia [35]. In the south of Western Siberia, it is found in the Tyumen, Kurgan, Omsk, and Novosibirsk regions and in the Altai Territory, which are the eastern distribution of species [32]. The northern limit is in the Trans-Ural Region at 65° N. In Siberia, the location detached from the main range is in the south of the Tyumen Region, 56°40′ N (Figure 1). Outside Kazakhstan, this species is rare in some areas; therefore, it is listed as threatened in the Red Books of such regions of Russia as Samara, Saratov, and Omsk, as well as the Krasnodar Territory [36,37,38,39].

Rh. altaicum has valuable medicinal properties. It is characterized by a wide distribution area and relatively high yield compared to other representatives of this genus in Kazakhstan. These characteristics make it a promising source of biologically active substances for the pharmaceutical industry. In particular, Rh. altaicum can become an alternative to Rh. carthamoides, which is listed in the Red Book of Kazakhstan as an endangered species [40]. Populations of Rh. carthamoides are actively decreasing due to excessive collection in natural conditions. In contrast, Rh. altaicum is insufficiently studied, especially in Kazakhstan, where studies of its population structure and resource potential have not been previously conducted.

Given the urgency of the problem of biodiversity conservation and the search for new sources of plant raw materials, the aim of this work was to study the current state of Rh. altaicum populations in Northern and Central Kazakhstan. The objectives of the study included assessment of its phytocenotic characteristics of habitats, biological features and ontogenetic structure of populations, as well as data on morphological variability of the species. In addition, the floristic composition of plant communities with Rh. altaicum was studied. The data obtained may become the basis for the development of strategies for the sustainable use of Rh. altaicum, which is especially important in conditions of decreasing natural resources of other valuable plant species.

2. Materials and Methods

2.1. Study Area

Field studies were carried out in the Karaganda and Akmola regions in 2022–2024 in the phase of flowering and fruiting of Rh. altaicum. These areas are located in Northern and Central Kazakhstan. In total, 7 populations of Rh. altaicum were studied, of which 5 populations are in Karaganda region and 2 populations are in Akmola region (Figure 2,

Table 1. Characteristics of plant populations with Rh. altaicum.

Population No.	Location Name, Altitude, Coordinates	Habitat	General Information
Pop 1	Karaganda region, the vicinity of the village of Karabas, 503 m a.s.l., 49°34′48.0″ N, 72°53’38.1″ E	Grass and Artemisia meadow near a road	Soils are anthropogenically disturbed, chestnut, meadow, almost not saline. Anthropogenic disturbance of the phytocenosis is high. The community is dominated by Elymus repens (L.) Gould and Artemisia nitrosa Web. ex Stechm., with 18 species in total. Artemisia abrotanum L., Plantago urvillei Opiz., Phragmites australis (Cav.) Trin. ex Steud., and Rh. altaicum make the largest contribution in addition to the dominant species.
Pop 2	Karaganda region, near the city of Abay, 500 m a.s.l., 49°38’03.4″ N, 72°50’38.3″ E	Well-moistened hollow near a road	Soils are dark chestnut, meadow, slightly saline. The anthropogenic disturbance of the phytocoenosis is medium. The dominant species are Carex stenophylla Wahlenb., Juncus gerardii Loisel., Rh. altaicum. The community has 16 species in total. In addition to the dominant species, Agrostis gigantea Roth and Elymus repens make the largest contribution.
Pop 3	Karaganda region, near the city of Abay, 49°40′31.3″ N, 72°51′50.3″ E	Mown meadow	The mown meadow, the plants are scattered, the anthropogenic disturbance of the phytocoenosis is medium. Soils are are dark chestnut, slightly saline. The community is dominated by Artemisia abrotanum and Bromus inermis Leyss.; there are 11 species in total. In addition to the dominant species, Agropyron cristatum (L.) Gaertn., Saussurea amara (L.) DC. and Elymus repens make the largest contribution.
Pop 4	Karaganda region, between Abai and Saran, 485 m a.s.l., 49°40′57.6″ N, 72°51′37.2″ E	Flood meadow, on the outskirts of drying lakes	Soils are dark chestnut, meadow, medium saline. Anthropogenic disturbance of the phytocenosis is low. The dominant species are Calamagrostis epigejos (L.) Roth, Glycyrrhiza uralensis Fisch. ex DC., Bromus inermis. There are 16 species in total. Juncus compressus Jacq. also makes a significant contribution to the vegetation cover.
Pop 5	Karaganda region, Temirtau district, 363 m a.s.l., 50°04′49″ N, 73°13′30″ E	Swampy meadow	Soils are chestnut, medium-saline. The anthropogenic disturbance of the phytocoenosis is medium. The dominant species are Phragmites australis, Juncus gerardi. There are 23 species in total: Calamagrostis epigeios, Alopecurus arundinaceus Poir., Artemisia nitrosa, Elymus repens also make a significant contribution.
Pop 6	Akmola region, Zhaltyr village, 291 m a.s.l., 51°44′05.7″ N, 69°54′42.1″ E	Flooded meadow	Soils are slightly saline, dark chestnut. Anthropogenic disturbance of the phytocenosis is low. The dominant species is Elymus repens, there are 27 species in total: Bolboschoenus maritimus (L.) Palla, Eleocharis palustris (L.) Roem. et Schult., Rh. altaicum also make a significant contribution.
Pop 7	Akmola region, Astana district, the vicinity of the village of Karazhar, the valley of the Nura River, the Astana–Malinovka highway, 341 m a.s.l., 51°05′27.9″ N, 71°11′05.3″ E	Swampy meadow	Soils are dark chestnut, medium-saline. Anthropogenic disturbance of the phytocenosis is high. The dominant species are Artemisia abrotanum, Calamagrostis epigeios. The total number of species is 18: Galatella dahurica DC, Saussurea amara also make a significant contribution.

).

2.2. Population Studies

The following main characteristics of populations were recorded: age structure, ontogenesis, projective cover, morphometric parameters of generative individuals of Rh. altaicum, floristic composition of plant communities with Rh. altaicum, total projective cover, and ecological and phytocenotic characteristics of species that made up the communities studied (Figure 3).

To study population structure, areas with a high density of flowering individuals of Rh. altaicum were selected. The studies were carried out using a detailed field survey.

Rh. altaicum is an herbaceous, perennial, short-rooted plant that can reach a height of 40–100 cm (Figure 4). The leaf blades are elliptical, sharp, bare or slightly pubescent, especially on the underside. The lower leaves are petiolate, serrated, whole, or pinnate at the base with 1–3 pairs of oblong lobes, 8–30 cm long and 3–15 cm wide. In the middle and upper parts of the stem, leaves are whole, toothed, sharp, and sessile. The stem is a cylinder carrying one very large, 3–6 cm in diameter inflorescence. The flowers are purple, bisexual, and tube-like. The seeds are light brown, tetrahedral, 6–8 mm long and 2 mm wide, with a cream, 2–2.5 times longer than the seed, two-row hairy tuft of short bristles [32,33,41].

2.3. Ontogenetic Studies

Features of age-related conditions and ontogenetic (age) structure were studied in situ according to the guidelines of T.A. Rabotnov [42], A.A. Uranov [43], and O.V. Smirnova et al. [44]. The age structure and number of plants in the populations were estimated on plots with an area of 1 m², with five replicates. The ontogenetic structure of populations was defined as the percentage of individuals in different ontogenetic stages.

2.4. Study of the Floristic Composition of Communities with Rh. altaicum

The study of the floristic composition of communities with Rh. altaicum was carried out on standard plots of 100 m². Within each population, five sampling sites were established. The total population area was determined using GPS. When processing floral descriptions, the IBIS program developed by A.A. Zverev [45] was used.

The methodological approaches and terminology of K. Raunkier [46] were used in the analysis of life forms. Species assessment in relation to moisture gradient was carried out using the ecological scale of A.P. Shennikov [47]. The biomorphs of individuals was estimated according to I. G. Serebryakov [48]. Species identifications were performed according to the Plants of the World Online [49]. Species in genera and genera in families were arranged alphabetically. Species abundance was assessed by the Brown–Blanquet scale [50].

2.5. Data Analysis

When determining the variability of plant traits of Rh. altaicum, the following morphological parameters of 10 middle-aged generative individuals from each population were measured: stem height, length, and width of the lower, middle, and upper leaves. The following statistical parameters were calculated: arithmetic mean, arithmetic mean error, the average value of the intra-population variability of the trait, inter-population variability, and correlation coefficient. The analysis was carried out using the Statistica 10.0 program.

Statistical analysis of population dynamics varies depending on the limits imposed, which vary according to the standard deviation of the coefficient of variation, the mean error, the degree of confidence, and the degree of precision. When primary data were analyzed, correlation coefficients were calculated using the R program for Windows (R version 3.6.0, 2019).

A non-metric multidimensional scaling (NMDS) analysis “https://jonlefcheck.net/2012/10/24/nmds-tutorial-in-r/ (accessed on 25 February 2025) of the morphometric parameters of seven Rh. altaicum populations was conducted using the Bray–Curtis metric. This method allowed for the visualization of differences between populations. The results are presented as points, each representing an individual sample, with colors indicating membership in one of the seven populations.

3. Results

3.1. Floristic Composition of Plant Communities with Rh. altaicum

In plant communities with participation of Rh. altaicum, 67 species from 23 families and 38 genera were identified (Figure 5A). Seven families included 51 species, or 76.1% of the total number of species in the studied communities. The family Asteraceae was represented by 16 species, Poaceae—by 15 species, Cyperaceae and Amaranthaceae—by 7 and 5 species, respectively. They were followed by Apiaceae (three species), Plantaginaceae (four species), and Juncaceae (two species). The genus Carex was represented by five species followed by Artemisia and Plantago with three species each (Figure 5B).

According to the classification of ecological groups of plants in relation to moisture, the following predominated: mesophytes (23 species, or 34.3% of the total number of species), xeromesophytes and mesoxerophytes (10 species each, or 14.9%), mesohygrophytes (7 species, or 10.4%), and hygromesophytes (6 species, or 17.9%). Hygrophytes and hygrohydrophytes were represented by four species each and made up 10.4%. Xerophytes were represented by only three species (Petrosimonia triandra (Pall.) Simonk., Suaeda acuminata (C.A.Mey.) Moq., Grubovia sedoides (Pall.) G.L.Chu). It should be noted that the group of mezoxerophytes and xerophytes mostly included halophilic plants: Atriplex verrucifera Bieb., Artemisia nitrosa Web. ex Stechm, Saussurea salsa (Pall.) Spreng., Petrosimonia triandra, Suaeda acuminata, Grubovia sedoides (Appendix A).

The largest number of species was perennials (61 species, or 92.5%). Six species were annuals–biennials, most of them from the family Amaranthaceae (Grubovia sedoides, Chenopodium album L., Petrosimonia triandra, Suaeda acuminata) (Appendix A).

Analysis of life forms according to Raunkier showed that the overwhelming majority (68.7%) of herbaceous plants were hemicryptophytes. The second group of plants was cryptophytes (19.4%). Therophytes and hamefittes made up 9% and 2.9%, respectively (Appendix A).

3.2. Ontogeny of Rh. altaicum

A detailed study of the age-related ontogenetic stages of Rh. altaicum was carried out in Pop 6 and Pop 7. When studying the species ontogeny, eight age-related stages were identified, from seedlings to senile plants. As a result, the following features of age-related (ontogenetic) stages were noted (Figure 6).

Latent period. Fruits (seeds) are light brown, tetrahedral, ribbed, and slightly transversely wrinkled, with small spines at the top, 6.78 ± 0.32 mm long and 2.63 ± 0.15 mm wide. The weight of 1000 seeds is 11.75 ± 1.01 g. Once in the soil, the ripe seeds undergo natural stratification for 7–8 months.

Seedlings (p). The above-ground part is made up of a rounded yellowish 0.56 ± 0.46 cm long hypocotyl with a diameter of 0.17 ± 0.16 cm, as well as two dark green cotyledons with a smooth surface and edge. The germination takes place underground. The length is 0.63 ± 0.41 cm, and the width is 0.25 ± 0.12 cm. The surface of cotyledons is light green, with a pronounced medium vein, the edges are smooth. The root is yellowish-white, horizontal, 3–4 cm long. The stage lasts for 20–30 days.

The transition to the juvenile stage (j) occurs after the death of cotyledons and the formation of true leaves. The first true blade has a simple, ovoid shape; the edges are entire, green in color, with a pronounced central vein. Blades are narrow-lanceolate, 3.86 ± 0.52 cm long and 1.47 ± 0.52 wide, with a long petiole (up to 50% of the total leaf length). The root system is a long, rather thick, slightly branched taproot. In some cases, the plant hibernates in this state and then forms a small rhizome with 1–2 parochial roots, but the blades remain narrowly linear.

Immature individuals (im). Under natural conditions, the leaves of immature individuals have narrow lanceolate blades, especially serrated at the edges, equal to the length of the long petioles up to 7.66 ± 0.44 cm long and 1.76 ± 0.19 cm wide. There is a gradual death of the main root and increased growth of second- or third-order roots. The formation of new roots leads to the immersion of the hypocotyl into the soil. In this state, a short rhizome forms and the first thick accessory roots appear. In nature, the duration of the immature stage is 1–2 years.

In the virgin stage (v), there is an increase in the number of renewal buds and rosette modules and the development of a powerful rhizome with numerous renewal buds. The increase in the number of leaves continues; they become species-specific. Leaf length is 24.59 ± 0.97 cm and width is 9.93 ± 0.49 cm. In addition to the typical leaves with full edge blades, some leaves have a pinnate leaf blade consisting of one large and 2–3 small lobes. The leaf blade is up to 15.91 ± 0.98 cm long and 5.5 ± 0.34 cm wide.

The young generative stage (g1) is characterized by the appearance of generative organs. Production of new structures prevails over withering away. In nature, individuals usually progress to this age state in the third year. In mid-May, one orthotropic generative shoot develops in one of the rosette shoots. The shoot height is 48.76 ± 2.32 cm, the shoot diameter is 0.59 ± 0.04 cm, and the diameter of the inflorescence is 4.22 ± 0.04 cm. On the shoot, 5–6 stem leaves form (the lower ones dry up by the time of flowering). In this age stage, leaves are mostly with a sawtooth edge, the average stem leaf is 12.79 ± 1.08 cm long and 4.38 ± 0.21 cm wide. In the upper part of the shoot, the size of the leaves is significantly smaller. The duration of this age state is 2–4 years.

In the medium generative stage (g2), numerous rhizomes with rosette and orthotropic shoots form Figure 6 (g2). Their number reaches 3–5 per plant, 2–3 orthotropic vegetative shoots also form there. The shoot length is 77.68 ± 2.46 cm; the number of leaves is 7–8. The lower leaf blades are usually pinnate-lobed with a large apical lobe, 16.99 ± 0.69 cm long and 7 ± 0.37 cm wide, the upper stem leaf blades are wide oval with entire margin, 12.65 ± 0.65 cm long and 6.02 ± 0.36 cm wide. The shoot diameter reaches 9–12 mm in the middle part. A distinctive feature of this age stage is a large inflorescence reaching 6.85 ± 0.13 cm in diameter. The duration of this age stage is 3–6 years. The duration of the productive period depends on two factors: the intensity of anthropogenic impact (mowing, trampling, other anthropogenic impact) and habitat ecology (duration of flooding or drought).

In the old generative stage (g3), the number of rosette shoots increases, the generative shoots are usually small; they mainly remain underdeveloped and do not bloom. The lower leaves are divided into narrow lobes. The rhizome branches into several pieces on which only rosette shoots form. The duration of this age state is 7–9 years.

In the senile stage (s), plants consist of dying rhizomes, with single vegetative rosettes. Maceration of rhizomes occurs and a senile individual splits into separate clones with reduced vitality. The size of leaf blades is somewhat reduced but remain species-specific. The duration of this age state is 10–15 years.

3.3. Age Structure of Populations

In the flowering phase, intensive germination of Rh. altaicum seeds and a rapid transition of seedlings to juvenile and immature states were recorded in Pop 6. At the same time, the share of juvenile and immature plants in the population of Rh. altaicum was 51.5%. The age structure of populations is presented in the diagrams (Figure 7).

Three populations (Pop 1, Pop 2, Pop 4) were dominated by generative individuals. Their share varied from 52.4% to 63.6%. In the age spectrum of Pop 3 and Pop 5, virgin individuals prevailed (54.5–62.1%), and the loss of juvenile and immature plants was noted. Incompleteness of the age spectra of these populations is associated with a high degree of anthropogenic disturbance. For example, in 2023, the entire territory of Pop 3 was ploughed, and Agropyron cristatum was sown. As a result, the regeneration of Rh. altaicum has been slow; it is now forming small groups of individuals of different ages.

In Pop 7, the share of generative individuals was very low, only 1.4%. This is most likely an anomalous case associated with the rapid drying of the meadow. Under these conditions, potentially generative individuals did not bloom and remained in a vegetative state.

The total projective vegetation cover in plant communities with Rh. altaicum was quite high, 73–98% (

Table 2. Characteristics of Rh. altaicum populations.

Indicator	Pop 1	Pop 2	Pop 3	Pop 4	Pop 5	Pop 6	Pop 7
Total projective vegetation cover, %	73	90	80	65	70	98	95
Projective cover of Rh. altaicum, %	2	15	0.5	0.5	1.5	3.8	1.2
Area, m2	450	300	1000	4000	800	60,000	2400
Average density of individuals, pcs/m2	2.1	2.7	2.9	1.1	1.1	7.4	7.2

). The projective cover of the studied species was the highest in Pop 2 (15%) and Pop 6 (3.8%). According to the density of individuals, all populations were divided into two groups: with a low, 100–300 pcs/100 m² (Pop 1–5), and high, ≥700 pcs/100 m² (Pop 6–7), density.

3.4. Morphological Variability

The morphological variability of Rh. altaicum was assessed based on several key traits including plant height and the length and width of the lower, middle, and upper leaves. In the studied populations, the plant height averaged 68.75 cm, which is typical of this species (

Table 3. Variability of morphometric features in Rh. altaicum populations.

No	Morphometric Features, cm
	H	LUL	WUL	LML	WML	LLL	WLL
Pop 1
M ± m	71.12 ± 3.83	7.74 ± 0.25	3.28 ± 0.25	11.57 ± 0.39	6.54 ± 0.61	15.12 ± 0.61	6.75 ± 0.49
CV %	16.18	9.82	22.42	10.33	27.77	12.24	21.67
Pop 2
M ± m	74.95 ± 6.02	6.05 ± 0.46	2.89 ± 0.45	14.04 ± 0.94	5.99 ± 0.79	17.07 ± 1.11	6.44 ± 0.59
CV %	26.64	25.16	51.90	22.31	44.23	20.62	29.15
Pop 3
M ± m	52.44 ± 3.2	5.51 ± 0.39	1.88 ± 0.14	12.22 ± 0.59	5.47 ± 0.21	13.41 ± 0.52	5.77 ± 0.48
CV %	18.32	21.34	22.40	14.48	11.57	11.57	25.34
Pop 4
M ± m	84.40 ± 3.66	6.58 ± 0.36	2.82 ± 0.40	10.64 ± 0.72	5.46 ± 0.47	17.54 ± 0.56	7.72 ± 0.52
CV %	13.69	16.48	42.62	21.51	27.10	10.11	21.42
Pop 5
M ± m	54.38 ± 3.69	5.43 ± 0.40	1.59 ± 0.22	14.68 ± 0.90	6.33 ± 0.43	14.50 ± 0.58	6.90 ± 0.30
CV %	20.38	22.05	40.60	18.38	20.40	11.91	13.02
Pop 6
M ± m	80.83 ± 3.37	5.23 ± 0.25	2.23 ± 0.19	12.24 ± 0.48	5.88 ± 0.27	16.55 ± 0.45	6.12 ± 0.45
CV %	12.52	14.17	25.62	11.83	13.54	8.12	21.96
Pop 7
M ± m	61.5 ± 1.73	6.01 ± 0.49	3.02 ± 0.4	10.28 ± 0.48	5.80 ± 0.27	14.99 ± 0.7	7.17 ± 0.58
CV %	10.53	24.24	41.22	13.90	13.93	14.03	24.10
m.av.	65.52	6.08	2.53	12.24	5.92	15.60	6.70
CVav, %	16.89	19.04	35.25	16.12	22.65	12.66	22.38

Note: H—plant height; LUL—upper leaf length; WUL—upper leaf width, LML—middle leaf length; WML—middle leaf width; LLL—lower leaf length; WLL—lower leaf width; CV_av—the average value of the intra-population variability of the trait; Pop– Population.

). In individual populations, it varied from 52.9 (Pop 3) to 84.4 (Pop 4) cm, the coefficient of variation (CV, %) was 16.89%. The length of the lower stem leaf was 15.6 cm and the width was 6.7 cm, which is consistent with the size range typical of the species. The inter-population variability of the former trait was not large: max was 17.5 cm (Pop 4), min was 13.4 (Pop 3). The length of the middle leaf averaged 12.24 cm and the width was 5.92 cm, which was slightly lesser than in the lower stem leaves. The inter-population variability of the latter trait was low: max 6.54 cm (Pop 1), min 5.8 (Pop 7). The length of the upper stem leaf was 6.08 cm and the width was 2.53 cm. The inter-population variability of the latter trait was low: max was 3.28 (Pop 1), min was 1.59 cm (Pop 5). In most populations of Rh. altaicum, the upper leaf width was a highly variable trait (CV of 35.25%). Significant variation was in the middle and lower leaf length (22.65% and 22.38%, respectively). The upper leaf length had low variability in Pop 1, medium in Pop 4 and Pop 6, and high in Pop 2, 3, 5, 7.

Figure 8 illustrates the height distribution of Rh. altaicum in various populations (Pop 1–7) as the most important morphological parameter examined. The populations differed in the median height values. Thus, Pop 2 had the largest median value, which may indicate more favorable growing conditions, while Pop 1 and Pop 3 had lower values, which may indicate less favorable conditions. The outliers displayed as dots outside the whiskers may indicate unusual plants that are significantly different from the rest.

Figure 9 shows correlation between morphological features of Rh. altaicum.

The correlation matrix (Figure 9) shows the relationship between morphometric traits of Rh. altaicum in different populations. The highest positive correlation (significant at p = 0.05) was observed between plant height (H) and lower leaf length (LLL) indicating that taller plants tend to have longer lower leaves. A significant positive relationship was also observed between the upper leaf length (LUL) and width (WUL). The correlations indicate that tall plants have longer lower leaf blades, and the length and width of the upper leaves are positively correlated. Most coefficients were in the range from 0.3 to 0.5, which indicates the presence of moderately strong correlations between morphometric features.

Figure 10 shows the results of the NMDS (Non-metric Multidimensional Scaling) analysis which uses the Bray–Curtis metric to show differences between populations. Populations closer together have more similar data composition (e.g., similar morphological traits or ecological conditions). Populations further apart have more pronounced differences.

According to the data, Pop 5 and Pop 3 have relatively compact groups of points, indicating stability and homogeneity in their morphological or ecological characteristics. Pop 7 and Pop 6 show a scattering of points, which may indicate more diversity within the population or possible outliers. It is notable that some Pop 2 points are distant from the main clusters, which may indicate unique characteristics of individual specimens.

4. Discussion

Rh. altaicum has varying degrees of vulnerability to adverse factors in different parts of its distribution range. This also explains the different state of populations within the entire range and its parts. The phytocenotic environment of this species was recorded by Smirnova et al. [51] in the Saratov region, where 8 and 10 co-occurring species were described in two populations.

In Kazakhstan, the study of Rh. altaicum in natural populations has not been previously conducted. The species was mentioned only by L.A. Demchenko [52] in the descriptions of Elymus repens (L.) Gould communities in the steppe and semi-desert areas of Northern Kazakhstan as part of halophytic grass meadows together with Saussurea amara and Limonium lilacinum (Boiss. & Balansa) Wagenitz growing on flooded salty meadow soils and in lake basins in the Kustanai region.

Earlier, we provided more detailed information about the species composition of plant communities with Rh. altaicum in the Altyn-Dala State Nature Reserve [53]. The communities were only 35 species from 32 genera and 20 families.

In the Karaganda and Akmola regions, plant communities with Rh. altaicum had 67 species and therefore were more species-rich than those described in the earlier studies. The most rich community by species composition was Pop 6 with 27 species and Pop 3 had the least species with 11 species. This is because Pop 6 in flood plains is characterized by high humidity and moderate salinization of dark chestnut soil, which creates environmentally friendly conditions for a more diverse floristic composition. The Pop 3 site, on the contrary, was subjected to a strong anthropogenic influence in the form of plowing, which adversely affected the species composition of the site.

In the studied plant communities, Rh. altaicum occupies an intermediate position between meadow–bog and meadow communities. Among the main formations of the meadow type of vegetation with Rh. altaicum we should mention Elymus repens meadows along extensive flooded depressions. In addition, there were Calamagrostis epigejos (L.) Roth, Bromus inermis Leyss, Phragmites australis (Cav.) Trin. ex Steud, and Juncus gerardii Loisel. meadows.

Depending on the soil moisture gradient, which is the main environmental factor, there is a gradual transition from real meadows to steppe, where Artemisia nitrosa and Artemisia abrotanum L., act as sub-edifiers. The appearance of Artemisia nitrosa is a sign of desertification of steppe areas. This range of habitats of the species studied is confirmed by other researchers [54].

It should be noted that the predominant associations with Rh. altaicum are Elymus communities (mixed-grass and Elymus sp., Elymus sp., Artemisia sp.). The mixed-grass and Elymus spp. association characteristic of Pop 6 is represented by flood meadows under conditions of periodic short-term flooding.

In the Karaganda and Akmola regions, the most frequently co-occurring species in all studied communities were Saussurea amara, Limonium gmelinii (Willd.) O. Kuntze, Lactuca tatarica (L.) C.A. Mey., Juncus gerardii, Elymus repens, Cirsium arvense var. arvense, Calamagrostis epigejos, Artemisia abrotanum, Artemisia nitrosa, Chenopodium album, Glycyrrhiza uralensis, Lepidium latifolium L. The most common dominant species in all communities studied by us and other researchers was Elymus repens [52,53], and common co-occurring species were Lepidium latifolium, Phragmites australis, Saussurea amara, Lythrum virgatum L., Limonium gmelini, Artemisia nitrosa [55].

The shoot length is the important indicator of inter-population variability. In the present study, the mean shoot length was 65.52 cm; it ranged from 52.44 in Pop 3 to 84.4 in Pop 4. Similar results were obtained by Smirnova et al. [51] who found that the plant high was in the range from 42.5 to 125.2 cm. The results suggest substantial differences in plant height in populations from different ecological conditions. In a similar study [53], a positive correlation between plant height and lower leaf length was found; in plants above 80 cm in height, the lower leaf length was 29.0 ± 5.4 cm. The results obtained suggest that taller plants have longer lower leaf blades.

The shoot height of Rh. altaicum (63 cm on average) was quite common for this species; it was found to be an important indicator of population variability. Similar results were presented by Smirnova [51], where the plant height ranged from 42.5 to 125.2 cm. In unfavorable growing conditions, a decrease in the height of Rh. altaicum was observed.

The plant density of Rh. altaicum was relatively low, from 1.1 to 7.4 pcs/m² compared to the average density of Rh. altaicum in the Southern Urals, where the average plant density can reach 69.8 pcs/m² (from 23.5 to 69.8 pcs/m²) [56]. In the Saratov region, the density of Rh. altaicum ranges from 7.1 to 14.8 pcs/m² [51]. Revyakina [33] noted that the density of Rh. altaicum in certain areas of the lake Kulundinskoye shore was 3–4 generative shoots per 1 m².

In all populations studied, there was an almost complete absence of senile and sub-senile individuals, and only in some populations there was the loss of juvenile and immature individuals. The incompleteness of populations is due to the difficulty of diagnosis as well as the increasing anthropogenic load and narrow ecological amplitude of Rh. altaicum. The absence of senile individuals in the age spectrum is associated with ontogenesis reduction due to the rapid death of plants in the old generative state; individuals undergo complete ontogenesis only under favorable growing conditions, sufficiently high soil moisture, and in the absence of anthropogenic disturbances. Field studies also demonstrated that the transition from the middle-aged to the old-age state in Rh. altaicum depends on the ecological conditions of growth and, above all, the drying up of lakes and marshlands. It is possible that this is a reversible process, and the improvement of environmental conditions will lead to partial rejuvenation of some individuals.

In addition to negative environmental conditions, severe damage to the natural populations of Rh. altaicum in the study area is caused by anthropogenic pressure, including unsustainable grazing, haymaking, and plowing. To develop measures for the conservation of any species, information is needed on the number and state of its populations, as well as the degree and type of anthropogenic pressures in unprotected areas. For a commodity species such as Rh. altaicum, it is also necessary to develop a sustainable harvesting approach. Such studies involved Rh. carthamoides in the Russian Altai [57]. As a result, the crucial importance of the state of the vegetative parts of the plant (renewal zone) for the phytocenotic stability of the species was established. In the conditions of increased anthropogenic impact, the vegetative structures are most vulnerable to the negative effects of the latter; therefore, their weakening leads to a suppression of not only vegetative but also seed reproduction, and ultimately not only to a decrease in the number of individuals and raw material reserves but also to a decrease in the genetic diversity of the species.

According to the data obtained, the most favorable conditions for the species under study were at the site of Pop 6 represented by flood plains and characterized by high humidity and moderate salinization of dark chestnut soils. Pop 2 with the highest projective cover of Rh. altaicum can also be described as a favorable habitat for this species. Pop 1 and Pop 4 had a high proportion of generative plants. Therefore, these areas can be used for seed selection and partial collection of Rh. altaicum living plants (partial excavation of rhizomes) for further introduction of the species.

5. Conclusions

The conducted studies showed that the condition of Rh. altaicum populations largely depends on ecological conditions and, most of all, on moisture regime, salinity, and anthropogenic factors. Therefore, the most favorable habitats of the species include well-watered meadows on slightly and moderately saline soils. For the studied species, such conditions were observed in Pop 6, represented by flood meadows, high humidity, and moderate salinity of dark chestnut soil. The least favorable conditions were observed in Pop 7, which is characterized by medium soil salinity, high degree of climate aridity, and strong anthropogenic influence.

Thus, the data obtained have important implications for in further research aimed at studying the adaptive mechanisms of this species and its resistance to changing environmental conditions and contributing to the development of strategies for its conservation.