CC BY
0
BIOMORPHOLOGICAL TRAITS AND LEAF DRY MATTER CONTENT ARE IMPORTANT TO PLANT PERSISTENCE IN A HIGHLY UNSTABLE VOLCANIC GROUND
Anton P. Korablev1* , Elizaveta V. Sandalova1' o. Kirill A. Arapov1 , Ksenia M. Zaripova1'3
Komarov Botanical Institute of RAS, Russia
*e-mail: akorablev@binran.ru 2Lomonosov Moscow State University, Russia 3St. Petersburg Federal Research Center of the Russian Academy of Sciences, Russia
Received: 09.12.2023. Revised: 18.02.2024. Accepted: 12.03.2024.
The colonisation of newly formed territories by plants during primary succession is a crucial stage in the formation of ecosystems. Adaptations of species to withstand harsh environment allow them to survive and form pioneer communities. We analysed ten categorical and quantitative plant traits to examine their role in plant resistance to substrate instability in primary volcanic habitats. The research questions were: 1) which plant traits enable plants to persist under the most unstable ground conditions?; 2) what are the ecological strategies of species that grow under the condition of stress, such as low mineral nutrition, coupled with intense disturbance, such as unstable ground? The research was conducted on the Tolbachinsky Dol plateau in Kamchatka, Russia, on loose volcanic sediments of the 1975 eruption. At altitudes ranging from 700 m a.s.l. to 1000 m a.s.l., 40 sample plots were established along the gradients of altitude and degrees of ground instability. The species composition of vascular plants and the percentage cover of species, as well as other habitat characteristics, were assessed. Linear models were used to investigate the relationship between traits and ground instability. The principal component analysis was used to identify groups of characteristic traits. Leaf dry matter content (LDMC) had the largest explained variance. The LDMC community weighted means decreased with increasing disturbance (ground instability). A whole set of categorical traits, i.e. plant functional types, characterised the adaptation of plants to unstable ground. These characteristics include life-form (according to Serebryakov classification), density of shoots arrangement, morphology of underground organs, and, to a lesser extent, dispersal mode. The study analysed 45 species, and it was found that only four of them were adapted to perform under conditions of high substrate instability. The study showed that the mutual interaction of a suite of biomorphological traits and leaf density characteristics formed a syndrome of pioneer species adapted to unstable ground. The ecological strategies of the majority of species in the studied communities were characterised by the predominance of the stress-tolerant strategy, explained by the extremely poor mineral nutrition in the primary habitats. Under conditions of both low nutrient availability and high disturbance intensity, species with a mixed stress-tolerant-ruderal strategy are favoured. In the gradient of increasing disturbance, the role of the ruderal axis increased while stress tolerance decreased. However, the role of ecological strategy may be weakened by the presence of other important adaptive traits.
Key words: adaptation, ecological strategy, extreme habitat, functional trait, Kamchatka, leaf area, lifeform, specific leaf area, volcanic habitat
Introduction
In newly formed areas, the vegetation development is a crucial stage in the formation and functioning of ecosystems (Clements, 1916; Aleksandrova, 1964; Chapin et al., 2011). To be established in a new habitat, a plant has to overcome a series of stages, namely reaching the habitat, germinating, surviving under specific abiotic conditions, and competing with other plants (Belyea & Lancaster, 1999). The success of this event is largely determined by the evolutionarily established biological and physiological features of the plant (Keddy, 1992). Such features of a
plant, which reflect its adaptive strategies and impact on ecosystem functions, are called functional traits (Garnier et al., 2016; Vasilevich, 2016). The search for general patterns in vegetation formation and making predictions is one of the fundamental issues in ecology. To facilitate this, ecologists consider the functional traits of species alongside their taxonomy (MacArthur, 1984; Garnier et al., 2016).
During the initial stages of the vegetation development in highly disturbed habitats or newly established areas, predicting succession can be challenging due to the high variability in species
composition (Walker & del Moral, 2003). However, by considering succession at the level of species traits, it is possible to identify common traits of colonising plants and predict the species composition of emerging communities (Lavorel & Garnier, 2002). Recent studies have demonstrated a close relationship between species traits within vascular plants (Díaz et al., 2016), as well as the relationship between their traits and environmental conditions (Joswig et al., 2021). The composition of a plant community, as well as the traits of comprising their species, is determined by a combination of abiotic conditions and interactions between the plants themselves (Belyea & Lancaster, 1999; Kraft et al., 2015). In habitats with a less developed vegetation cover and severe abiotic conditions, habitat selection predominates. This enables a clearer understanding of the relationships between species and their environment. Areas of primary succession, which lack remnants of previous vegetation and soils, are excellent for investigating plant-habitat relationships (Walker & del Moral, 2003).
Research involving traits of species growing in primary habitats have been conducted on glacial deposits (Marteinsdóttir et al., 2018; Fran-zén et al., 2019; Anthelme et al., 2021), dunes (Bermúdez & Retuerto, 2013; Ciccarelli, 2015), areas formed by human activity (Prach et al., 1997; Rehounková & Prach, 2010; Mudrák et al., 2021), and volcanic activity (Tsuyuzaki & del Moral, 1995; Zobel & Antos, 2009; Voronkova et al., 2011; Korablev et al., 2020; Muñoz et al., 2021). Volcanic deposits, unlike other habitats, are characterised by some of the most extreme conditions. The substrate is inherently sterile, lacking in organic matter and nitrogen (Walker & del Moral, 2003). In addition to a scarce supply of mineral nutrients, plants develop under conditions of highly unstable ground (del Moral & Bliss, 1993), contrasting microclimatic conditions (Chapin & Bliss, 1989; Crisafulli et al., 2015), and high concentrations of toxic compounds and heavy metals (Zakharikhina & Lit-vinenko, 2019; Bilaya et al., 2022). The species composition and species richness of volcanic communities depend on the duration of succession (Aplet et al., 1998; Cutler, 2010; Korablev & Neshataeva, 2016; Vilmundardóttir et al., 2018). Relief characteristics are equally important, both at the microlevel (Titus & Tsuyuzaki, 2003; Elias & Dias, 2007; Cutler et al., 2008; Marteinsdóttir et al., 2013; Korablev et al., 2020) and at the
mesorelief level (Aplet et al., 1998). The properties of the volcanic substrate depend largely on its physico-chemical nature (Muñoz et al., 2021). If the substrate is represented by scoria or teph-ra, a loose pyroclastic material, its instability is also one of the main limiting factors (del Moral & Bliss, 1993; Voronkova et al., 2011; Korablev et al., 2018). Volcanic ecosystems are a common subject of research related to testing various succession theories (Tagawa, 1992; Walker & del Moral, 2003; del Moral, 2007; Cutler, 2010; Marleau et al., 2011) and plant adaptations to environmental conditions (Tsuyuzaki & del Moral, 1995; Voronkova et al., 2008; Barba-Escoto et al., 2019; Muñoz et al., 2021). Predicting community development following ecosystem disturbance requires an understanding of the direction of species adaptation to extreme habitat conditions (Walker & del Moral, 2003).
Previous studies have analysed the bio-morphological traits and seed germination of pioneer species in scoria fields on volcanoes in Kamchatka (Voronkova et al., 2008). Additionally, research has been conducted on plant life-forms and seed dispersal pathways along the successional gradient on the Tolbachinsky Dol (Korablev et al., 2018, 2020). The study found that plant biomorphological traits and dispersal modes accurately indicate the habitat conditions in the primary landscape. However, it is unclear which other plant traits are adaptations to stress in volcanic habitats.
The study was aimed to establish the correlation between individual plant traits and their adaptation to ground instability, the main destabilising factor on scoria fields. The research questions were: 1) which plant traits enable plants to survive under the most unstable ground conditions?; 2) what are the ecological strategies of species that grow under the condition of stress, such as low mineral nutrition, coupled with intense disturbance, such as unstable ground? The second question is interesting from the perspective of Grime's theory of plant ecological strategies, according to which the emergence of a strategy adapted simultaneously to stress and disturbance is evolution-arily inadvisable due to the general unsuitability of such habitats for life (Grime & Pierce, 2012).
Material and Methods
Study area
The studies were carried out on the Tolbachinsky Dol volcanic plateau (55.72621° N,
160.22220° E), situated in the south-west of the Klyuchevskoy volcanic group (Fig. 1). This area is a part of the Klyuchevskoy Nature Park and is designated as a UNESCO World Heritage Site under the name «Volcanoes of Kamchatka». The plateau is composed of lava flows and ash-scoria deposits. The soils in this area are poorly developed and contain bands of ash, often with interlayers of buried humus horizons (Zakharikhina & Litvinenko, 2011). The climate is temperate continental with an annual precipitation of 700 mm. At an altitude of 700 m a.s.l., the average monthly temperature is 12.2°C in July and -22.6°C in January. The plateau has three altitude belts of vegetation. The first, forest belt, up to 800 m a.s.l., is composed of Larix gmelinii var. cajanderi (Mayr) Silba and Betula ermanii Cham. The second, krumholtz belt, between 800-1000 m a.s.l., is made up of Pinus pumila (Pall.) Regel and Al-nus alnobetula subsp. fruticosa (Rupr.) Raus. The third belt is mountain tundra, consisting of dwarf-shrub and lichen tundra. Pioneer communities in various stages of regenerative succession occupy large areas.
A large eruption occurred on the Tolbachinsky Dol plateau in 1975-1976, which has resulted in the formation of two lava fields and an extensive ash scoria plain (Fedosov, 1984). The eruption destroyed the vegetation over an area of approximately 170 km2 and caused considerable damage over an area of more than 400 km2 in the following years (Korablev & Neshataeva, 2016). In 2012-2013, a new eruption took place on the plateau, characterised mainly by lava spattering. This eruption did not have a significant impact on the vegetation of the scoria fields. The scoria fields are a hilly area in the axial part of the plateau, at altitudes of 700-1800 m a.s.l., covered with loose pyroclastic deposits, called scoria (or tephra). These deposits are very unstable due to the transport of light scoria particles down the relief by water and wind. The ground is characterised by a low content of mineral nutrients, where the gross nitrogen content is 0.026 ± 0.002%; organic matter content determined by the loss on ignition method is 1.53 ± 0.50%; pH is close to neutral (Bi-laya et al., 2022). The vegetation cover is extremely sparse, usually represented by single individuals and patches of plants, and is generally tenths to hundredths of a percent.
Fig. 1. Location of the study area (marked with an asterisk) on the Kamchatka Peninsula (A), and sample plots on the scoria field of the Tolbachinsky Dol plateau (B). Levels of disturbance are indicated by colour: 1 - habitats with minimal ground instability; 2 - with moderate ground instability; 2 - with high ground instability.
Field study
In 2023, 40 permanent 10 x 10-m sample plots were established along altitude and substrate instability gradients in the 1975 scoria field (Fig. 1B). The full species composition of vascular plants, dominant mosses and lichens was determined in each sample plot, and the percentage coverage of each species was estimated. A number of habitat characteristics were recorded, including the area of unstable loose substrate (hereafter referred to as ground instability), the thickness of the scoria layer from the 1975-1976 eruption, and the microrelief. Based on values of ground instability and vegetation cover, habitats were classified into three categories reflecting the intensity of disturbance (Fig. 2), namely 1 - habitats with minimal ground instability; 2 - with moderate ground instability; 3 - with the highest ground instability. Their general characteristics are summarised in Table 1. Habitats of category 1 are characterised by a relatively uniform vegetation cover with the predominance of shrub willows (Salix bebbiana Sarg., S. sphenophylla A.K.Skvortsov, S. uden-sis Trautv. & C.A.Mey.), Populus suaveolens Fisch. ex Poit. & A.Vilm., and Leymus ajanensis (J.J.Vassil.) Tzvelev. In habitats with a medium degree of disturbance (category 2), extensive patches of Leymus ajanensis (up to 2 m2 in area) are often formed, shaping mounds of 50 cm or more due to local stabilisation of the substrate. The ground remains unstable between the mounds. In addition to Leymus ajanensis, the herbs Smelowskia par-ryoides (Cham.) Polunin, Papaver microcarpum DC., Stellaria eschscholtziana Fenzl, Saxífraga bronchialis subsp. funstonii (Small) Hultén and the semi-dwarf-shrub Artemisia glomerata Ledeb. are constant in these habitats. Habitats of category 3 are characterised by high ground instability throughout the area, often with aeolian and water ripples on the surface formed by processes of redeposition of loose material. The set of constant species is similar to habitats of category 2, but the percentage plant coverage is much lower, and
Smelowskia parryoides is the dominant and most typical species.
Plant traits
We analysed plant traits that may serve as important indicators of their adaptation to the colonisation of disturbed areas and existence in unstable ground (Electronic Supplement 1). The following traits were considered: 1) dispersal mode; 2) dry mass of 1000 seeds (seed mass, SM); 3) life-form (according to Serebryakov, 1962); 4) vegetative height of the plant, i.e. the shortest distance between the upper boundary of the main photosynthetic tissues of plants and the substrate level; 5) density of shoots arrangement of an individual; 6) morphology of underground organs; 7) leaf area (LA); 8) specific leaf area (SLA), considered as the ratio of leaf area to its dry mass; 9) leaf dry matter content (LDMC), considered as the ratio of dry mass of a leaf to its water-saturated mass expressed in percent; 10) Grime's ecological strategy.
Fig. 2. Three habitat categories of disturbance intensity (ground instability) on the Tolbachinsky Dol plateau (Kamchatka, Russia). Designations: A - habitats with minimal ground instability; B - with moderate ground instability; C - with high ground instability.
Table 1. Characteristics of habitat categories identified by disturbance intensity (ground instability) on the Tolbachinsky Dol volcanic plateau (Kamchatka, Russia)
Category of disturbance Ground instability in the sample plot, % Number of vascular plant species per sample plot Percentage coverage of vascular plants, % Percentage coverage of mosses, %
m ± SE min-max m ± SE min-max m ± SE min-max m ± SE min-max
1 24.0 ± 3.1 10.0-40.0 23.0 ± 1.3 13-29 4.0 ± 0.4 2.0-7.0 5.0 ± 0.9 1.0-10.0
2 76.0 ± 4.9 40.0-97.0 10.0 ± 1.5 3-20 2.0 ± 0.2 1.0-3.0 3.0 ± 0.6 0.1-9.0
3 99.0 ± 0.2 97.0-99.5 4.0 ± 0.4 1-6 1.0 ± 0 0.1-1.0 1.0 ± 0.1 0.1-2.0
Note: m - arithmetic mean; SE - standard error of the mean; min-max - range of values.
We measured the traits of the analysed species in 2017-2023. Some of the data were derived from literature sources. Dispersal modes were classified according to Pérez-Harguindeguy et al. (2013), with additional categories based on Será & Sery (2004). The analysed modes included anemochores with seeds equipped with tufts, parachutes, and hairs (AP); anemochores with «wings» or membranes on seeds (AW); anemochores without special appendages, with light seeds (1.00-0.05 mg) that are rolled over the surface by wind (AU); ballistochores (B); endozoochores (EndZ); exozoochores (ExoZ); and myrmecochores (M). Species with other dispersal modes were not met on the sample plots. Seed dry mass was measured according to the method described by Pérez-Harguindeguy et al. (2013). Data for each species were averaged based on 3-10 (on average 5) biological replicates, depending on the prevalence of the species. If seed mass data were insufficient for a species, values were taken from the TRY plant trait database (Kattge et al., 2020). There were three such species, namely Sabulina verna, Salix caprea, and Salix udensis. The lifeform, density of shoots arrangement, and morphology of underground organs were determined based on literature sources (Bezdelev & Bezdeleva, 2006; Yurtsev et al., 2010), as well as our field observations and data from Voronkova et al. (2008). The study did not analyse individual types of root systems, but instead focused on the overall system of underground plant organs, which provides a more accurate representation of species functions (Fre-schet et al., 2021). Plant height, leaf area, specific leaf area, and leaf dry matter content were measured under both field and laboratory conditions using the methodology outlined by Pérez-Harguindeguy et al. (2013). The ecological strategies of plant species were calculated based on three leaf traits, namely water-saturated leaf mass, leaf dry mass, and leaf area, using the StrateFy programme (Pierce et al., 2017). The programme calculates the co-ordinates of each species in three axes using regression equations derived by Pierce et al. (2017) from trait analysis of a large array of species using the principal component method. C is responsible for competitive strategy (violents according to Ramensky, 1938); S is responsible for stress-tolerant strategy (patients); R is responsible for ruderal strategy (explerents).
Data analysis
Community means weighted by species abundance were calculated for each sample plot for quantitative traits. This was done on the full species
composition of vascular plants in the FD package, function dbFD() (Laliberte & Legendre, 2010) in the R software environment (R Core Team, 2020). A matrix of sample plots by traits was obtained. Percentage coverage data were not logarithmised due to the low species abundance (0.1% to 2.0%). Species proportions of plant functional types were calculated for each categorical trait (dispersal mode, lifeform, density of shoots arrangement, morphology of underground organs), weighted by their abundance. Pearson correlation coefficient was used to examine linear dependencies. To assess the correlation significance, the permutation procedure implemented in the perm.cor.test() function in the jmuOutlier package was used based on 9999 permutations (Garren, 2019), as the distribution of most variables was not normal. A linear regression model, function lm() in the Stats package, was used to assess the degree of association of each trait with ground instability. The distribution of data for most traits differed from the normal. Hence, the residuals of the models were analysed for normality and the absence of pronounced trends. The residuals of most models were normal or close to normal distribution, except for the group of short-rhizomatous and long-rhizomatous species. A slight trend was found in model residuals for the shrubs, but we did not detect correlations of residuals with other habitat characteristics. In order to better interpret the results, we deliberately avoided transforming the data to strengthen linear relationships, as the transformation did not produce a significant increase in R2 and did not change the distribution of residuals. In order to construct ternary plots, we calculated the occurrence of species in habitats of each disturbance category as the ratio of the number of sample plots where the species was present to the total number of sample plots in this category. We only considered species with an occurrence of more than 20% in each category.
We compared the linear models built for each of the traits based on R2, which represents the proportion of variance in the data explained by the model. We converted the explained variance into percentages by multiplying R2 by 100. To make the comparison of categorical traits with quantitative traits more formal, we calculated the average value of the explained variance for each categorical trait.
Indirect ordination by principal component analysis (PCA), function prcomp() in the Stats package, was used to assess the relationship between weighted means of traits and functional types, as well as their relationship with ground instability. The matrix sample plots by traits was used for the ordination. Com-
munity weighted means of trait values and the proportions of species belonging to different functional types were standardised. The first three axes were found to be significant, explaining 72.7% of the data variance. The correlations between the PCA axes and the weighted means of species and functional types, as well as ground instability, were calculated using the cor() function in the Stats package.
We initially tested the hypothesis that the distribution of the studied traits is related to all measured factors, including distance to refugia and tephra thickness of the last eruption. These factors were of great importance in studies of Korablev et al. (2018, 2020). However, the relationship was found to be insignificant. Therefore, we further analysed the relationship of the traits solely with ground instability.
Results
Dispersal mode and seed mass
A total of 45 vascular plant species were identified in 40 sample plots, contributing to a local flora of 310 species on the Tolbachinsky Dol (Nesha-taeva, 2014). Out of the 45 species, 37 ones were anemochores, with 18 belonging to the AU category, 15 to the AP category, and four to the AW category. Only eight species had other agents of dispersal, namely three endozoochores, two myrmecochores, two ballistochores, and one epizoochore. The most common species were herbaceous plants, including Smelowskia parryoides, a pioneer in scoria fields (100% occurrence), Leymus ajanensis (85%), Pa-paver microcarpum, and Stellaria eschscholtziana (both 70%). All of these species belong to the AU category, which means that they have wind-dispersed seeds without special appendages. The proportion of various dispersal modes to the number of species in each sample plot was analysed. Bal-listochores and myrmecochores, found in only four sample plots, and an exozoochore, represented by one species, were excluded from the analysis. A significant positive relationship (r = 0.61, p < 0.001) was found between ground instability and AU (Fig. 3). Negative relationships were observed between ground instability and EndZ, AP and AW categories, namely r = -0.56 (p < 0.001), r = -0.51 (p < 0.01), and r = -0.40 (p < 0.05), respectively. Dissemination in the study area is mainly characteristic of woody plants. EndZ were only found in the first disturbance category. The community weighted means of seed mass had a non-mono-tonic dependence on ground instability (r = 0.41, p < 0.01). The second disturbance category was typically dominated by Leymus ajanensis, which
has relatively large seeds (3400 mg/1000 seeds). In the third disturbance category, pioneer communities were co-dominated by species with lighter seeds, ranging at 97-912 mg/1000 seeds.
Life-form and plant height
A total of five species of trees, six shrubs, five dwarf-shrubs, one semi-dwarf-shrub, and 28 poly-carpic herbs were identified. Annual herbs were not present. The semi-dwarf-shrub, represented by one species (Artemisia glomerata), was excluded from further analyses. The relationship between species proportion and ground instability was positive only for perennial herbaceous plants (r = 0.58, p < 0.001), which were the only life-form found in habitats of the third disturbance category (Fig. 3). Shrubs, trees, and dwarf-shrubs showed a high negative correlation with ground instability, namely r = -0.81 (p < 0.001), r = -0.72 (p < 0.001), and r = -0.70 (p < 0.001), respectively. In habitats of the second disturbance category, we often recorded trees, although they represent a small proportion of the total number of species. Specifically, we observed 1-2-year-old specimens of Populus suaveolens in these communities. Dwarf-shrubs were only observed in habitats of the first disturbance category. It was expected that the weighted mean plant height would decrease with an increasing degree of disturbance. However, both the weighted mean plant height and seed mass have a non-monotonic dependence and are insignificant (Fig. 3). In communities dominated by Leymus aja-nensis, the weighted average plant height increased. In the third disturbance category, however, there was a high degree of variation, depending on the species composition of pioneer communities.
Density of shoots arrangement
We recorded a total of 45 plant species, including 25 with sparse or single shoots, 12 with a dense arrangement of shoots forming loose or dense turf (caespitose herbs), and eight cushion-shaped species, characterised by very dense and compact arrangement of low shoots, forming a cushion-like structure (herbs and one semi-dwarf-shrub). The present study has found a strong positive correlation (r = 0.71, p < 0.001) between ground instability and the proportion of cushion-shaped species, while a negative correlation was observed between ground instability and the proportion of species with sparse shoot arrangement (r = -0.81, p < 0.001) (Fig. 3). Caespitose herbs are present in communities regardless of ground instability and constitute an average of 20-30% of the total number of species.
АР
R2 = 0.24*
AW
R2 = 0.14*
R2 = 0.36***
EndZ R2 = 0.30***
£ 0.5
§_0.4 со
Ъ 0.3
8.0.1
0.0
сЧ > •
• ' •• •
• •
•
0.30.2-
o £= О
% 0.1 ■
Q- 0.0-
*
• *
••
25 50
Seed mass
75 100
R2 = 0.15**
1000 500
•
• • , •
• > • ••J
■
25
Trees
50 75 100
R2 = 0.51***
сn
■§ 0.15
CD
|о.ю
a о
■-E 0.05 о
0.00
•
• •• •
• • <1 ••
25 50
75
Cusion-shaped R2 = 0.49**
75 100
R2 = 0.75***
Short-rhizomatous
R2 = 0.39***
25 50 75 100
Long-rhizomatous
• 4« • • •
i \
• • •i
Long-rhizome-tap rooted
25 50 75 100
Ground instability, %
25 50 75 100
Ground instability, %
25 50 75 100
Ground instability, %
25 50 75 100
Ground instability, %
Fig. 3. Correlations of weighted means of plant traits and proportions of species of each functional type with the intensity of ground instability on the Tolbachinsky Dol volcanic plateau (Kamchatka, Russia). The red line is a linear regression. The shaded area is 95% confidence interval. Species traits and the names of functional types are located above the diagrams. Designations: AB - anemochores with seeds attached with pappus or other long hairs; AK - anemochores with seeds equipped with large «wings»; AP - anemochores without apparent modifications for wind transport; EndZ - endozoochores; LA - leaf area; SLA - specific leaf area; LDMC - leaf dry matter content; C - competitor strategy; S - stress-tolerant strategy; R - ruderal strategy. R-squared of the model and its significance are indicated as follows: *** - < 0.001, ** - < 0.01, * - < 0.05, ns - non-significant.
Morphology of underground organs
The 45 species were classified into five categories based on the structure of their underground organs, namely fibrous-rooted (13 species), short-rhi-zomatous (seven species), long-rhizomatous (six species), long-rhizomatous tap-rooted (four species), and tap-rooted (15 species). The study found a positive relationship with ground instability only for the proportion of tap-rooted plants (r = 0.65, p < 0.001) (Fig. 3). As ground instability increased, the proportion of species with fibrous root system and short-rhizomatous species decreased: r = -0.87 (p < 0.001) and r = -0.64 (p < 0.001), respectively. Long-rhizomatous and long-rhizomatous tap-rooted herbs form communities in habitats of all disturbance categories, but were not found in habitats of the most disturbed category.
Leaf traits
The study found that the community-weighted mean leaf area and specific leaf area were not correlated with ground instability (Fig. 3). However, there was a strong negative correlation between leaf dry matter content and ground instability (r = -0.74, p < 0.001). In highly disturbed habitats, pioneer communities were composed of species with leaves that retained more water.
Ecological strategy
The competitive ecological strategy was generally underrepresented in pioneer community species, and its values were not related to ground instability (Fig. 3). The study revealed a positive correlation (r = 0.52, p < 0.001) between ground instability and values of the ruderal strategy. In the most severely disturbed category, the constituent species of the community exhibited a much more distinct ruderal strategy. Conversely, the stresstolerant strategy of species slightly decreased with increasing ground instability (r = -0.44, p < 0.01).
We assessed the strategies of the most consistent species in habitats of three disturbance categories, or ground instability (Fig. 4). Overall, the strategies of most species tended towards stress tolerance. In habitats within the lowest disturbance category, 31 constant species were recorded. These species were evenly distributed in the lower right part of Fig. 4A. Habitats within the medium disturbance category harbour 17 constant species (see Fig. 4B). The number of constant species showed a noticeable decrease, particularly those with a large proportion of stress-tolerance. These species included
Salix berberifolia Pall. and Dryas octopetala L., which are S-strategists, as well as Salix spheno-phylla (S/CS-strategist), and Poa lanata Scribn. & Merr. and Vaccinium uliginosum L. (both S/ SR-strategists), which were frequently found in habitats within the third disturbance category. In habitats classified as highly disturbed, species with a high value of stress-tolerance were absent. Out of the 13 species initially recorded in this group, only five remained constant (Fig. 4C). Of them, four species exhibited a mixed stress-tolerant-ruderal strategy, namely Smelowskia parryoides, Papaver microcarpum, Stellaria eschscholtziana, and Artemisia glomerata. The remaining species, Leymus ajanensis, was characterised by a competitor-stress-tolerant strategy, being a long-rhizomatous herb.
Adaptations of species to unstable ground
The principal component analysis was used to investigate the distribution of traits. It revealed three significant axes of variation. The first axis, explaining 37.7% of the data variation, had a high negative relationship with ground instability (r = -0.86, p < 0.001) (Electronic Supplement 2). The correlation between traits and the first axis indicated plant adaptations to the substrate instability (Electronic Supplement 2). The first axis identified a group of plant traits that are characteristic of species adapted to growing in unstable ground (Fig. 5). These herbs have a cushion-shaped taproot and a distinct ruderal strategy. They have a low leaf dry matter content and seeds without appendages for wind dispersal. The least tolerant to ground mobility are plants with lignified single or sparse shoots, a fibrous root system, high leaf dry matter content, a more distinct stress-tolerant strategy, and seeds with hairy appendages. The second axis accounted for 23.5% of the data variation, but it did not correlate with any of the measured habitat characteristics. Along this axis, we can identify another group of plant traits that are relatively indifferent to the substrate instability (Fig. 5). These are tall, long-rhizomatous caespitose herbs with a distinct competitive strategy, large leaves, low values of specific leaf area, and relatively heavy seeds. The third axis explained 11.5% of the data variation and also did not correlate with the measured habitat characteristics. Traits, such as caespitose type of shoot arrangement and long-rhizomatous taprooted type of morphology of underground organs, show moderate association with this axis (Electronic Supplement 2).
A)
100
В)
100
^R-strategy
С)
100
R-strategy
^R-strategy
Fig. 4. Ternary plots of ecological strategies for constant species (occurrence > 20%) in habitats of three disturbance categories on the Tolbachinsky Dol plateau (Kamchatka, Russia). Designations: A - habitats with minimal ground instability; B -with moderate ground instability; C - with high ground instability. Coloured circles - species, diamond - arithmetic mean for all species in the disturbance category.
3-
lo
со 0-
cnj
о
CL
-3-
• 1
2
• 3
PC 1 (37.7%)
Fig. 5. PCA diagram of community weighted means of plant traits and proportions of species of various functional types in sample plots on the Tolbachinsky Dol volcanic plateau (Kamchatka, Russia). Coloured circles are sample plots in the three categories of disturbance intensity: 1 - habitats with minimal ground instability, 2 - with moderate ground instability, 3 - with high ground instability. Vectors of plant traits and functional types are shown as follows: 1 - anemochores with seeds attached with pappus or other long hairs (AP); 2 - anemochores with seeds equipped with large 'wings' (AW); 3 - anemochores without apparent modifications for wind transport (AU); 4 - endozoochores (EndZ); 5 - seed weight; 6 - herbs; 7 - dwarf-shrubs; 8 - shrubs; 9 - trees; 10 - plant height; 11 - sparse shoots; 12 - caespitose; 13 - cusion-shaped; 14 - fibrous root system; 15 -short rhizomatous; 16 - long-rhizomatous; 17 - long-rhizomatous taprooted; 18 - taprooted; 19 - leaf area (LA); 20 - specific leaf area (SLA); 21 - leaf dry matter content (LDMC); 22 - C-strategy; 23 - S-strategy; 24 - R-strategy.
The traits of species forming pioneer communities with sufficient constancy (more than 50% occurrence) in habitats of the third disturbance category were analysed. This category refers to habitats where 97.0-99.5% of the substrate area is unstable. The spe-
cies identified were Smelowskia parryoides (100% occurrence), Papaver microcarpum (57%), Stellaria eschscholtziana (50%), and Leymus ajanensis (57%). All of these species are polycarpic herbs, seeds of which are dispersed by wind and lack any specialised
appendages. Smelowskia parryoides, Papaver mi-crocarpum, and Stellaria eschscholtziana exhibit the set of traits, which are highlighted on the first PCA axis (Fig. 5). The plants are small, only 4-5 cm, and have relatively small leaves (35-94 mm2) with low values of specific leaf area (16-17 mm2/mg). They have a moderate leaf dry matter content (20-26%) compared to other plants in Kamchatka. Additionally, they are characterised by a tap root system. These plants belong to the stress-tolerant-ruderal ecological strategy. Leymus ajanensis exhibits the group of traits that are identified on the second PCA axis (Fig. 5). Leymus ajanensis is a tall herbaceous plant, up to 65 cm in height, with large leaves measuring 2961 mm2. It has a higher leaf dry matter content (30%) but lower values of specific leaf area (13.6 mm2/mg). The plant's root system is fibrous, with a long, thin rhizome providing additional nutrients and aiding in vegetative spread. This species is the only successful pioneer species in the study area that belongs to the competitive-ruderal ecological strategy.
To evaluate the relationship between plant traits and ground instability, we estimated the proportion of variation in data explained by each linear model (Fig. 3). The number of models for each categorical trait corresponds to the number of functional types considered in this study. We excluded some functional types, such as the four dispersal modes and one life-form (semi-dwarf-shrub), due to the lack of their representativeness in the study area. If we arrange the traits in descending order of their relationship with ground instability, we obtain the following range: leaf dry matter content (53.2%) > life-form (49.2%) > density of shoots arrangement (37.6%) > morphology of underground organs (30.3%) > dispersal mode (25.8%) > ecological strategy (15.8%) > seed mass (15.1%). Thus, in addition to the leaf dry matter content, bio-morphological features of the plant are important traits for tolerance to unstable ground.
Discussion
Leaf traits
Disturbed and early successional communities are characterised by the predominance of species with a low leaf dry matter content and high values of specific leaf area (Pakeman et al., 2011; Cicca-relli, 2015). The low variation in the community weighted mean of specific leaf area across the studied communities and the absence of any discernible trend suggested that habitat selection was operating at the level of this trait. It means that these primary communities were composed of species, which have a similar strategy for resource acquisi-
tion. The studied species exhibited low values of specific leaf area, which is consistent with an economical resource acquisition strategy and characteristic of poor soils and cool climates (Wright et al., 2004; Joswig et al., 2021). This also reflects a higher contribution to plant defense structures (Lambers & Poorter, 2004). Meanwhile, we observed a consistent decrease in the community weighted mean of leaf dry matter content towards the highest degree of disturbance. According to Hodgson et al. (2011), leaf dry matter content is an indicator of soil fertility, with poorer conditions resulting in higher leaf dry matter content. However, our data indicate that under the most disturbed conditions, the soil profile had a lower organic matter content based on ignition losses, a coarser particle size distribution, and a correspondingly lower water-retaining capacity. The high leaf dry matter content is often associated with a longer leaf lifespan and resistance to physical damage (Hodgson et al., 2011). Our results do not align with the findings of Hodgson et al. (2011), but a similar trend has been described for dune communities in the Mediterranean region (Ciccarelli, 2015). Therefore, further research is required to determine the contribution of this trait to resistance to the unstable ground. This investigation should involve the use of more informative leaf traits, as suggested by Ivanova et al. (2018).
Ivanova et al. (2018) observed that a decrease in leaf dry matter content results in an increase in leaf thickness, for the same values of specific leaf area. They also found that leaf thickness increases with increasing climate aridity. However, Ivanova et al. (2018) discovered significant changes in the structure of leaf mesophyll. For instance, Song et al. (2008) demonstrated that plants with a low leaf dry matter content are better adapted to drought conditions and use water more efficiently in alpine communities. Low leaf dry matter content values suggest that plants can store more water (Lam-bers & Poorter, 2004; Wright et al., 2005). This is particularly important in primary substrates with low water-retaining capacity. Therefore, the lower weighted mean of leaf dry matter content in the studied communities may be partly explained by the low water-retaining capacity of the substrate in the most disturbed sites. However, it appears that under our conditions, any gradient is very weak. The trend in the leaf dry matter content can also be attributed to the absence of shrub and dwarf-shrub species in the most disturbed sites. These species generally have a higher dry matter content than pioneer herbs in our region.
Life-form
The distribution of plant life-forms can serve as an indicator of the successional gradient and intensity of disturbance (Prach et al., 1997; Walker & del Moral, 2003; Korablev et al., 2018). In the present study, it was found that the distribution of life-forms accounted for between 32% and 65% of the variation in the intensity of ground instability. The majority of the explained variance was attributed to the woody life-forms, which were completely absent in the unstable ground conditions. It was shown previously that only herbaceous plants grow in the most isolated sites, which are the furthest from seed sources, and at the initial stage of succession (Korablev et al., 2018, 2020). Voronkova et al. (2008) also identified herbs as pioneer species in volcanic habitats of Kamchatka. Our present study demonstrates that herbaceous plants are highly tolerant to the unstable volcanic ground. This is consistent with previous studies in other temperate volcanic regions (del Moral & Bliss, 1993; Tsuyuzaki & del Moral, 1995; Tsuyuzaki, 2009), but not in the tropics (Velazquez et al., 2000; Walker et al., 2006; Sutomo et al., 2011). A predominance of herbaceous plants in the initial stages of succession is also noted. Herbaceous plants are typical in habitats with unstable ground, such as sandy coastal dunes (Ciccarelli, 2015). Consequently, herbs are considered the most successful life-form in conditions of unstable ground and poor mineral nutrition, at least at temperate latitudes.
Density of shoots arrangement
Voronkova et al. (2008) studied the biomorpho-logical traits of pioneer species in volcanoes in Kamchatka, and found that they are characterised by a dense arrangement of aboveground shoots. In our study, we observed a decrease in the species diversity with a single arrangement of shoots in the gradient of ground instability. Instead, we found an increase in the proportion of species with a dense arrangement of shoots, which form a «cushion». Such an adaptation to the contrasting microclimatic conditions and unstable substrate offers several advantages. Inside the «cushion», transpiration decreases, temperature variation reduces, moisture accumulates, and favourable local conditions of soil formation are formed. Additionally, wind-borne detritus and fine soils accumulate, and «cushions» provide better protection to assimilating organs and plant buds from wind-borne scoria and snow particles (Gorchakovskii & Stepanova, 1995; Voronkova et al., 2008). The proportion of caespitose species in our study remained relatively constant, which also reflects their tolerance to the unstable ground. The close arrangement of shoots enables local stabilisation of the
substrate and protects shoots and seedlings within the turf from wind-borne solid particles.
Morphology of underground organs
Several studies have highlighted the significant impact of morphology of underground plant organs, particularly the root system, in adapting to adverse conditions of soil nutrition and erosion (Gyssels et al., 2005; Bardgett et al., 2014; Freschet et al., 2021). Our study confirmed that plants with fibrous root system, including short-rhizomatous plants, were the least tolerant to the unstable ground and were absent in the most disturbed category. Additionally, our results showed that the proportion of tap-rooted plant species increased under the most unstable ground conditions. Del Moral & Bliss (1993) also reported the predominance of tap-rooted species of the genus Lupinus on volcanic sediments of Mount St. Helens volcano. The taproot system effectively anchors the plant in the unstable ground (del Moral & Bliss, 1993; Voronkova et al., 2008). It has been demonstrated that plants with a long rhizome are resistant to the ground instability. This is supported by studies on volcanoes in Kamchatka (Voronkova et al., 2008; Korablev et al., 2018). The study comparing pioneer species at Mt. Usu volcano (Japan) and Mt. St. Helens volcano (USA) also found a common trait of having a long rhizome (Tsuyuzaki & del Moral, 1995). Rhizomatous plants are adaptable to unstable substrate conditions due to their preference for clonal reproduction and the formation of isolated ramets. This enables the species to persist under active erosion (Klimesova, 2021). However, the frequent disturbance can significantly reduce rhizome size and longevity (Bartuskova et al., 2022). In addition to adaptations for unstable ground, underground organs provide another significant advantage for life in barren volcanic substrates. Plants have been known to employ a strategy of allocating more biomass to underground storage organs in response to stress and disturbance (Qi et al., 2019). For instance, Harris et al. (2023) analysed biomass data from 47 species of rhizomatous plants. They found that, on average, a rhizome accounts for 30.2% (up to 74.4%) of the total biomass. A rhizome and taproot can store nutrients, primarily carbohydrates, in large quantities. The plants can quickly produce aboveground biomass after physical damage and during the winter dormancy period. This occurs precisely when tephra particles are actively moved on the surface during snowmelt (Freschet et al., 2021).
Dispersal mode and seed mass
In the study area, the dominant dispersal mode is anemochores. This is typical for primary areas in
general (Walker & del Moral, 2003). Anemochores lacking special appendages on seeds for wind transport were prevalent in our study in habitats with the most unstable ground. This dispersal mode was abundant in the most isolated and harsh habitats at Mt. St. Helens volcano (USA) (Fuller & del Moral, 2003) and in the study area (Korablev et al., 2020). Korablev et al. (2020) demonstrated that physical barriers and biological amelioration of habitats were the main factors explaining the distribution of dispersal modes in the study area. Ground instability was found to be insignificant. Species with seeds that have pappus, long hairs, or «wings» were more common in habitats with woody debris, heterogeneous microrelief, and dense vegetation. The distribution of dispersal modes was not expected to be related to the ground instability in our current study. However, anemochorous species exhibited distinct trends in the disturbance gradient. Species with appendage-free seeds were prevalent in all habitats, and their proportion increased in the most severe habitats. Additionally, there was no woody debris, and the microrelief remained even. The relationship between seed shape and structure and ground instability cannot explain this phenomenon. Instead, it can be attributed to the intercorrelation of traits. The number of species of other anemochores increased in the sites with the most stable ground. Most of these species have woody life-forms, such as trees and dwarf-shrubs, which are the least adapted to the unstable ground. Furthermore, the increased presence of vascular plants in the least disturbed sites promotes the improved seed trapping and subsequent germination in stable substrate conditions. The restriction of endozoochorous species to the sites with the most stable ground can be attributed to the preference of their dispersal agents, primarily birds, for areas with denser vegetation that provides shelter from predators and a source of food. In our study, we found a moderate positive correlation (r = 0.41, p < 0.01) between seed mass and the intensity of disturbance, contrary to the usual negative correlation (Sonnier et al., 2010). The lowest community weighted means of this trait were found in more stable habitats. Its values increased in communities dominated by Leymus ajanensis, but in the most disturbed habitats, there was a high variation and no clear patterns.
Ecological strategy
The initial succession stages are typically characterised by the dominance of species with a ruderal ecological strategy (Prach et al., 1997; Caccianiga et al., 2006; Rehounkova & Prach, 2010). In our study, the primary succession in scoria fields with poor min-
eral nutrition involved species with a distinct stresstolerant component, whereas the value of the ruderal strategy did not exceed 40% for most species (Fig. 4A). This was expected, as the ruderal strategy, along with the competitor strategy, requires sufficient concentrations of available nitrogen in the soil for rapid growth. This nutrient is extremely scarce in volcanic substrates (Bilaya et al., 2022). However, the relationship between strategies and disturbance intensity (and frequency) is more intriguing. Our data indicate that an increase in disturbance leads to an increase in the community weighted means of ruderal strategy (Fig. 3). Plants with more distinct stress-tolerant strategy disappear from the most disturbed sites, as do the majority of species with a more distinct competitive strategy (Fig. 4B). In contrast to ruderal strategy species, stress-tolerant plants exhibit slower growth rates and contribute more to the plant defense structures. This includes stiff leaves, longer leaf lifespan, and the accumulation of secondary metabolites (Lambers & Poorter, 2004), which enhance resistance to physical damage and stress. Furthermore, species that are tolerant to stress incur the highest construction cost per unit of plant mass compared to species with other strategies (Pyankov et al., 2001). In conditions where wind- and water-borne abrasive materials, such as tephra, are present, slow growth and high construction cost can be a disadvantage as the plant may not have sufficient time to regenerate biomass efficiently. According to Grime & Pierce (2012), there is no evidence that competitors are adapted to stress or disturbance. Although there were no typical competitors among the observed species, some exhibited competitive strategy values as high as 50% (e.g. in Populus suaveolens). In the highest disturbance category, four out of the five species had C-axis values of 9% or less (Fig. 4C). Leymus ajanensis was an exception to the rule. It is a relatively tall, long-rhizomatous herb with stiff leaves and dense shoots. It possesses several morphological adaptations enabling it to thrive under unstable ground conditions. This exception suggests that the significance of ecological strategy may be reduced by the presence of other adaptive traits. In our study, ecological strategies accounted for a small proportion of the explained variance in the data when compared to biomorphological traits.
Adaptations of species to unstable ground
Based on the analysed data, two groups of plants can be distinguished that are resistant to the growth in unstable volcanic ground, namely those that increase their abundance in habitats with the most unstable substrate, and those that are relatively indifferent to ground
instability. The first group of species is characterised by a set of traits typical for pioneer plants in Kamchatka scoria fields (Voronkova et al., 2008; Korablev et al., 2018). The main traits are a dense arrangement of aboveground shoots, often forming a cushion-like structure, and a taproot. The adaptive significance of these traits has been discussed previously. These traits are typical for plants found in high latitudes and high mountains (Billings, 1974; Matveeva, 2015). Under these conditions, the cushion-shaped growth form serves as a defense against physical damage caused by wind-borne snow. The second group of species, which are not affected by the substrate instability, is characterised by a larger leaf area and plant height, the presence of a rhizome and a more distinct competitive strategy. Ciccarelli (2015) identified similar traits in species growing on unstable and embryonic dunes in the Mediterranean region. However, in the study of Ciccarelli (2015), these species had high values of specific leaf area, which does not coincide with our results. In general, the presence of rhizomes and taproots are common adaptations of plants of unstable sands (Danin, 1991; Mahdavi & Bergmeier, 2016). A similar combination of categorical traits characteristic of plants of various climatic zones indicates that adaptations of species to the same disturbance factors are manifested regardless of their taxonomy. These disturbance factors are physical damage to aboveground shoots by solid particles and ground erosion.
Conclusions
We have studied a range of categorical and quantitative traits of plants in relation to their adaptation to substrate instability in primary volcanic habitats. The characteristics of plants that enable them to survive the erosion and abrasive effects of volcanic materials dispersed by wind and water have been identified. The leaf dry matter content was one of the key traits, with weighted mean values decreasing as the disturbance intensity (ground instability) increased. The adaptation of plants to the unstable ground is characterised by a range of categorical traits, or functional types, including life-form, density of shoots arrangement, morphology of underground organs, and, to a lesser extent, dispersal mode. Categorical traits based on fairly rough classifications showed in our study a clearer response to the factor under study than quantitative traits. Of the 45 species analysed in this study, only four species can be considered being successful pioneers, adapted to grow under conditions of high substrate instability. These are Smelowskia parryoides, Papaver microcarpum, Stellaria eschscholtziana,
and Leymus ajanensis. According to their life-form, these plants are polycarpic herbs. They are anemo-chores, meaning they rely on the wind for transport and do not have any special appendages on their seeds. They are characterised by a taproot system and a cushion-shaped growth form, or the presence of a long rhizome. Our study has revealed that the combination of specific biomorphological characteristics and leaf traits determines the adaptability of pioneer species to an unstable substrate.
The ecological strategies of most species in the primary communities in our study were characterised by the predominance of a stress-tolerant strategy. Under conditions of low nutrient supply and high disturbance intensity, species with a mixed stress-toler-ant-ruderal strategy benefit the most. As disturbance increases, the importance of the ruderal strategy increases while stress tolerance decreases.
Acknowledgements
The study was supported by the Russian Science Foundation grant №23-24-00650 (https://rscf.ru/en/proj-ect/23-24-00650/). We thank Valentin Yakubov (Federal Scientific Center of the East Asia Terrestrial Biodiversity FEB RAS, Russia) for identifying some species of vascular plants. The research team expresses great gratitude for the assistance in organising field work to the staff of the Kamchatka branch of the Pacific Institute of Geography FEB RAS (especially Marina Vyatkina) and the administration of the Kamchatka Volcanoes Natural Park. Some of the measurements of functional traits were carried out on the equipment of the resource center «Observatory of Environmental Safety» (St. Petersburg State University, Russia) and the Joint-Use Center «Cellular and Molecular Technologies for the Study of Plants and Fungi» (Komarov Botanical Institute of RAS, Russia). We are grateful to Vadim Smirnov (Center for Forest Ecology and Productivity of the RAS, Russia) for consultations on data analysis.
Supporting Information
Additional data to the paper of Korablev et al. (2024) can be found in the Supporting Information.
References
Aleksandrova V.D. 1964 Study of vegetation cover changes. In: Field Geobotany. Vol. 3. Leningrad: Nauka. P. 300447. [In Russian] Anthelme F., Cauvy-Fraunie S., Francou B., Caceres B., Dangles O. 2021. Living at the Edge: Increasing Stress for Plants 2-13 Years after the Retreat of a Tropical Glacier. Frontiers in Ecology and Evolution 9: 584872. DOI: 10.3389/fevo.2021.584872 Aplet G.H., Hughes R.F., Vitousek P.M. 1998. Ecosystem development on Hawaiian lava flows: Biomass and species composition. Journal of Vegetation Science 9(1): 17-26. DOI: 10.2307/3237219
Barba-Escoto L., Ponce-Mendoza A., García-Romero A., Calvillo-Medina R.P. 2019. Plant community strategies responses to recent eruptions of Popocatépetl volcano, Mexico. Journal of Vegetation Science 30(2): 375-385. DOI: 10.1111/jvs.12732 Bardgett R.D., Mommer L., De Vries F.T. 2014. Going underground: Root traits as drivers of ecosystem processes. Trends in Ecology and Evolution 29(12): 692699. DOI: 10.1016/j.tree.2014.10.006 Bartusková A., Lubbe F.C., Qian J., Herben T., Klimesová J. 2022. The effect of moisture, nutrients and disturbance on storage organ size and persistence in temperate herbs. Functional Ecology 36(2): 314-325. DOI: 10.1111/1365-2435.13997 Belyea L.R., Lancaster J. 1999. Assembly Rules within a Contin-gentEcology. Oikos 86(3): 402-416. DOI: 10.2307/3546646 Bermúdez R., Retuerto R. 2013. Living the difference: Alternative functional designs in five perennial herbs coexisting in a coastal dune environment. Functional Plant Biology 40(11): 1187-1198. DOI: 10.1071/FP12392 Bezdelev A.B., Bezdeleva T.A. 2006. Life forms of seed plants of the Russian Far East. Vladivostok: Dalnauka. 295 p. [In Russian] Bilaya N.A., Korablev A.P., Zelenkovsky P.S., Chukov S.N. 2022. Ecological and Geochemical Features of Soils of the Tolbachik Dol Volcanic Plateau. Eurasian Soil Science 55(4): 404-412. DOI: 10.1134/S1064229322040044 Billings W.D. 1974. Arctic and alpine vegetations: Plant adaptations to cold summer climates. In: J.D. Ives, R.G. Barry (Eds.): Arctic and Alpine Environments. London: Methuen. P. 403-443. Caccianiga M., Luzzaro A., Pierce S., Ceriani R.M., Cerabolini B. 2006. The functional basis of a primary succession resolved by CSR classification. Oikos 112(1): 10-20. DOI: 10.1111/j.0030-1299.2006.14107.x Chapin D.M., Bliss L.C. 1989. Seedling Growth, Physiology, and Survivorship in a Subalpine, Volcanic Environment. Ecology 70(5): 1325-1334. DOI: 10.2307/1938192 Chapin F.S., Matson P.A., Vitousek P.M. 2011. Principles of Terrestrial Ecosystem Ecology. New York: Springer. 529 p. DOI: 10.1007/978-1-4419-9504-9 Ciccarelli D. 2015. Mediterranean coastal dune vegetation: Are disturbance and stress the key selective forces that drive the psammophilous succession?. Estuarine, Coastal and Shelf Science 165: 247-253. DOI: 10.1016/j.ecss.2015.05.023 Clements F.E. 1916. Plant succession: An analysis of the development of vegetation. Washington: Carnegie Institution of Washington. 512 p. DOI: 10.5962/bhl.title.56234 Crisafulli C.M., Swanson F.J., Halvorson J.J., Clarkson B.D. 2015. Volcano Ecology: Disturbance Characteristics and Assembly of Biological Communities. In: H. Sigurdsson (Ed.): The Encyclopedia of Volcanoes (Second Edition). USA: Academic Press. P. 12651284. DOI: 10.1016/B978-0-12-385938-9.00073-0 Cutler N. 2010. Long-term primary succession: A comparison of non-spatial and spatially explicit inferential techniques. Plant Ecology 208(1): 123-136. DOI: 10.1007/s11258-009-9692-2 Cutler N.A., Belyea L.R., Dugmore A.J. 2008. Spatial patterns of microsite colonisation on two young lava flows
on Mount Hekla, Iceland. Journal of Vegetation Science 19(2): 277-286. DOI: 10.3170/2008-8-18371 Danin A. 1991. Plant adaptations in desert dunes. Journal of Arid Environments 21(2): 193-212. DOI: 10.1016/ S0140-1963(18)30682-7 del Moral R. 2007. Limits to convergence of vegetation during early primary succession. Journal of Vegetation Science 18(4): 479-488. DOI: 10.1111/j.1654-1103.2007.tb02562.x del Moral R., Bliss L.C. 1993. Mechanisms of Primary Succession: Insights Resulting from the Eruption of Mount St Helens. Advances in Ecological Research 24: 1-66. DOI: 10.1016/S0065-2504(08)60040-9 Diaz S., Kattge J., Cornelissen J.H., Wright I.J., Lavorel S., Dray S., Reu B., Kleyer M., Wirth C., Prentice I.C., Garnier E., Bonisch G., Westoby M., Poorter H., Reich P.B., Moles
A.T., Dickie J., Gillison A.N., Zanne A.E., Chave J., Wright S.J., Sheremet'ev S.N., Jactel H., Baraloto C., Cerabolini B., Pierce S., Shipley B., Kirkup D., Casanoves F., Joswig J.S. et al. 2016. The global spectrum of plant form and function. Nature 529(7585): 167-171. DOI: 10.1038/nature16489
Elias R.B., Dias E. 2007. The role of habitat features in a primary succession. Arquipelago. Life and Marine Sciences 24: 1-10. Fedosov S.A. (Ed.). 1984. The Great Fissure Tolbachik Eruption (1975-1976, Kamchatka). Moscow: Nauka. 638 p. [In Russian] Franzen M., Dieker P., Schrader J., Helm A. 2019. Rapid plant colonization of the forelands of a vanishing glacier is strongly associated with species traits. Arctic, Antarctic, and Alpine Research 51(1): 366-378. DOI: 10.1080/15230430.2019.1646574 Freschet G.T., Pages L., Iversen C.M., Comas L.H., Rewald
B., Roumet C., Klimesova J., Zadworny M., Poorter H., Postma J.A., Adams T.S., Bagniewska-Zadworna A., Bengough A.G., Blancaflor E.B., Brunner I., Cornelissen J.H.C., Garnier E., Gessler A., Hobbie S.E., Meier I.C., Mommer L., Picon-Cochard C., Rose L., Ryser P., Scherer-Lorenzen M., Soudzilovskaia N.A., Stokes A., Sun T., Valverde-Barrantes O.J., Weemstra M. et al. 2021. A starting guide to root ecology: Strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements. New Phy-
■ tologist 232(3): 973-1122. DOI: 10.1111/nph.17572
Fuller R.N., del Moral R. 2003. The role of refugia and dispersal in primary succession on Mount St. Helens, Washington. Journal of Vegetation Science 14(5): 637644. DOI: 10.1111/j.1654-1103.2003.tb02195.x Garnier E., Navas M.L., Grigulis K. 2016. Plant functional diversity: Organism traits, community structure, and ecosystem properties. Oxford: Oxford University Press. 231 p. DOI: 10.1093/acprof:oso/9780198757368.001.0001 Garren S.T. 2019. Permutation Tests for Nonparametric Statistics. Ver. 2.2. Available from https://cran.r-project.org/ web/packages/jmuOutlier/jmuOutlier.pdf Gorchakovskii P.L., Stepanova A.V. 1995. Formation of Morphological Structure of the Alpine Cushion-Shaped Dwarf Semishrub Gypsophila uralensis Less. in the Course of Ontogenesis. Ekologiya 26(6): 424427. [In Russian]
Grime J.P., Pierce S. 2012. The evolutionary strategies that shape
ecosystems. Oxford: John Wiley & Sons, Ltd. 240 p. Gyssels G., Poesen J., Bochet E., Li Y. 2005. Impact of plant roots on the resistance of soils to erosion by water: A review. Progress in Physical Geography 29(2): 189-217. DOI: 10.1191/0309133305pp443ra Harris T., Klimes A., Martínková J., Klimesová J. 2023. Herbs are not just small plants: What biomass allocation to rhizomes tells us about differences between trees and herbs. American Journal of Botany 110(7): e16202. DOI: 10.1002/ajb2.16202 Hodgson J.G., Montserrat-Martí G., Charles M., Jones G., Wilson P., Shipley B., Sharafi M., Cerabolini B.E.L., Cornelissen J.H.C., Band S.R., Bogard A., Castro-Díez P., Guerrero-Campo J., Palmer C., Pérez-Rontomé M.C., Carter G., Hynd A., Romo-Díez A., De Torres Espuny L., Royo Pla F. 2011. Is leaf dry matter content a better predictor of soil fertility than specific leaf area?. Annals of Botany 108(7): 1337-1345. DOI: 10.1093/aob/mcr225 Ivanova L.A., Yudina P.K., Ronzhina D.A., Ivanov L.A., Holzel N. 2018. Quantitative mesophyll parameters rather than whole-leaf traits predict response of C3 steppe plants to aridity. New Phytologist 217(2): 558570. DOI: 10.1111/nph.14840 Joswig J.S., Wirth C., Schuman M.C., Kattge J., Reu B., Wright I.J., Sippel S.D., Rüger N., Richter R., Schaep-man M.E., van Bodegom P.M., Cornelissen J.H.C., Díaz S., Hattingh W.N., Kramer K., Lens F., Niinemets Ü., Reich P.B., Reichstein M., Römermann C., Schrodt
F., Anand M., Bahn M., Byun C., Campetella G., Cerabolini B.E.L., Craine J.M., Gonzalez-Melo A., Gutiérrez A.G., He T. et al. 2021. Climatic and soil factors explain the two-dimensional spectrum of global plant trait variation. Nature Ecology and Evolution 6(1): 36-50. DOI: 10.1038/s41559-021-01616-8
Kattge J., Bönisch G., Díaz S., Lavorel S., Prentice I.C., Leadley P., Tautenhahn S., Werner G.D.A., Aakala T., Abedi M., Acosta A.T.R., Adamidis G.C., Adam-son K., Aiba M., Albert C.H., Alcántara J.M., Alcázar C.C., Aleixo I., Ali H., Amiaud B., Ammer C., Amoroso M.M., Anand M., Anderson C., Anten N., Antos J., Apgaua D.M.G., Ashman T.L., Asmara D.H., Asner
G.P., Aspinwall M. et al. 2020. TRY plant trait database - enhanced coverage and open access. Global Change Biology 26(1): 119-188. DOI: 10.1111/gcb.14904
Keddy P.A. 1992. Assembly and response rules: Two goals for predictive community ecology. Journal of Vegetation Science 3(2): 157-164. DOI: 10.2307/3235676 Klimesová J. 2021. An Integrated Plant Architecture: Roots, Shoots, and Everything in Between. Annual Plant Reviews online 4(2): 529-550. DOI: 10.1002/9781119312994.apr0753 Korablev A.P., Neshataeva VYu. 2016. Primary plant successions of forest belt vegetation on the Tolbachinskii Dol volcanic plateau (Kamchatka). Biology Bulletin 43(4): 307-317. DOI: 10.1134/S1062359016040051 Korablev A.P., Smirnov VE., Neshataeva V.Y., Kuzmin I.V. 2018. Plant Life-Forms and Environmental Filtering during Primary Succession on Loose Volcanic Substrata
(Kamchatka, Russia). Biology Bulletin 45(3): 255-264. DOI: 10.1134/S106235901803007X Korablev A., Smirnov V, Neshataeva V, Kuzmin I., Nekrasov T. 2020. Plant dispersal strategies in primary succession on the Tolbachinsky Dol volcanic Plateau (Russia). Journal ofVeg-etation Science 31(6): 954-966. DOI: 10.1111/jvs.12901 Kraft N.J.B., Godoy O., Levine J.M. 2015. Plant functional traits and the multidimensional nature of species coexistence. Proceedings of the National Academy of Sciences of the United States of America 112(3): 797802. DOI: 10.1073/pnas.1413650112 Laliberté E., Legendre P. 2010. A distance-based framework for measuring functional diversity from multiple traits. Ecology 91(1): 299-305. DOI: 10.1890/08-2244.1 Lambers H., Poorter H. 2004. Inherent Variation in Growth Rate Between Higher Plants: A Search for Physiological Causes and Ecological Consequences. Advances in Ecological Research 34: 283-362. DOI: 10.1016/ S0065-2504(03)34004-8 Lavorel S., Garnier E. 2002. Predicting changes in community composition and ecosystem functioning from plant traits: Revisiting the Holy Grail. Functional Ecology 16(5): 545-556. DOI: 10.1046/j.1365-2435.2002.00664.x MacArthur R.H. 1984. Geographical Ecology: Patterns in the Distribution of Species. Princeton: Princeton University Press. 288 p. Mahdavi P., Bergmeier E. 2016. Plant functional traits and diversity in sand dune ecosystems across different bio-geographic regions. Acta Oecologica 74: 37-45. DOI: 10.1016/j.actao.2016.06.003 Marleau J.N., Jin Y., Bishop J.G., Fagan W.F., Lewis M.A. 2011. A Stoichiometric Model of Early Plant Primary Succession. American Naturalist 177(2): 233-245. DOI: 10.1086/658066 Marteinsdóttir B., Thórhallsdóttir T.E., Svavarsdóttir K. 2013. An experimental test of the relationship between small scale topography and seedling establishment in primary succession. Plant Ecology 214(8): 1007-1015. DOI: 10.1007/s11258-013-0226-6 Marteinsdóttir B., Svavarsdóttir K., Thórhallsdóttir T.E. 2018. Multiple mechanisms of early plant community assembly with stochasticity driving the process. Ecology 99(1): 91-102. DOI: 10.1002/ecy.2079 Matveeva NV (Ed.). 2015. Plants andfungi of the polar deserts in the northern hemisphere. Saint-Petersburg: Marafon. 320 p. [In Russian] Mudrák O., Rehounková K., Vítovcová K., Tichy L., Prach K. 2021. Ability of plant species to colonise human-disturbed habitats: Role of phylogeny and functional traits. Applied Vegetation Science 24(1): e12528. DOI: 10.1111/avsc.12528 Muñoz G., Orlando J., Zuñiga-Feest A. 2021. Plants colonizing volcanic deposits: Root adaptations and effects on rhizo-sphere microorganisms. Plant and Soil 461(1-2): 265-279. DOI: 10.1007/s11104-020-04783-y Neshataeva V.Yu. (Ed.). 2014. Vegetation cover of the Central Kamchatka volcanic plateaus (Kluchevskaya group of volcanoes). Moscow: KMK Scientific Press Ltd. 461 p. [In Russian]
Pakeman R.J., Lennon J.J., Brooker R.W. 2011. Trait assembly in plant assemblages and its modulation by productivity and disturbance. Oecologia 167(1): 209-218. DOI: 10.1007/s00442-011-1980-6 Pérez-Harguindeguy N., Díaz S., Garnier E., Lavorel S., Poorter H., Jaureguiberry P., Bret-Harte M.S., Cornwell W.K., Craine J.M., Gurvich D.E., Urcelay C., Veneklaas E.J., Reich P.B., Poorter L., Wright I.J., Ray P., Enrico L., Pausas J.G., de Vos A.C., Buchmann N., Funes G., Quétier F., Hodgson J.G., Thompson K., Morgan H.D., ter Steege H., van der Heijden M.G.A., Sack L., Blonder B., Poschlod P. et al. 2013. New handbook for standardised measurement of plant functional traits worldwide. Australian Journal of Botany 61(3): 167234. DOI: 10.1071/BT12225 Pierce S., Negreiros D., Cerabolini B.E.L., Kattge J., Díaz S., Kleyer M., Shipley B., Wright S.J., Soudzilovskaia N.A., Onipchenko V.G., van Bodegom P.M., Frenette-Dussault C., Weiher E., Pinho B.X., Cornelissen J.H.C., Grime J.P., Thompson K., Hunt R., Wilson P.J., Buffa G., Nyakunga O.C., Reich P.B., Caccianiga M., Mangili F., Ceriani R.M., Luzzaro A., Brusa G., Siefert A., Barbosa N.P.U., Chapin F.S. et al. 2017. A global method for calculating plant CSR ecological strategies applied across biomes world-wide. Functional Ecology 31(2): 444-457. DOI: 10.1111/1365-2435.12722 Prach K., Pysek P., Smilauer P. 1997. Changes in Species Traits during Succession: A Search for Pattern. Oikos 79(1): 201-205. DOI: 10.2307/3546109 Pyankov V.I., Ivanov L.A., Lambers H. 2001. Plant construction cost in the boreal species differing in their ecological strategies. Russian Journal of Plant Physiology 48(1): 67-73. DOI: 10.1023/A:1009002715572 Qi Y., Wei W., Chen C., Chen L. 2019. Plant root-shoot biomass allocation over diverse biomes: A global synthesis. Global Ecology and Conservation 18: e00606. DOI: 10.1016/j.gecco.2019.e00606 R Core Team. 2020. R: A Language and Environment for Statistical Computing. Vienna: R Foundation for Statistical Computing. Available from https://www.R-project.org Ramensky L.G. 1938. Introduction to the Complex Soil-Geobotanical Investigation of Lands. Moscow: Selk-hozgiz. 620 p. [In Russian] Rehounková K., Prach K. 2010. Life-history traits and habitat preferences of colonizing plant species in long-term spontaneous succession in abandoned gravel-sand pits. Basic and Applied Ecology 11(1): 45-53. DOI: 10.1016/j.baae.2009.06.007 Será B., Seiy M. 2004. Number and weight of seeds and reproductive strategies of herbaceous plants. Folia Geobotanica 39(1): 27-40. DOI: 10.1007/BF02803262 Serebryakov I.G. 1962. Ecological morphology of plants: Life forms of angiosperms and conifers. Moscow: Vys-shaya Shkola. 380 p. [In Russian] Song M., Duan D., Chen H., Hu Q., Zhang F., Xu X., Tian Y., Ouyang H., Peng C. 2008. Leaf 513C reflects ecosystem patterns and responses of alpine plants to the environments on the Tibetan Plateau. Ecography 31(4): 499-508. DOI: 10.1111/j.0906-7590.2008.05331.x
Sonnier G., Shipley B., Navas M.L. 2010. Quantifying relationships between traits and explicitly measured gradients of stress and disturbance in early succes-sional plant communities. Journal of Vegetation Science 21(6): 1014-1024. DOI: 10.1111/j. 1654-1103.2010.01210.x Sutomo S., Fardila D., Putri L.S.E. 2011. Species composition and interspecific association of plants in primary succession of Mount Merapi, Indonesia. Biodiversitas 12(4): 212-217. DOI: 10.13057/biodiv/d120405 Tagawa H. 1992. Primary succession and the effect of first arrivals on subsequent development of forest types. GeoJournal 28(2): 175-183. DOI: 10.1007/BF00177231 Titus J.H., Tsuyuzaki S. 2003. Distribution of plants in relation to microsites on recent volcanic substrates on Mount Koma, Hokkaido, Japan. Ecological Research 18(1): 91-98. DOI: 10.1046/j.1440-1703.2003.00536.x Tsuyuzaki S. 2009. Causes of plant community divergence in the early stages of volcanic succession. Journal of Vegetation Science 20(5): 959-969. DOI: 10.1111/j. 1654-1103.2009.01104.x Tsuyuzaki S., del Moral R. 1995. Species attributes in early primary succession on volcanoes. Journal of Vegetation Science 6(4): 517-522. DOI: 10.2307/3236350 Vasilevich VI. 2016. Functional diversity in plant communities. Botanicheskii Zhurnal 101(7): 776-795. DOI: 10.1134/S0006813616070024 [In Russian] Velázquez A., Giménez de Azcárate J., Weinmann M.E., Bocco G. 2000. Vegetation dynamics on Paricutin, a recent Mexican volcano. Acta Phytogeographica Suecica 85: 71-78. Vilmundardóttir O.K., Sigurmundsson F.S., Moller Peder-sen G.B., Belart J.M.C., Kizel F., Falco N., Benedikts-son J. A., Gísladóttir G. 2018. Of mosses and men: Plant succession, soil development and soil carbon accretion in the sub-Arctic volcanic landscape of Hekla, Iceland. Progress in Physical Geography 42(6): 765791. DOI: 10.1177/0309133318798754 Voronkova N.M., Kholina A.B., Verkholat V.P. 2008. Plant biomorphology and seed germination in pioneer species of Kamchatka volcanoes. Biology Bulletin 35(6): 599-605. DOI: 10.1134/S106235900806006X Voronkova N.M., Verkholat V.P., Kholina A.B. 2011. Specific features of plants at early stages of the colonization of loose volcanic matter. Biology Bulletin 38(3): 237-241. DOI: 10.1134/S1062359011030150 Walker L.R., del Moral R. 2003. Primary succession and ecosystem rehabilitation. Cambridge: Cambridge University Press. 422 p. DOI: 10.1017/CBO9780511615078 Walker L.R., Bellingham P.J., Peltzer D.A. 2006. Plant characteristics are poor predictors of microsite colonization during the first two years of primary succession. Journal of Vegetation Science 17(3): 397-406. DOI: 10.1111/j.1654-1103.2006.tb02460.x Wright I.J., Reich P.B., Westoby M., Ackerly D.D., Baruch Z., Bongers F., Cavender-Bares J., Chapin T., Cornelissen J.H., Diemer M., Flexas J., Garnier E., Groom P.K., Gulias J., Hikosaka K., Lamont B.B., Lee T., Lee W., Lusk C., Midgley J.J., Navas M.L., Niinemets U., Oleksyn J., Osada N., Poorter H., Poot P., Prior L., Py-
ankov VI., Roumet C., Thomas S.C. et al. 2004. The worldwide leaf economics spectrum. Nature 428(6985): 821-827. DOI: 10.1038/nature02403 Wright I.J., Reich P.B., Cornelissen J.H.C., Falster D.S., Garnier E., Hikosaka K., Lamont B.B., Lee W., Oleksyn J., Osada N., Poorter H., Villar R., Warton D.I., Westoby M. 2005. Assessing the generality of global leaf trait relationships. New Phytologist 166(2): 485-496. DOI: 10.1111/j.1469-8137.2005.01349.x Yurtsev B.A., Koroleva T.M., Petrovsky V V, Polozova T.G., Zhukova P.G., Katenin A.E. 2010. Summary of the flora of the Chukotka tundra. Saint-Petersburg: BBM. 628 p. [In Russian]
Zakharikhina LV, Litvinenko Yu.S. 2011. Genetic and Geo-chemical Characteristics of Soils of Kamchatka. Moscow: Nauka. 244 p. [In Russian] Zakharikhina LV, Litvinenko Yu.S. 2019. Volcanism and geochemistry of soil and vegetation cover of Kamchatka. Communication 2. Specificity of forming the elemental composition of volcanic soil in cold and humid conditions. Vulkanologia i sejsmologia 3: 25-33. DOI: 10.31857/ S0203-03062019325-33 [In Russian] Zobel D.B., Antos J.A. 2009. Species properties and recovery from disturbance: Forest herbs buried by volcanic tephra. Journal of Vegetation Science 20(4): 650-662. DOI: 10.1111/j.1654-1103.2009.01057.x
БИОМОРФОЛОГИЧЕСКИЕ ПРИЗНАКИ РАСТЕНИЙ И СОДЕРЖАНИЕ СУХОГО ВЕЩЕСТВА В ЛИСТЕ ВАЖНЫ ДЛЯ УСТОЙЧИВОСТИ РАСТЕНИЙ К ПОДВИЖНОМУ ВУЛКАНИЧЕСКОМУ ГРУНТУ
А. П. Кораблев1* , Е. В. Сандалова12 , К. А. Арапов1 , К. М. Зарипова13
1Ботанический институт имени В.Л. Комарова РАН, Россия *e-mail: akorablev@binran. т Московский государственный университет имени М.В. Ломоносова, Россия 3 Санкт-Петербургский федеральный исследовательский центр РАН, Россия
Колонизация растениями вновь образованных территорий (первичная сукцессия) - важнейший этап формирования экосистем. Именно адаптации видов к существованию в неблагоприятных условиях среды позволяют им выживать и формировать пионерные сообщества в первичных экотопах. Нами были рассмотрены 10 качественных и количественных признаков растений в контексте их адаптации к подвижности субстрата в условиях первичных вулканических местообитаний. Поставленные в исследовании вопросы: 1) Какие признаки растений позволяют им существовать в условиях наиболее подвижного грунта? 2) Какими экологическими стратегиями обладают виды, существующие одновременно в условиях стресса (низкого минерального питания) и интенсивных нарушений (подвижного грунта)? Исследования выполнены на плато Толбачинский дол (Камчатка, Россия) на рыхлых отложениях извержения 1975 г. На высотах 700-1000 м н.у.м. по градиентам высоты и степени подвижности грунта был заложен ряд пробных площадей. Оценены видовой состав сосудистых растений и проективное покрытие видов, а также другие характеристики местообитания. Связь признаков с подвижностью грунта исследована с помощью линейных моделей; группы характерных признаков выделены на основе метода главных компонент. В числе наиболее важных признаков выделяется содержание сухого вещества в листе (LDMC), средневзвешенные значения которого снижаются при увеличении степени нарушения (подвижности грунта). Помимо LDMC целый набор качественных признаков видов характеризует приспособленность растений к подвижному грунту: жизненная форма (по И.Г. Серебрякову), плотность расположения побегов и морфология системы подземных органов, а также в меньшей степени способ распространения плодов. Из 45 видов, проанализированных в исследовании, лишь 4 приспособлены к существованию в условиях высокой подвижности субстрата. Исследование показало, что сочетание ряда биоморфологических характеристик и процент содержания сухого вещества в листе формируют синдром пионерных видов, адаптированных к подвижному грунту. Экологические стратегии большинства видов в исследованных сообществах характеризуются преобладанием стресс-толерантной стратегии, что объясняется крайне бедными условиями минерального питания в первичных местообитаниях. В условиях одновременно низкой обеспеченности питательными веществами и высокой интенсивности нарушений преимущество получают виды смешанной стресс-толерант-рудеральной стратегии. В градиенте усиления нарушения возрастает участие видов с большей долей рудеральной стратегией при одновременном уменьшении стресс-толерантности. Однако роль экологической стратегии может ослабляться наличием других важных адаптационных признаков.
Ключевые слова: адаптация, вулканическое местообитание, экологическая стратегия, жизненная форма, Камчатка, площадь листа, функциональный признак, экстремальное местообитание, удельная листовая поверхность
