Current population trends and morphological variability of Gagea alberti (Liliaceae) in KazakhstanAbstract
Gagea alberti is widespread across Kazakhstan, Kyrgyzstan, southern Russia, western China, and Mongolia. In the present study, we investigated the population status of G. alberti based on the morphological traits of five populations from Kazakhstan, each representing a distinct ecological habitat. In the present study, we investigated the population status of G. alberti based on the morphological traits of five populations from Kazakhstan, each representing a distinct ecological habitat. High variability in traits such as plant height, number of flowers, and leaf and petal sizes indicates the plasticity of the species and its ability to adapt to unstable environmental conditions. Despite significant morphological variability, taxonomic traits, such as bulb structure and cross-sectional shape of the basal leaves, remain stable. Populations growing under extreme conditions demonstrate unique adaptations, such as the development of sclerified roots, which allow them to effectively use condensed moisture and survive in arid conditions. This study provides new insights into the morphological variability and adaptive mechanisms of G. alberti, which are essential for understanding its evolutionary processes and preserving the species in a changing environment.
Keywords:
ecology; environmental adaptation; habitat; morphological traits
Resumo
Gagea alberti é amplamente distribuída por Cazaquistão, Quirguistão, sul da Rússia, oeste da China e Mongólia. No presente estudo, investigamos o estado populacional de G. alberti com base nas características morfológicas de cinco populações do Cazaquistão. Cinco populações diferentes foram estudadas em cinco habitats ecológicos. A alta variabilidade em características, como altura da planta, número de flores e tamanhos de folhas e pétalas, indica a plasticidade da espécie e sua capacidade de adaptação a condições ambientais instáveis. Apesar da significativa variabilidade morfológica, características taxonômicas, como a estrutura do bulbo e a forma da seção transversal das folhas basais, permanecem estáveis. Populações que crescem em condições extremas demonstram adaptações únicas, como o desenvolvimento de raízes clarificadas, que lhes permitem utilizar eficazmente a umidade condensada e sobreviver em condições áridas. Este estudo fornece novos insights sobre a variabilidade morfológica e os mecanismos adaptativos de G. alberti, que são essenciais para a compreensão de seus processos evolutivos e para a preservação da espécie em um ambiente em mudança.
Palavras-chave:
ecologia; adaptação ambiental; habitat; características morfológicas
1. Introduction
The genus Gagea Salisb. belongs to the Liliaceae family and is characterized by the highest degree of polyploidization, with exclusively diploid species in early divergent groups and undecaploids (11x) in terminal groups (Peruzzi et al., 2009). The existence of fully polyploid terminal groups and different polyploid series in several species of Gagea illustrates the dynamic evolution of the genus’ genome (Peruzzi, 2003, 2008). Therefore, many members display high phenotypic and genetic variability (Peterson and Peterson, 1999).
A total of 63 species of Gagea have been recorded in Kazakhstan (Kubentayev et al., 2021), with the majority distributed in the mountainous regions of southern Kazakhstan. The vast plains of northern and central Kazakhstan are home to no more than 14 species (Kupriyanov, 2020; Alibekov et al. 2025), including the recent records of G. tenera Pascher and G. kamelinii Levichev. (Kubentayev et al., 2023; Nobis et al., 2025). Among the Gagea species in Kazakhstan, only four are national endemics: G. almaatensis Levichev, A. Peterson, & J. Peterson, G. ularsaica Levichev, G. azutavica Kotukhov, and G. iliensis Popov. (Kubentayev et al., 2024a; Sumbembayev et al., 2025). In addition, in 2025, another narrow endemic from the mountains of Karatau in southern Kazakhstan, G. kotuchovii Kubentayev et Levichev, was described (Kubentayev et al., 2025a). Only G. neopopovii Golosk. is protected at the state level in the country (Baitulin, 2014).
Gagea alberti Regel is widespread across Kazakhstan, Kyrgyzstan, southern Russia, western China, and western Mongolia (Kubentayev et al., 2025b). The higher classification of this species belongs to the well-differentiated section Plecostigma (Turcz.) Pascher (Peterson et al., 2016). Gagea alberti was described by Regel in 1880 based on his collections in the vicinity of Kuldzha (northwestern China, near the border with Kazakhstan). This species is characterized by high ecological plasticity and phenotypic variability, making it an important species for studying evolutionary processes and the mechanisms of adaptation. Gagea altaica Schischk. & Sumnev. and G. sarysuensis Murz. have recently been regarded as synonyms of G. alberti because of its ecological forms (Kubentayev et al., 2025b). The global conservation status of Gagea alberti has been listed as Least Concern (Kubentayev et al., 2025b).
Plant variability, both phenotypic (external characteristics) and genotypic (DNA level), plays a vital role in the ability of plants to adapt to environmental changes (Nicotra et al., 2010). Representatives of the relatively young and actively diverging Gagea exhibit reasonably high natural morphological variability (Wörz et al., 2012; Levichev, 2013; Peterson et al., 2016). This is because of the patterns of morphological variability in ontogenesis, polyploidization, and hybridization (Levichev, 1999, 2011; Peterson et al., 2008, 2011, 2016; Peruzzi et al., 2011). Some studies have mentioned the phenotypic variability of some Gagea species from Europe and the Mediterranean (Peterson and Peterson, 1999; Peterson et al., 2010; Wörz et al., 2012; Stojanović, 2020; Horák et al., 2023). However, studies on the intraspecific variability of representatives of Gagea in Central Asia are lacking.
To fill this gap, we studied G. alberti phenotypic variability and its mechanisms of adaptation to various habitat conditions in Kazakhstan. These results will allow us to better understand the mechanisms underlying the evolution and adaptation of this species. They also have practical significance for developing measures to preserve biodiversity in the face of anthropogenic impacts and global climate change.
2. Materials and Methods
2.1. Study area
Field studies were conducted in three administrative regions (Karaganda, Ulytau, and Kyzylorda) of central and southern Kazakhstan between 2020 and 2024 (Table 1). In central Kazakhstan, the study area fell within the central part of the “Kazakh Uplands.” The region’s terrain is diverse, encompassing vast plains, steppes, and prominent mountainous and elevated areas. These geographical features shape watersheds and river valleys and contribute to the variety of landscapes, including semi-desert and steppe zones. The climate in the region is continental, with cold winters (temperatures can drop to –30 °C and below) and hot and dry summers (often exceeding 30 °C). Precipitation is low, making the region dry (Kupriyanov, 2020).
In southern Kazakhstan, research was conducted in the Shieli district of the Kyzylorda region, in the middle reaches of the ancient Syrdarya River. This area has a continental climate within the natural desert zone. In summer, the temperature can reach high values (35–40 °C); in winter, it can fall to –20 °C and below. In the zoning system of the Sahara-Gobi Desert region, this territory belongs to the Irano-Turan subregion (Rachkovskaya, 2006). This site is characterized by sandy hill formations with poorly fertile sandy soils, rendering it very sensitive to climate change, such as drought or sudden temperature changes.
We examined five populations (Pop 1– Pop 5) of G. alberti under various ecological conditions (Figure 1) using generally accepted geobotanical methods for plant populations (Kashin et al., 2015; Aidarkhanova et al., 2022). Traditional field geobotanical research methods with an ecological-physiognomic approach were used to detect phytocoenotic features. Plant communities were classified into ecological and physiognomic types, each dominated by species from one ecobiomorphic and ecologically related group. Medium-density individuals were also considered. The number of adult plants per square meter was determined using 30 replicates for each population. The soil types associated with each population in Kazakhstan were named according to the classification of Pachikin et al. (2014).
The condition of the studied populations was assessed according to the methodology of Kashin et al. (2015), depending on the level of anthropogenic impact. This methodology uses a simple classification of population condition that includes four categories: unstable (degrading) condition, moderate condition, good condition (close to background), and background, that is, undisturbed, condition.
2.2. Phenotypic variability study of G. alberti
The basal leaf morphology and shoot structure of Gagea species provide profound insights for taxonomic research (Zarrei et al., 2010; Levichev, 2013; Qiu et al., 2023). Therefore, to study the phenotypic variability of G. alberti, the morphological parameters of the basal and cauline leaves were measured along with plant height (cm), number of flowers, and flower petal size. To study morphological parameters, 30–40 middle-aged plants were selected from each population during the flowering period.
2.3. Statistical analysis
Statistical processing was performed using the nonparametric Mann–Whitney U test to determine the significance of differences in floristic composition and morphological indicators between the studied populations. Box plots were generated using the ggplot2 package in R v. 4.3.1 to illustrate the observed variation (Wickham, 2016; R Core Team, 2024). Correlation coefficients were calculated using the corrplot package after completing the primary data analysis. A cluster tree was generated using the neighbor-joining method to evaluate morphological similarities among populations (Saitou and Nei, 1987). All analyses were conducted using the ape and ggtree packages in R (Yu et al., 2017; Paradis and Schliep, 2019).
3. Results
3.1. Ecological and phytocoenotic characteristics of habitats and abundance of G. alberti
Gagea alberti has high ecological plasticity and significant morphological variability. Table 2 presents the floristic composition of communities containing G. alberti. It must be noted that the floristic composition is relatively poor in species diversity, which is associated with the very early spring vegetation of G. alberti.This species was found in various habitats, and five ecological types were distinguished (Table 3). The number of individuals in a population is a key indicator of its condition and was used to assess the condition of the population. The characteristics of the five studied populations of G. alberti are described below.
Pop 1 grew on the foothill terraces of granite uplands (Figure 2A) along cracks in granite rocks in light chestnut diluvial rubble soils. The soil comprised small fragments of granite rocks washed from the mountains by meltwater and accumulating at the foot of hills and in gorges. The slope faces southwest and has an inclination of 3–5º. There was some grazing in this area, but this did not significantly affect the status of the G. alberti populations.
Gagea alberti in Kazakhstan: A. Pop 1, B. Pop 2, C. Pop 3, D. Pop 4 and E. Pop 5. (1, general habits; 2, 3, general appearance; 4, 5, flowers; 6, basal leaf transverse section; and 7, stem cross-section).
Pop 2 grew on a flat plain in a semi-desert dominated by Artemisia terrae-albae Krasch and Krascheninnikovia ceratoides (L.) Gueldst on dark chestnut, loamy, and solonetzic soils (Figure 2B). The soils were shallow, with a high proportion of small pebbles, stones, and rubble. This area is subjected to cattle grazing.
Pop 3 grew on sandy hills in the middle reaches of the ancient Syrdarya River (Figure 2C). G. alberti was found in the undergrowth of sparse stands of Populus diversifolia Schrenk in light brown sandy alluvial soils. In this population, cattle consumed the vegetative mass of plants.
Pop 4 grew on the northwestern slope (inclination 10–15º) and on the top of the low Targyl Hill on the northern shore of Lake Balkhash (Figure 2D). The area’s relief is uneven, shaped by outcrops of ancient, heavily weathered rocks and large stone fragments. The soil is characterized by a short profile with strong stoniness. This is due to the shallow depth of dense soil-forming rocks on the surface, which emerge toward the top of the hill. The soils were poorly developed, stony-gravelly, dark chestnut. The vegetation in this area is poorly developed because of the thin humus layer and severe aridity. Cattle grazing was observed in the lowlands and on gentle slopes, but this did not significantly affect the state of the G. alberti population.
Pop 5 grew on alluvial plains or in depressions in highly saline soils (Figure 2E). The site is characterized by an almost flat relief with winding flat-bottomed depressions. The soils at this site were loamy, meadow-chestnut, and solonetzic-saline. The vegetation was very sparse, with no more than ten species recorded. The community containing G. alberti was dominated by the halophytic species Atriplex cana CA Mey., and Artemisia nitrosa Weber ex Stechm. The state of the G. alberti populations was assessed as satisfactory. The site is located near the village of Sarlyk and is subjected to anthropogenic impacts in the form of grazing and trampling by the local population.
Pop 4 was exposed to optimal growth conditions for G. alberti, growing on the slopes and tops of dry, stony/rocky hills on poorly developed dark chestnut soils. Extreme habitat conditions for G. alberti were noted in Pop 5 on flooded salt marshes with halophytic vegetation, where the lowest density of plants was observed (1.14 ± 2.8 individuals per m2). This species appears to be poorly adapted to saline soils with excessive moisture content.
The floristic composition of communities with G. alberti in all populations varied significantly owing to different habitat conditions. Among all the populations studied, Pop 3 stands out because of its ecological characteristics and the phytocoenotic characteristics of the community, which were examined on the hummocky sands in the middle reaches of the ancient Syrdarya River. These features are likely influenced by the substantial removal of this population to the south and the prevailing desert habitat conditions.
Populations 1, 2, and 3 were assessed as stable. Anthropogenic disturbance in these areas was moderate, resulting primarily from grazing. The moderate level of grazing did not significantly affect these populations of G. alberti. The state of the G. alberti population in Pop 4 was assessed as good, with the highest observed abundance (18.9 ± 2.8 individuals per m2). Pop 5 was assessed as unstable (degrading). This location is near the village of Sarlyk and is subject to anthropogenic impacts, such as heavy grazing and trampling.
Pop 3 grew on brown soils, whereas the other four populations grew on dark or light chestnut soils. Soil type did not seem to play a major role in the variability of the species. However, variations in other components of the soil substrate, such as rubble content, sandiness, stoniness, the proportion of loam, and salinity, appear to play a crucial role in shaping species variability and determining population structure.
3.2. Morphological variability and adaptive strategies of G. alberti
Table 4 presents the results of the analysis of the morphological parameters of the five populations of G. alberti. Plant height, number of flowers, and the size of the leaves and flower petals were studied.
Morphological parameters of the five G. alberti populations (Values shown as M ± m / Min–Max).
Plant height varied across populations, with the greatest variation observed in population 4 (mean ± SD, range: 8.44 ± 3.56 cm, 3–15.2 cm). Pop 5 exhibited the least variable plant heights (5.19 ± 0.922 cm, 4.1–7 cm). The number of flowers also varied between populations. Plants in Pop 3 had the most flowers (3.53 ± 1.35 flowers, 2–6 flowers), whereas the fewest flowers were observed in Pop 1 (1.2 ± 0.41 flowers, 1–2 flowers). These findings may indicate differences in reproductive strategies or adaptations to different environmental conditions. The populations also varied significantly in leaf length and width. Pop 2 had the largest mean basal leaf length (14.88 ± 190 cm, 10–17.2 cm) and width (0.29 ± 0.021 cm, 0.18–0.26 cm). The greatest mean cauline leaf length was observed in Pop 2 (5.44 ± 0.95 cm, 3.3–7.4 cm), and width was observed in Pop 5 (0.22 ± 0.020 cm, 0.18–0.25 cm). The length and width of the perianth petals also differed between the populations. Pop 4 had the greatest mean perianth petal length (1.32 ± 0.382 cm, 0.8–2.1 cm), and the greatest mean petal width was observed in Pop 3 (0.24 ± 0.03 cm, 0.21–0.34 cm). These differences may be due to the variation in pollinators or the plants’ adaptations to different environmental conditions.
Among the morphological parameters considered, plant height and number of flowers were the most significant. These parameters are directly related to the plants’ competitiveness and reproductive success and show significant variability between populations, which may reflect their adaptation to different environmental conditions. Therefore, plant height and the number of flowers are key morphological traits that should be considered when studying the ecology and adaptation of G. alberti populations.
Figure 3 presents boxplots illustrating the morphological parameters of G. alberti across the five assessed populations. These boxplots visualize the distribution of the data, highlighting the interquartile range, median, and potential outliers. Plant height varies considerably among the populations; Pops 2, 3, and 4 exhibited greater variation, whereas Pop 1 and Pop 5 had narrower height ranges. This may suggest more stable environmental conditions or lower genetic diversity in the latter populations.
Boxplots showing variation in morphological parameters of Gagea alberti across the studied populations (Pop1–Pop5). (A) Plant height (cm); (B) Number of flowers (pcs); (C) Basal leaf length (cm); (D) Basal leaf width (cm); (E) Stem leaf length (cm); (F) Stem leaf width (cm); (G) Petal length (cm); (H) Petal width (cm).
The greatest variability in the number of flowers was observed in Pops 3 and 4, potentially reflecting the influence of diverse environmental conditions or genetic factors on the reproductive traits of these populations. The number of flowers in Pops 1, 2, and 5 was more consistent, suggesting more uniform environmental conditions or limited genetic variation. The number of flowers is an important morphological parameter, as it directly influences reproductive success: a greater number of flowers increases the probability of pollination and subsequent seed production, which is vital for population survival and dispersal.
Plant height was positively correlated with the number of flowers and cauline leaf length (Table 4, Figure 4). This means that tall plants had more flowers and longer cauline leaves than short ones. The number of flowers was positively correlated with cauline leaf width. This indicates that plants with more flowers had wider cauline leaves than those with fewer flowers. Basal leaf length was positively correlated with basal leaf width and cauline leaf length. This indicates that long basal leaves are generally broad and accompanied by long cauline leaves.
Correlation matrix of morphological parameters measured in five G. alberti populations. The color and size of the circles indicate the correlation’s magnitude and direction of the correlation, respectively. Pop, population; PH, plant height; NF, number of flowers; LBLL, basal leaf length; LBLW, basal leaf width; SLL, stem leaf length; SLW, stem leaf width; FPL, flower petal length; FPW, flower petal width.
The neighbor-joining analysis revealed that Pop 1 has unique morphological traits that distinguish it from the other four populations (Figure 5). This could be explained by the high average values for most parameters, such as the length and width of the basal and cauline leaves and perianth petals. Pops 1 and 5 had more features in common with other populations, especially Pop 1 with Pop 4 and Pop 5 with Pop 3, which is explained by their morphological similarity, all having small average parameter values. Pop 4’s high variability in morphological parameters was notable and was reflected in the dendrogram.
Pop 3 was distinguished by its morphological parameters, particularly the pronounced influence of cauline leaf width. This pattern may reflect adaptive or genetic differentiation within the population, likely driven by its desert habitat. G. alberti in Pop 3 grows on sandy hills in the middle reaches of the ancient Syrdarya River. To survive such extreme conditions, these plants exhibit strongly developed clarified roots (apogeotropically thickened roots that absorb atmospheric moisture, accumulate nutritious organic matter near the bulb, and protect against mechanical damage).
Pops 1 and 5 shared similar characteristics across most morphological parameters, except for plant height and number of flowers. These observations underscore the importance of plant height as a key morphological trait, as it may serve as an indicator of both genetic diversity and adaptation to environmental variation.
4. Discussion
Morphological parameters such as plant height, number of flowers, leaf length and width, and flower petal size provide important information about the adaptive abilities of different populations to their habitat conditions (Sultan, 2000; Valladares et al., 2007; Nicotra et al., 2010). For example, G. alberti in Pop 4 is characterized by highly variable plant heights, possibly due to changing environmental conditions in this population. High degrees of variability may indicate substantial genetic diversity or adaptation to unstable environmental conditions. In contrast, populations with less variability in height (e.g., Pop 5) may be more resistant to environmental conditions.
Significant correlations between morphological traits (e.g., plant height and number of flowers) indicate that these parameters are interrelated and may influence the reproductive success of populations, which is consistent with the findings of Fairhurst et al. (2022) and Osmonali et al. (2025). Such relationships are important for understanding the influence of ecology on plant survival and dispersal. Correlations between leaf parameters (basal and cauline) indicate the existence of synergies in the development of these traits, which is an important feature for plant adaptation to specific environmental conditions. For example, long basal leaves in Pop 2 may be associated with wide cauline leaves, which in turn may contribute to increased plant photosynthetic activity under water-stressed conditions.
Plant height, leaf lengths, and number of flowers demonstrated high intra- and interpopulation variability. This is consistent with the data on morphological variability of G. pratensis (Stojanović, 2020). Conversely, flower petal size and leaf width were characterized by relatively low variability.
Of particular interest is Pop 3, which grew under extreme desert conditions on sandy hills. Plants of this population had strong clarified roots that absorb moisture from the air and protect the plant against mechanical damage. Similar adaptations have been described in detail in other species of the genus Gagea by Levichev and Kurbaniyazova (2022). In contrast to the main roots, which absorb nutrients and moisture from the soil, sclerified roots demonstrate negative geotropism; they tightly braid the bulb and end near the soil surface (Levichev, 1999). The position and geotropic orientation of the clarified root ensure the collection of the smallest doses of moisture of any origin (Levichev, 1982). Sand naturally contains varying degrees of air cavities, where water vapor condenses because of temperature fluctuations between day and night. The unique structural features of the clarified root allow it to capture and retain this condensation (and drops of rain, fog, or morning dew) in the surface layer of the soil. Once absorbed into the thick-walled root cells, the moisture is retained and cannot evaporate. The transport of this moisture through the pores in the walls and the enfilade of empty cells into the living tissues of the replacement bulb is not hindered and occurs according to the capillarity principle.
Notably, in Pop 4, G. alberti plants are very short (2.8 ± 0.8 cm) close to the top of the hill, whereas on the slopes and closer to the base of the hill, they were relatively tall (8.5 ± 0.8 cm). This is likely a result of the low soil fertility and significant wind exposure at the top of the hill. Small specimens of G. alberti (up to 3 cm in height) were also found on the gravelly banks of streams and rivers, which also have poorly fertile soil.
It was found that the soil type did not play a major role in the variability of the species, which is consistent with the findings of Peterson et al. (2010). However, additional soil substrate components, such as rubble, sand, stones, loam, and varying levels of salinity, play a very important role in shaping species variability and influence population structure.
Despite G. alberti significant morphological variability at the population level, the structure of the bulb, cross-sectional shape of the basal leaves, and peduncle have remained unchanged and are considered reliable taxonomic characteristics of the genus Gagea (Levichev 1999, 2001, 2002, 2005). Differences in some morphological parameters, such as the size of the cauline and basal leaves, presence of clarified roots, and number of flowers, were due to the habitat conditions of the studied populations. The size and shape of the basal leaves of G. alberti observed in our study are consistent with those reported from China by Qiu et al. (2023). Similar manifestations of pronounced morphological variability have also been reported in genera closely related to Gagea within the family Liliaceae, particularly in some tulip species (Tulipa), especially representatives of Tulipa sect. Biflores, where environmentally driven variation substantially complicates species delimitation and reliable identification (Kubentayev et al., 2024b).
5. Conclusions
This study revealed significant morphological differences between populations of G. alberti, caused by adaptations to various environmental conditions. The high morphological variability of traits such as plant height, number of flowers, and leaf and petal sizes indicates the plasticity of the species and its ability to adapt to unstable environmental conditions. Populations growing under extreme conditions demonstrated unique adaptations, such as the development of clarified roots, which allow them to effectively use condensed moisture and survive under arid conditions. The results of this study provide new insights into the morphological variability and adaptive mechanisms of G. alberti, which are important for understanding evolutionary processes and preserving the species in a changing environment.
Acknowledgements
This research was supported by research grants from the Science Committee of the Ministry of Science and Higher Education of the Republic of Kazakhstan (Grant No. AP26101537), as well as partially by the institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences, “Systematics, flora and plant resources of the vascular plants of Eurasia” (125020701739-5), the Korea National Arboretum (Project No. KNA1-2-49-25-2), and the Korea Basic Science Institute (National Facilities and Equipment Center) grant funded by the Ministry of Education (Grant No. 2023R1A6C101B022).
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Data Availability Statement
The data supporting the findings of this study are available from the corresponding author upon reasonable request.
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Edited by
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Editor:
Jairo Lizandro Schmitt
The data supporting the findings of this study are available from the corresponding author upon reasonable request.
