Biology of Scutellaria baicalensis Georgi (Lamiaceae) from Different Ecological and Geographical Places of Growth during Introduction

Abstract

The variability in the development of Scutellaria baicalensis Georgi (Lamiaceae) plants collected from natural habitats (Zabaykalsky krai, Amur oblast, and Primorye) and grown under the same culturing conditions (Novosibirsk) is analyzed. It has been found that interpopulation differences in morphological characteristics of S. baicalensis and the timing of the onset of phenophases developed in nature are preserved under new growing conditions. Data analysis shows the existence of significant differences (t > 3) between the steppe Zabaykalsky and forest Primorye coenopolations (CPs) in plant height, number of pairs of leaves, and number of shoots, both in nature and during introduction. The flowering period in the Zabaykalsky CPs comes earlier than in the Primorye CP, both in nature and in culture. Individuals of Zabaykalsky CPs bloom in early July in culture. The flowering period in the Primorye CP begins at the end of July–August; the seed ripening period is extended, especially in the first years of introduction. It is possible to allow the formation of steppe Zabaykalsky and forest Primorye ecotypes.

The study of plant behavior under climate change in different parts of the range is important both for understanding microevolutionary processes within species; the possibility of predicting plant development processes; and the practical application in horticulture, agriculture, forestry, and the fight against invasive species (Korsakova, 2019; Park et al., 2019).

Introduced plants, entering new conditions of temperature amplitudes, moisture regimes, spectral compositions of light, soil cover, and other abiotic factors, begin to experience unusual effects of seasonal climate rhythms, which cannot but affect their growth, development, and productivity.

Scutellaria baicalensis Georgi (family Lamiaceae) is a tap-rooted herbaceous perennial plant with sympodially growing generative monocyclic shoots. The range of the species is Mongolian–Daurian–Manchurian. S. baicalensis is widespread in China (Zhili, Shentung), northeastern Mongolia, Dauria, Manchuria, and Japan (Illyustrirovannaya…, 2009). Three of its fragments enter the territory of Russia: in Eastern Zabaykalsky (Zabaykalsky krai), the Middle Amur Region (Amur oblast), and southwestern Primorye (Primorsky krai).

The species is a valuable medicinal plant used both in folk and modern medicine in different countries. Flavonoids are its main active ingredients. S. baicalensis has a wide spectrum of pharmacological activity. It is used as an antihypertensive and sedative drug and as a hemostimulator in antitumor therapy (Goldberg et al., 1994; Razina and Pshenichkina, 1989). Extracts have antioxidant and anti-inflammatory activity (Gao et al, 1999; Yoon et al., 2020) and a hepatoprotective effect (Potapova, 2016), as well as an antibacterial effect against a number of pathogenic species of human microorganisms (Kim et al., 2009). It was also found that the active substances of S. baicalensis in vitro act on the SARS-CoV19 virus, blocking the viral attack and preventing the proliferation of the virus (Song et al., 2020).

A number of researchers have studied the ecological, biological, and phytocoenotic features; age structure; and biological and operational stock of species populations, ontogeny, raw and seed productivity, biological activity, and flavonoid content of coenopolations (CPs) of S. baicalensis in Zabaykalsky krai, Amur oblast, and Primorsky krai (Banaeva, 1994; Bukhasheeva et al., 2007; Manyakhin, 2010; Shishmarev, 2012).

The study of the development of the species under the same cultural conditions is of particular interest, because the studied CPs were located in different geographical points differing in natural and climatic conditions.

The purpose of this study is to analyze the variability of morphological characteristics and the rhythm of seasonal development of S. baicalensis specimens collected in different ecological and geographical conditions of growth during introduction.

MATERIAL AND METHODS

To study the development under the same culture conditions, plant seeds were collected in natural CPs of S. baicalensis of Zabaykalsky Krai (near the villages of Bishigino, 51°51′12″ N 116°26′28″ E; Borzya 50°23′ N 116°32′ E, and Verkhnie Klyuchi 51°57′41″ N 116°45′56″ E, and the Krasnokamensk railway station 50°04′21″ N 118°13′42″ E), Amur oblast (near the city of Svobodny 51°23′ N 128°08′ E), Primorsky krai (near the village of Komissarovo 44°59′24″ N 131°47′05″ E) and then sown in the experimental plot of the Central Siberian Botanical Garden (CSBG), Novosibirsk (TsSBS 54°49′33″ N 83°06′34″ E).

Phenological observations were carried out in 1987–2005 according to (Beideman, 1974). The average daily air temperature and precipitation during the periods of passage of the phenophases of the species were analyzed according to the average long-term data (Archive…, 2022; Weather…, 2022). Location of meteorological stations: Borzya, 50°40′ N 116°50′ E, 676 m a.s.l. (Zabaykalsky krai); Svobodny 51°45′ N 128°10′ E, 200 m a.s.l. (Amur oblast); the settlement of Pogranichny 44°40′ N 131°30′ E, 211 m a.s.l. (Primorsky krai); Novosibirsk planetarium 54°98′ N 83°03′ E, 160 m a.s.l. (Novosibirsk oblast).

RESULTS

The study areas differ in climatic characteristics (Fig. 1).

Fig. 1.

Climatic characteristics of the study areas.

The climate of Zabaykalsky krai is sharply continental with insufficient moisture, a long duration of sunshine per year, and significant fluctuations in daily and annual air temperatures. Winter is cold and long, with little snow; spring is warm, short, dry, windy; and summer is warm, dry in the first half, with precipitation in the second. The predominance of direct solar radiation causes intense heating of the soil surface, which contributes to the early thawing of the upper horizons. The average annual air temperature in the study area is negative (about –1.5°С). Frosts are possible in early June. About 350 mm of precipitation falls per year. Up to 80% of the annual rainfall falls in July–August. In winter, precipitation is rare; the depth of snow cover does not exceed 10–15 cm. The growing season is about 150 days. Chestnut, chernozem soils predominate, meadow-chernozem, gray forest soils are common, solonchaks, solonetzes and meadow-alkaline soils are often found.

Amur oblast is characterized by an ultracontinental climate with monsoon features, a significant amount of sunshine, and large amplitudes of daily and annual temperatures. Winter is cold, with little snow; there are frequent sharp temperature changes associated with the invasion of cyclones in spring; summers are mostly hot. The average annual air temperature in the study area is –0.2°С. The growing season lasts an average of 140 days. The last frosts are possible until the end of April and the first at the end of September. The annual rainfall is over 550 mm. Precipitation falls mainly during the warm period. In winter, the average snow cover reaches 12 cm. Brown forest and podzolic-brown forest soils predominate in the study areas.

The climate of the cis-Khanka Plain of Primorsky krai is monsoonal. This region is characterized by uneven precipitation and periodic droughts, especially in spring and the first half of summer, and large fluctuations in seasonal and daily temperatures. Winter is with little snow, spring is cool and dry, and summer is hot. The average annual air temperature is 4.8°C. The last frosts are observed at the end of April, but they are possible in June. The average annual rainfall is over 450 mm. Precipitation often falls in the form of showers, mainly in the second half of July–August. The duration of the growing season is about 188 days. The height of the snow cover is 10–12 cm. Soils are meadow–soddy, meadow gley podzolized, and brown–podzolic.

CSBG is located in the forest-steppe zone of Western Siberia in a moderately cool and moderately humid agroclimatic region. The climate of the forest-steppe zone is characterized by sharp continentality with significant fluctuations in seasonal and daily temperatures. Winters are long and cold; summers are short and hot. The average annual air temperature is 2.6°С. The last spring frosts are observed in the first decade of June; the first autumn frosts are observed in the second half of September. The growing season lasts an average of 158 days. The growing season begins in late April–early May. Precipitation in May falls in the form of rain and sleet. Annual rainfall averages about 400 mm. The average snow depth is 35 cm. The soils on the territory of the CSBG are predominantly soddy–podzolic and gray forest (Рh 5.5–6.9) (Rastitel’noe…, 2014).

The natural features of Zabaykalsky contributed to the formation of local steppe vegetation. The Zabaykalsky CPs were located in open steppe areas and slopes of hills. Individuals of the Amur and Primorye CPs grew under more mesophytic conditions. The Amur CP Svobodny was confined to the forest-steppe zone. The Primorye CP Komissarovo was confined to the oak woodlands.

The formation of generative organs, flowering, and ripening of fruits and seeds are the most important phases of plant development during the growing season.

According to the Popov Herbarium of the Central Siberian Botanical Garden, Siberian Branch, Russian Academy of Sciences (CSBG SB RAS) (NSK), Novosibirsk; the Krasnoborov Herbarium, CSBG SB RAS (NS), Novosibirsk; the Krylov Herbarium of Tomsk State University (TK); the Herbarium of the Institute of Biology and Soil Science of the Far Eastern Branch, Russian Academy of Sciences (FEB RAS) (VLA), Vladivostok; collections of employees of the Pacific Institute of Bioorganic Chemistry of the FEB RAS, Vladivostok; the Herbarium of the Regional Chita Museum of Local Lore (Lekarstvennye…, 1990); and the author’s own observations, it was found that the onset of phenophases in individuals of S. baicalensis in Zabaykalsky occurs two weeks earlier than in Primorye. Therefore, plant budding is observed in Zabaykalsky in the second decade of June; flowering is observed in July and until mid-August. In Primorye, plants bud in early July and flowering occurs in mid-July.

During the introduction, the following phenological states were identified for individuals of all studied CPs: spring regrowth, budding, flowering, fruiting, and summer–autumn regrowth.

Features of the rhythm of development of S. baicalensis individuals in different CPs under the same culture conditions manifested in different periods of onset and duration of individual phenophases (Fig. 2).

Fig. 2.

Phenological spectra of S. baicalensis during introduction on average for 1987–2005.

DISCUSSION

It can be seen from the presented data that the climatic conditions of natural habitats and the area of introduction of S. baicalensis differ significantly from each other in the sum of positive temperatures, the amount of precipitation, and the duration of the growing season.

Morphological characteristics of specimens of natural and introduced CPs are given in (Pshenichkina and Pshenichkin, 2018). Data analysis shows the existence of significant differences (t > 3) between the steppe Zabaykalsky and forest Primorye CPs in plant height, the number of shoots per individual, and the number of pairs of leaves per shoot, both in nature and during introduction. The height of the plants of the Zabaykalsky CP group averaged 37 cm, the number of shoots was 17–18, and the number of pairs of leaves was 17. Individuals of the Primorye CP Komissarovo were taller (on average 65 cm in height), with a smaller number of shoots (up to 13 pieces) and pairs of leaves (up to 15 pieces). Characteristics of individuals of the Amur CP Svobodny have intermediate values.

The ontogenesis of S. baicalensis has four periods and nine age states: seedlings, juvenile, immature, virginal, young and middle-aged generative, senile, and quasi-senile (Banaeva, 2000; Bukhasheeva, 2000).

A number of studies have revealed the influence of regional and local climatic factors on the ontogenetic structure of S. baicalensis (Sandanov et al., 2017; Sandanov and Rosbakh, 2019). It was determined that seed renewal in S. baicalensis is significantly reduced with an increase in continentality and, accordingly, an increase in the aridity of the climate, which leads to a decrease in the number of individuals of the pregenerative period and an increase in the proportion of virginal and senile individuals.

Our studies have shown that the maximum in the age spectrum in the Zabaykalsky CP group falls on generative young individuals (40–60% of the total number of individuals). The Amur and Primorye CPs have two-peak spectra. The first maximum falls on the immature age group (Svobodny 30%; Komissarovo 17%) and the second—Svobodny for the generative young (27%) and Komissarovo for the generative middle-aged group (33%).

The course of ontogeny during introduction is the same for all CPs transferred from different ecological and geographical conditions of growth. However, there is a sharp acceleration of ontogeny in culture caused by a reduction in the length of time an individual stays in a particular age state. These processes are typical for introduced species.

As early as in the first year of life in culture, S. baicalensis specimens of all studied CPs bloom and produce seeds, whereas the transition of individuals to the generative state in nature begins at 10–15 years of age. Observations have shown that the timing of the onset of phenological phases, in particular, flowering (in the first year of life, when plants go through the stages of development from a seedling to a generative young state) occurs several days later than in subsequent years for this CP. As can be seen from the phenospectra (Fig. 2), the time from spring regrowth to the beginning of flowering is not the same for different CPs. The shortest period (35 days) is observed in plants of the Zabaykalsky group of CPs. These plants grew in rather harsh conditions and did not require much heat to transition to flowering. The sum of positive temperatures averaged 45°C for Novosibirsk, 43°C for Zabaykalsky krai, 50°C for the Amur oblast, and 40°C for Primorye. The average June temperature is 16.3°C in Novosibirsk, 15.5°C in Zabaykalsky region, 17.8°C in the Amur oblast, and 13.0°C in Primorye. The average air temperature in Primorye reaches 17.5°C only in July, which can explain the later flowering of S. baicalensis there compared to Zabaykalsky krai.

Individuals cultured in Zabaykalsky CPs bloom within 7–20 days from the beginning of July. Plants growing in Primorye have developed a greater demand for heat and moisture in the process of evolution, which affected the culture conditions on the duration of the period from regrowth to flowering, which increased to 40 days. Plants of the Primorye CP Komissarovo, both transferred to the culture and growing in nature, bloomed later than the Zabaykalsky plants (in late July–August). Their flowering period was more extended (up to 60 days).

Apparently, the selection in the process of evolution in the harsh conditions of Zabaykalsky took place with the shortening of the growing season. Precocity was even more evident in culture. Thus, the flowering of the main shoot in plants of the Zabaykalsky group growing in nature occurs in July, while in culture conditions it happens much earlier (from the end of June).

The difference in the timing of flowering in the CPs over the years ranged from 3 to 5 days, depending on weather conditions. A reduction in the duration of phenophases, as well as earlier dates for their onset, were observed during the study for all plants, both Zabaykalsky, Amur, and Primorye. This is explained by the changes in the regional climate caused by global warming. Thus, it was found that the average daily air temperature in Novosibirsk increased by 0.16°C over the period from 1996–2015, the vegetation period lengthened by 12 days, and the active vegetation period of plants increased by 8 days (Fomin and Fomina, 2021). There was a shift in the limits of variability of S. baicalensis in the prefloral period and the duration of the flowering period. However, interpopulation differences in the timing of the onset of phenophases between the steppe Zabaykalsky and forest Primorye CPs persisted with the introduction of S. baicalensis.

CONCLUSIONS

It has been shown that S. baicalensis specimens collected in different ecological and geographical habitats in culture retain interpopulation differences in some morphological features (plant height, number of pairs of leaves per shoot, and number of shoots per individual) and the timing of the onset of phenophases. The formation of steppe Zabaykalsky and forest Primorye ecotypes can be assumed. The adaptive capabilities of these culturing populations in the new conditions are shown, and the reserve of their hereditary variability is mobilized.

FUNDING

This work was carried out as part of State Task АААА-А21-121011290027-6 under the project “Theoretical and Applied Aspects of Studying the Gene Pools of Natural Plant Populations and Conservation of Plant Diversity outside the Typical Habitat (Ex Situ).”

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any research involving humans or animals as research objects.

CONFLICT OF INTERESTS

The author declares no conflict of interest.