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Article

Silver Lime (Tilia tomentosa Moench) in Forest Vegetation at the Western Edge of the Natural Distribution

by
Irena Šapić
1,*,
Joso Vukelić
2,
Antun Alegro
3,
Stjepan Mikac
1,
Damir Ugarković
1,
Igor Poljak
4,* and
Dario Baričević
1
1
Department of Ecology and Silviculture, Faculty of Forestry and Wood Technology, University of Zagreb, Svetošimunska Cesta 23, 10000 Zagreb, Croatia
2
Department of Natural Resources Management, Oikon Ltd.—Institute of Applied Ecology, Trg Senjskih Uskoka 1-2, 10020 Zagreb, Croatia
3
Division of Botany, Department of Biology, University of Zagreb, Marulićev Trg 20/II, 10000 Zagreb, Croatia
4
Department of Forest Genetics, Dendrology and Botany, Faculty of Forestry and Wood Technology, University of Zagreb, Svetošimunska Cesta 23, 10000 Zagreb, Croatia
*
Authors to whom correspondence should be addressed.
Forests 2025, 16(3), 438; https://doi.org/10.3390/f16030438
Submission received: 21 January 2025 / Revised: 18 February 2025 / Accepted: 24 February 2025 / Published: 28 February 2025
(This article belongs to the Special Issue Distribution of Tree Species in a Changing Environment)
Browse Figures
Figure 1
<p>Geographic distribution of <span class="html-italic">Tilia tomentosa</span> in Europe (adapted from Meusel et al. [<a href="#B6-forests-16-00438" class="html-bibr">6</a>]), highlighting Zrinska Gora Mt as the westernmost point of its natural distribution.</p> "> Figure 2
<p>Ellenberg-type indicator values Box and whisker for three groups of forest associations on Zrinska Gora Mt regarding presence of silver lime (I &gt; 50%, II &lt; 50%, III = 0).</p> "> Figure 3
<p>PCA analysis of <span class="html-italic">Tilia tomentosa</span> communities in the western Balkans with passively projected vectors representing Ellenberg-type ecological indicator values (L—light, T—temperature, M—moisture, pH—soil reaction, N—nutrients); Country codes: CRO—Croatia, HU—Hungary, B&amp;H—Bosnia and Hercegovina, SRB—Serbia; Symbols indicate silver lime presence in communities (▲ &gt; 50%, ∆ &lt; 50%, ⃝ &lt; 10%); Red represents Western Balkan communities, blue represents communities from Zrinska Gora Mt.</p> ">
Review Reports Versions Notes

Abstract

:
Silver lime is a thermophilic, calciphile species that thrives in xero-mesophilic forest communities. The westernmost edge of its natural distribution is Zrinska Gora Mountain in central Croatia, where it is found in almost all types of forest vegetation, albeit with varying frequencies. Its ecological optimum is in specific ravines and grooves, where it forms the mesophilic, relict broad-leaved ravine forest community Polysticho setiferi-Tilietum tomentosae. This research was conducted on two levels. Firstly, the communities of Zrinska Gora were analyzed as the westernmost edge of the natural distribution. Secondly, the ecology of the Tilia tomentosa communities in the western part of its distribution (Croatia, Bosnia and Herzegovina, Hungary, and Serbia) was observed. Analysis of Ellenberg-type indicator values for 74 communities from the western Balkans revealed a slight trend of decreasing thermophilicity and increasing acidophilicity toward the western edge of the distribution area. Silver lime peripheral populations on Zrinska Gora develop under unique ecological conditions. The soil reaction of all communities falls below the lower limit of the optimal range for its development, and the relict association experiences lower temperature values compared to the other communities. All in all, the results of this study provide insights into the adaptability of silver lime to climate change.

1. Introduction

The silver lime (Tilia tomentosa Moench, Malvaceae) is a large-sized deciduous broad-leaved tree species native to Southeast Europe and Western Asia. Its relatively limited distribution area stretches from the Dinaric Mountains, through Moldova, to the northwestern part of Anatolia (Figure 1). This species typically thrives at altitudes between 150 and 500 m a.s.l. However, it can also be found at higher altitudes, up to 1000 m in southern Romania and eastern Bulgaria, and up to 1300 m in Albania [1].
Silver lime is a calciphile species that thrives in deep, mineral-rich soils abundant in humus. Predominantly, these are sandy soils with a pH value ranging from 5.8 to 8.2 [1]. It avoids clay and pseudogley soils typically found on plateaus and floodplains [2]. Sociologically, this species is classified within the order Quercetalia pubescentis, and its phytocoenoses are generally classified as xeromesophilic [3,4,5].
Forests 16 00438 g001
Figure 1. Geographic distribution of Tilia tomentosa in Europe (adapted from Meusel et al. [6]), highlighting Zrinska Gora Mt as the westernmost point of its natural distribution.
Figure 1. Geographic distribution of Tilia tomentosa in Europe (adapted from Meusel et al. [6]), highlighting Zrinska Gora Mt as the westernmost point of its natural distribution.
Forests 16 00438 g001
Within the central part of its natural distribution area, the silver lime forms mixed stands with species such as Quercus robur, Carpinus betulus, Ulmus minor and Acer campestre, as well as mixed stands of forest steppes, predominantly with Quercus pubescens and Fraxinus ornus. Silver lime can also thrive in relatively compact soils, where it grows alongside oaks like Quercus cerris, Q. frainetto, and Q. pubescens. In southeastern Romania, it even forms pure stands [2,7,8].
In the western Balkans, silver lime can be found in the lowland belt as a sporadic species in the pedunculate oak (Quercus robur) forests [5,9,10], and Quercus cerris forests with steppic elements [11,12]. Furthermore, in the colline and mountain belts, it occurs within thermophilic Quercus pubescens and Q. petraea communities [13,14], Quercus frainetto communities [15,16], Carpinus orientalis communities [17,18], in mixed stands with Carpinus betulus, Quercus petraea [19,20,21], and Fagus sylvatica [22,23,24]. In the eastern Balkans, it grows in mixed stands with Moesian beech [25], a species that has recently been considered a lowland ecotype of the common beech (F. sylvatica) [26,27]. In the western part of the distribution area, the relict character of silver lime is more prominent, making it common in broad-leaved ravine forests [28,29,30].
The westernmost edge of silver lime natural distribution is Zrinska Gora Mt in central Croatia, on the borderline of the Pannonian Plain and the Dinaric mountains. There, the relief, soil, and climate have created a specific ecological niche for silver lime. This niche differs from those in other parts of its distribution area, where it is mostly a thermophilic species developing in xero-mesophilic forest communities. On Zrinska Gora Mt, the silver lime is present in almost all types of forest vegetation but with varying frequencies [31]. However, its ecological optimum is in specific ravines and grooves where it forms the mesophilic broad-leaved ravine forest community Polysticho setiferi-Tilietum tomentosae (in the further text, Polysticho-Tilietum).
It is well known that these edge populations, also known as peripheral populations, may be more sensitive to climate change compared to those in the center of the distribution area [32]. Considering this, the adaptability of these populations is a key question, as they often occupy habitats that differ from those in the center of the distribution area [33]. Peripheral populations are typically characterized by unique ecological conditions and may exhibit different adaptive traits compared to central populations [34]. Understanding these differences is essential for developing effective conservation strategies, especially in the context of ongoing climate change [35]. Therefore, this study represents a new contribution to the more reliable development of long-term strategies in the management and conservation of silver lime peripheral populations and their habitats. The objectives of this study were: (I) to analyze the occurrence of silver lime in forest communities in the western part of its distribution area; (II) to determine synecological diversity; and (III) to identify the most important ecological factors determining its occurrence in the study area.

2. Materials and Methods

The primary input for analyzing the occurrence of Tilia tomentosa and the ecological factors crucial for its distribution are pre-determined forest communities. In this study, forest communities serve as the basic unit for defining habitat conditions.
The research was conducted on two levels. Firstly, the communities of Zrinska Gora Mt were analyzed as the westernmost edge of the natural distribution. Secondly, the ecology of Tilia tomentosa communities in the western part of the distribution area (Croatia, Bosnia and Herzegovina, Hungary, and Serbia) was observed.

2.1. Study Area

Zrinska Gora Mt is situated in central Croatia, at the far southwestern edge of the Pannonian plain. It is influenced by the Dinarides from the south and the Alps from the west. The area is characterized by highly indented relief with numerous elongated ridges and deep-cut creek valleys (Figure 1). The highest peak is 617 m above sea level, while the lowest point is at 115 m. The mountain is intersected by faults in various directions, creating a complex structure with long longitudinal and transverse, mostly asymmetrical ridges and narrow river and stream valleys. The largest part of Zrinska Gora Mt is composed of carbonate flysch and clastites of the Paleocene and Eocene ages, as well as clastites and carbonates with clastites from the Miocene age. The climate is moderately warm and humid with warm summers (Cfb code). The mean annual temperature is 10.8 °C, with an average temperature of 20.7 °C in July. Annual precipitation is 1075 mm, with the maximum occurring in September (meteorological station Hrvatska Kostajnica, 1981 to 2021, https://meteo.hr/, accessed on 6 September 2024). Meteorological data for the Western Balkan area were taken from the KNMI Climate Explorer web platform (https://climexp.knmi.nl/, accessed on 16 February 2025; Table S1).
The study area is generally characterized by soils with a pH lower than what is typically known for silver lime habitats [36]. The dominant soil type is distric cambisol, represented by numerous varieties and forms, most commonly as lessive and pseudogleyed subtypes, with textures ranging from sand-loam to clay-loam. The humus-accumulative horizon is rich in humus and well stocked with nitrogen, with a pH below 5, while the pH in the cambic horizon does not exceed 5.5. On the steep slopes and ridges above the silicate substrate, shallow humus silicate soils, known as rankers, have developed. These soils are also rich in humus and nitrogen, with a pH below 5.5. Due to their sandy-loamy texture and steep positions, these soils drain faster compared to the previous type, affecting the composition of vegetation. The presence of calcocambisols is defined by the occurrence of solid limestone rocks, mainly lithotamnium limestones. The humus-accumulative horizon in these soils is very humic and rich in nitrogen, with a pH of 4.7, while the pH in the cambic horizon ranges between 5 and 5.5. Along the canyons and narrow terraces beside the watercourses, colluvium appears as a result of soil erosion and deposition of rocks, stones, and organic matter from higher positions. To establish the correlation between Ellenberg-type indicator values and measured soil pH values, 50 composite samples of the soils surface layer were analyzed. A Pearson’s correlation test performed in XLSTAT confirmed a significant correlation. In beech forest (Cephalanthero-Fagetum), where the frequency of silver lime varied, 30 composite samples were made. In addition, 10 samples were taken in the black alder community (Stellario-Alnetum), where the silver lime has not been recorded, and 10 samples in the broad-leaved ravine forest community (Polysticho-Tilietum), where silver lime is the dominant tree species. The forest vegetation of Zrinska Gora Mt belongs to the Central European province with a weak Dinaric influence. It consists of 321 species and subspecies of vascular plants and 44 bryophyte species. Species and subspecies of higher plants belong to 78 families [31].

2.2. Vegetation Data

Zrinska Gora Mt was originally presented with 133 relevés classified into 11 forest communities [36], of which 10 communities (116 relevés) were included in the analysis. Relevés were made using the Central European phytocoenological method (Braun–Blanquet, 1964), on plots 20 × 20 m (400 m2). Cover and abundance of the tree layer (A), shrub layer (B), herb layer (C), and bryophytes (D) were assessed using the seven-degree Braun–Blanquet scale with gradings r to 5.
To better characterize the habitats favored by Tilia tomentosa on Zrinska Gora, the communities were classified into three groups. Group I includes communities where silver lime is present in more than 50% of the relevés. This group comprises the Polysticho-Tilietum, Cephalanthero-Fagetum circetosum lutetianae, and Festuco-Carpinetum communities, with a total of 58 relevés. Group II consists of 45 relevés from the Cephalanthero-Fagetum typicum, Castaneo-Fagetum, Aposeridi-Castaneetum, Potentillo-Quercetum, and Pteridio-Betuletum communities, where silver lime is present in less than 50% of the relevés, mostly in the shrub layer. Group III includes 13 relevés from the Querco-Castaneetum and Luzulo-Fagetum communities, where silver lime is absent. These two communities (Group III) were analyzed because they are floristically and ecologically very similar to those in which silver lime was recorded, and we were aiming to better understand the ecological requirements of this species and identify which ecological parameters prevent silver lime from appearing in them. The 17 relevés of the Stellario-Alnetum community were omitted from this analysis because it is clear that silver lime is absent there due to very high humidity, while other habitats are quite similar in terms of ecological parameters.
To compare the ecology of silver lime across the western Balkans (Croatia, Bosnia and Herzegovina, Hungary, and Serbia), its occurrence in forest communities and Ellenberg-type indicator values were analyzed from the westernmost edge towards the central part of the natural distribution. The initial dataset comprised 3225 vegetation plots with the occurrence of Tilia tomentosa across its entire natural distribution area, sourced from the European Vegetation Archive (EVA; [37] data exported on 26 February 2020). This dataset served as a guideline for identifying forest communities where silver lime occurs. In this study, only the communities from the western part of the range, limited to Serbia, Hungary, Croatia, and Bosnia and Herzegovina, were analyzed. The data were supplemented with relevés from the same communities and areas as originally published, to obtain more comprehensive data on the ecology of the communities. Finally, a total of 1281 relevés of forest communities (associations, sub-associations) from different areas of the western Balkans were analyzed, originally classified into 74 groups.
In this paper, all communities are presented with their original names as originally published. Nomenclature issues are not addressed in the paper; all data were used primarily for the purpose of ecological characterization of habitats. Research was conducted according to the principles of the standard Central European Phytocoenological School [38]. The nomenclature of taxa follows the internet database Euro+Med PlantBase [39] for vascular plants and Hodgetts et al. [40] for bryophytes. The affiliation of species and communities to higher syntaxons was determined according to the latest review of forest vegetation in Croatia [41].

2.3. Statistical Analysis

Relevés were stored in the TURBOVEG 2 database [42]. To quantify environmental factors on a micro scale, Ellenberg-type indicator values for light, temperature, moisture, reaction, and nutrients were used [43] with JUICE 7.0 [44]. Descriptive analysis of Ellenberg-type indicator values was conducted using STATISTICA 8.0 [45].
A non-parametric Kruskal–Wallis test (p < 0.05) was used to determine whether there are significant differences in environmental parameters between the three groups. Additionally, a Mann–Whitney U test (p < 0.05) of Ellenberg-type indicator values for Group II and Group III was performed. For better synecological characterization of the groups, species combinations were calculated using JUICE 7.0 [44]. Species with a frequency higher than 10% and modified fidelity phi-coefficient higher than 10 were considered for each group.
Pre-treatment of environmental data by variable normalization and PCA analysis with projected vectors based on Ellenberg-type indicator values was conducted using PRIMER 6 [46]. PCA analysis with unweighted average indicator values was used for interpretation of ecological conditions.

3. Results

3.1. Westernmost Edge of the Area of Distribution

In Zrinska Gora Mt, at the westernmost edge of its distribution, silver lime is present in 8 of 11 forest communities. In most communities, it appears sporadically, with a more pronounced presence only within the shrub layer (Table 1). It occurs frequently in more than 50% of relevés in the associations Polysticho-Tilietum, Cephalanthero-Fagetum circetosum lutetianae, and Festuco-Carpinetum (Group I), achieving a cover-abundance scale degree of + to 4, both in the tree and/or shrub layer. The Kruskal–Wallis test indicated that Group I significantly differs from Group II and Group III in terms of all ecological parameters.
These three communities of Group I have significantly higher values for three ecological parameters: moisture, pH, and nutrients. They are distinguished from the communities of Group II and Group III by significantly lower light values and lower temperatures (Table 1, Figure 2). The Polysticho-Tilietum community represents the coldest habitats of Zrinska Gora Mt, and is the only one where Tilia tomentosa dominates both the tree and shrub layers. This broad-leaved ravine forest community has colluvial soils with a mean pH (H2O) value of 5.44 (min. 5.16, max. 5.93) and a pH (CaCl2) value of 4.68 (min. 4.37, max. 5.33). It is the community with the highest pH measured compared to other analyzed forest communities (except for the black alder community, which was not included in this research due to a limiting moisture factor).
Group I is characterized by a high frequency and fidelity index of Tilia tomentosa, Fagus sylvatica, Ulmus glabra, and Sambucus nigra (Table 2) in both the tree layer (A) and in shrub layer (B). This group differs from the other two groups due to the increased frequency and fidelity index of Lamium galeobdolon, Galium odoratum, Mycelis muralis, Cardamine bulbifera, and other species characteristic for the order Fagetalia sylvaticae. Additionally, in the herb layer, species such as Polystichum setiferum, Cardamine waldsteinii, Doronicum austriacum, Lunaria rediviva, Aruncus dioicus, Athyrium filix-femina, Dryopteris filix-mas, Carex pendula, and Alliaria petiolata are more frequent. Generally, these species, are sociologically defined as characteristic for Fagetalia sylvaticae, Tilio-Acerion, Aremonio-Fagion, Alnion incanae, Adenostyletalia, and Galio-Urticetea, which all comprise mesophilic species of deeper, more humus-rich soils and shaded habitats, mainly geophytes. Group I is also differentiated by bryophytes (D) such as Plagiohilla porelloides, Conocephalum conicum, and Hylocomium splendens, which prefer moist and shady habitats, basic to moderately acidic, mainly on bare soil and rocks. These bryophytes occur predominantly in the Polysticho-Tilietum community.
Group II is characterized by an increased frequency and fidelity index of acidothermophilic species such as Chamaecytisus supinus, Festuca heterophylla, Luzula forsteri, Dianthus barbatus, Veronica officinalis, and Hieracium racemosum, which are sociologically defined as Quercetalia robori-petraeae species. It is also distinguished by thermophilic species identified as Quercetalia pubescentis, including Sorbus torminalis, Fraxinus ornus, Potentilla micrantha, Lathyrus niger, and others. Additionally, Group II features species like Genista tinctoria, Dactylis glomerata, Clinopodium vulgare, Carex hirta, and Galium lucidum, which prefer more light and are characteristic of the classes Trifolio-Geranietea, Molinio-Arhenatheretea, Galio-Urtictea, or Erico-Pinetea. In the tree layer, Group II is further differentiated by the frequency and fidelity values of species such as Quercus petraea and Betula pendula.
Group III differs by only a few species with increased frequency and fidelity indices. Besides Castanea sativa, which has an assigned fidelity index for both Groups II and III, only Luzula pilosa and the moss Dicranella heteromalla have fidelity values assigned exclusively to Group III. Luzula pilosa is an acidophyllic species characteristic of the Vaccinio-Piceetalia order, while Dicranella heteromalla is a very common moss found in a variety of acidic habitats, such as soil, rock, gravel, and tree stumps. Although there are many species with high frequencies linking Groups II and III, the presence of Quercetalia pubescentis species in Group II and these two species in Group III indicates a fine line between thermophilicity and acidophillicity. There is no statistically significant difference in temperature between these two groups, but the Mann–Whitney U test showed a significant difference in soil reaction indicator values.

3.2. Western Balkan Area of Distribution

The analysis of Ellenberg-type indicator values for 1281 relevés within 74 communities from the western part of the silver lime’s natural distribution area revealed different trends from the distribution center toward the western edge (Figure 3, Table S2). Changes can be observed separately for each environmental parameter. The analysis of the soil reaction indicator values showed that closer to the western edge of the area, silver lime occurs mostly in communities with the lowest values, while towards the central part of the area, it is present exclusively in communities with higher values. All analyzed communities of Zrinska Gora fall within the lowest values, while the most basophilic communities were Helleboro-Querco-Ostryetum, Carpineto orientalis-Quercetum, and Celto-Juglandetum in the territory of Serbia [25,47]. The occurrence of silver lime in the south of Hungary (Mecszek Mountains) and the northern and central parts of Bosnia and Herzegovina is particularly interesting. These areas also represent the western part of the range, with a high presence of Tilia tomentosa (>50% relevés) in communities with extremely low, but also high soil reaction indicator values.
When observing the light parameter, the lowest values are found in the far western part of the area, in the north of Bosnia and Herzegovina and central Croatia, because silver lime mainly grows in beech and hornbeam forests there. In the northwest of Serbia, towards the center of the area, the light values increase. The highest values of the moisture indicator are found in the lowland forests in the east of Croatia and the northwest of Hungary. However, silver lime has a lower presence in these communities, being present in less than 50% of relevés, and in some cases, less than 10%.
The analysis of Ellenberg-type indicator values for temperature also indicates a change in habitat conditions of communities with silver lime from the central to the western part of the area. The lowest values are mainly in central Croatia, in communities dominated by beech and hornbeam, while the broad-leaved ravine forests community Polysticho-Tilietum on Zrinska Gora has the absolute lowest values of all 74 analyzed communities. On the other hand, the most thermophilic communities are in Serbia and the north of Bosnia and Herzegovina, mainly in communities of oaks and hornbeams, which also have the highest light values of all compared. Communities in the territory of Serbia with increased values of temperature and light also have the lowest moisture indicator values. Among the lowest values there are also some communities of sedge oak, Turkey oak and manna ash in the lowland belt in eastern Croatia and southern Hungary, where silver lime occurs in less than 50% of relevés. The communities Polysticho-Tilietum, Cephalanthero-Fagetum circetosum lutetianae on Zrinska Gora Mt, and Polysticho setiferi-Aceretum pseudoplatani in southwest Hungary have the highest indicator values for moisture, when only communities where silver lime is present in more than 50% of the relevés are considered. Indicator values for nutrients are the only ones that do not show any geographical consistency.
When observing changes in the environmental parameters of communities according to dominant tree species, some trends can be noticed (Table S2). Within oak-hornbeam communities, there is a slight trend of decreasing indicator values for temperature, light, and soil reaction from the distribution center towards the western edge of the range. Within beech communities, only a decrease in soil reaction is observed towards the west. Specific ranges of ecological indicator values are found within broad-leaved ravine forests, especially in terms of temperature and moisture. The community described as Aceri-Tilietum mixtum in the Dinaric canyons of Bosnia and Herzegovina, with a pronounced Mediterranean influence [48], has the highest values for temperature and the lowest for moisture. In contrast, the Polysticho-Tilietum community on Zrinska Gora Mt has the lowest values for temperature and the highest for moisture. The Polysticho-Tilietum community reaches the absolute minimum indicator value (5.26) of all compared communities in the study area.

4. Discussion

Silver lime, known as a thermophilic species, is unexpectedly abundant in moist and cold ravines and grooves, yet poorly represented in thermophilic forest communities on Zrinska Gora Mt. This habitat shift can be partially explained by soil pH. Namely, acidic soils prevail in the study area, and specific pedogenetic processes have led to the appearance of less acidic soil in ravines and grooves, providing more suitable soil conditions for the silver lime. However, the soil pH of these habitats is still below the lower limit known as adequate for its development [1]. The consequences of this shift caused by soil pH include a move toward cooler, moister habitats with less light. Despite this, silver lime retains its thermophilic character, as evidenced by its presence in the shrub layer of warmer sessile oak communities of Group II, which has the highest number of Quercetalia pubescentis species. Based on this, it can be concluded that such habitats favor the development of young silver lime shrubs, making the plant more viable and competitive. The soil reaction and reduced moisture in these areas impede its further development, as it often achieves higher cover ratings in the shrub and ground layers, but very rarely develops into the tree layer. The possible selection of species by management activities should be taken into account, as these forests are managed according to the principles of classical regular management over large areas.
Species may change their relationship to environmental factors over a wider geographical area, and their ecological optima and ecological gradient amplitudes (e.g., pH) may differ between regions [49]. The ecological response of organisms to different environmental factors varies across a species’ geographical range. These specific plant responses to different habitats, i.e., variations, may be the result of local adaptations to environmental conditions across the species’ geographical range. The differentiation in the realized niche within the same global fundamental niche is the result of processes such as variations in biotic interactions in different parts of the species’ geographical range, species’ dispersal limitation or habitat compensation processes [50,51,52]. There is a wide range of metrics and methods for estimating species’ niche width [53,54,55], each with its own advantages and disadvantages.
It is well known that primary lime forests develop in extreme habitats where other tree species cannot thrive. With the advent of more competitive tree species of semi-shaded and shady forests, lime forests were preserved as relics in steep, dry, rocky, and colluvial habitats [56]. In Southeast Europe, silver lime forms broad-leaved ravine forests with a more or less thermophilic character [5,17,28,29,48,57,58]. Košir et al. [3] conducted phytogeographic differentiation of the broad-leaved ravine forests of Southeast Europe and identified silver lime as a diagnostic species of suballiance Ostryo carpinifoliae-Tilienion platyphylli, which includes the xerothermophilic forests of the Apennines and the Illyrian and Pannonian sectors. In Bosnia and Herzegovina, in the canyons of the Dinarides and the rivers Una, Vrbas, Drina, Bosna, Morača and Neretva, the Aceri-Tilietum mixtum association was described as a relict association of refugial character [48]. Considering the differences in geographical distribution, the author distinguishes two geographical variants: sub-Mediterranean and transcontinental. The transcontinental variant is closest to the association Polysticho-Tilietum due to the reduced content of thermophilic elements. Compared to other silver lime communities in Serbia, Tilio-Faxinetum excelioris [30] stands out with a reduced proportion of thermophilic species.
In the synoptic table (Table 2), Group I does not include any Quercetalia pubescentis species. Therefore, the characterization of silver lime as a xerothermophilic species in the westernmost part of its range, and its sociological affiliation with Quercetalia pubescentis, is questionable. Košir et al. [3] highlighted some open questions regarding the Ostryo carpinifoliae–Tilienion platyphylli suballiance and stated that further research and classification of broad-leaved ravine forests in the Balkans is needed.
During the last interglacial period, the natural range of the silver lime was much wider than it is today. According to Kupryjanowicz et al. [59], the reconstructed range extended about 600 km further to the north, northeast, and west than it does today. Based on the remains of pollen and nuts found in sediments, semi-communities with silver lime were reconstructed. In addition to Tilia tomentosa, the most common remains found in the sediments were of T. cordata and T. platyphyllos followed by Carpinus betulus, Corylus avellana, and Alnus glutinosa, with occasional findings of Acer and Quercus fruits. The closest equivalents to these interglacial communities of all three lime species from the entire present-day natural distribution can only be found in the western part of the range, in the stands of Carpinion betuli [21,60] and in the refugial broad-leaved ravine forests in the canyons of the Dinarides [48]. There is a low presence of Tilia cordata in the forest communities of Zrinska Gora, mostly in Group III communities. Although only silver lime is present in Polysticho-Tilietum, the community can be considered as refugial.
This research expands our knowledge of the ecological amplitude of silver lime. At the westernmost edge of its range, silver lime is either dominant or occurs sporadically in communities of different ecological conditions than previously known. The refugial broad-leaved ravine forest communities have higher indicator values for moisture and lower values for light and temperature compared to other communities with silver lime. Additionally, in the study area, this calcifile species appears in much more acidic soils than previously documented. The Polysticho-Tilietum community is also characterized by lower soil pH than was previously known for silver lime communities. A similar situation regarding soil reaction shift happened in the far eastern part of natural distribution, in Turkey, where peripheral silver lime populations develop in limeless bedrocks and soils. The soil pH changed from 5.6 to 6.6, with a minimum determined pH value of 5.2, and all soils were in the class of medium acidic and mild acidic [61].
The climate of the western border of the silver lime natural distribution area differs from the rest of the area of distribution [62]. According to the Europe Köppen Climate Classification Map, Zrinska Gora represents the western boundary of the Dfb climate, its eastern part has a temperate oceanic climate (Cfb), and the other western part a humid subtropical climate (Cfa). The majority of silver lime natural distribution has a humid boreal climate with warm summers, between 600 and 900 mm of rainfall annually, and the mean temperature of the warmest month is lower than 22 °C (Dfb code). In the central part of the natural distribution, there is a fragment of humid boreal climate with a temperature of the hottest month above 22 °C. According to data from the KNMI Climate Explorer web platform, significant differences in climate are evident in the western Balkans area covered by this study (Table S1). Northern Bosnia and Herzegovina, eastern and northwestern Serbia, eastern and central Croatia, and northern and southern Hungary have a continental precipitation regime with maximum precipitation during the warm part of the year (during the vegetation period) and a minimum during the cold part of the year. However, northern Bosnia and Herzegovina and Zrinska Gora differ with an average annual precipitation of about 1000 mm, while other areas have about 700 mm. In addition, minimum precipitation amounts (about 60 mm in January) and maximum precipitation amounts (about 100 mm in September) are somewhat higher than in the rest of the area. Southern Bosnia and Herzegovina has a maritime precipitation regime with a minimum precipitation during the warm part of the year (vegetation period) and maximum during the cold part of the year. Different climatic conditions, including slightly higher annual precipitation, are factors that likely influenced this ecological behavior and habitat shift. In the context of global warming, it is predicted that the distribution area of the silver lime could change, potentially leading to its ecological integration into the forest landscapes of Central Europe, which are currently dominated by European beech [63]. According to the scenario proposed by Box and Mantley [64], the entire range would shift eastward and slightly northward, from the Balkans to eastern Ukraine and southern Russia. This new understanding of the ecology of silver lime should be integrated into models used in global warming studies.

Methodological Remarks

The ecological amplitude of each species is broader if it occurs in a larger number of communities. Plant communities are restricted to specific habitats characterized by a unique combination of climatic, edaphic, and anthropogenic variables. By comparing the presence of a particular species in different syntaxa within the Braun-Blanquet system [65], one can roughly estimate “species behaviour” in various regions and predict potential shifts in “ecological behaviour”. However, the lack or very small number of relevés in certain parts of the range is a significant limitation of this comparison.
Ellenberg’s indicator values were originally determined for species in Central Europe [66]. The changing relationship of plant species to ecological factors in different regions calls into question the application of Ellenberg indices to other regions [67]. However, some authors confirm the applicability of the original Ellenberg’s indicators [68,69] or their calibration [70,71,72] in other areas of Europe. Ellenberg-type indicator values applicable at the European scale were used [3]. Assuming that the soil reaction is the basic measurable parameter influencing the specific distribution of silver lime in the study area, and considering the question raised about the reliability of Ellenberg indices, soil samples were taken to establish the correlation between Ellenberg-type indicator values and measured soil pH values.
Forest management certainly affects species distribution and floral composition. Research has been conducted in commercial forests that are managed naturally, over large areas, with regeneration under the canopy, in middle-aged and old stands with complete floral composition. Although the relict broad-leaved ravine forests are predominantly of a protective character, and as such should not be managed, according to the management principles of the research area, all observed forest communities are managed in the same way. These peripheral populations, primarily noble broad-leaved ravine habitats, should be treated as protective. As such, they should not be managed at all, or for better conservation, should be managed on a small scale using closer-to-nature and more intensive management methods.

5. Conclusions

This research extends knowledge about the ecology of silver lime. Analysis of Ellenberg-type indices at the western part of the natural distribution revealed a slight trend of decreasing thermophilicity and increasing acidophilicity towards the edge of the distribution area. At the far western point of distribution, the refugial broad-leaved ravine community Polysticho-Tilietum reaches extremely low temperature values compared to other communities, and the pH measured is much lower than the values known as suitable for the development of silver lime. The wider ecological amplitude will certainly have an impact on the adaptation of silver lime to the expected climate changes, which are extremely significant for the area of Southeast Europe.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/f16030438/s1, Table S1: Western Balkan climate data; Table S2: Average Ellenberg-type indicator values and Tilia tomentosa frequency in western Balkan forest communities.

Author Contributions

Conceptualization, I.Š.; methodology, I.Š., A.A., S.M. and J.V.; formal analysis, I.Š., D.B., S.M. and D.U.; investigation, I.Š., I.P., J.V. and A.A.; resources, I.Š., J.V., D.B., D.U. and I.P.; writing—original draft preparation, I.Š.; writing—review and editing, J.V., A.A. and I.P.; visualization, I.Š. and I.P.; supervision, J.V. and D.B. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Data Availability Statement

Data are contained within the article and Supplementary Materials.

Acknowledgments

We thank EVA database custodians who provided data from vegetation plots but did not participate as co-authors: I. Apostolova, G. Bonari, J. Csiky, A. Čarni, R. Ćušterevska, P. Dimopoulos, A. Indreica, M. Krstivojević Ćuk, E. Ruprecht, Ž. Škvorc, I. Tsiripidis, K. Vassilev.

Conflicts of Interest

Joso Vukelić is employed by Oikon Ltd. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript; or in the decision to publish the results.

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Figure 2. Ellenberg-type indicator values Box and whisker for three groups of forest associations on Zrinska Gora Mt regarding presence of silver lime (I > 50%, II < 50%, III = 0).
Figure 2. Ellenberg-type indicator values Box and whisker for three groups of forest associations on Zrinska Gora Mt regarding presence of silver lime (I > 50%, II < 50%, III = 0).
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Forests 16 00438 g003
Figure 3. PCA analysis of Tilia tomentosa communities in the western Balkans with passively projected vectors representing Ellenberg-type ecological indicator values (L—light, T—temperature, M—moisture, pH—soil reaction, N—nutrients); Country codes: CRO—Croatia, HU—Hungary, B&H—Bosnia and Hercegovina, SRB—Serbia; Symbols indicate silver lime presence in communities (▲ > 50%, ∆ < 50%, ⃝ < 10%); Red represents Western Balkan communities, blue represents communities from Zrinska Gora Mt.
Figure 3. PCA analysis of Tilia tomentosa communities in the western Balkans with passively projected vectors representing Ellenberg-type ecological indicator values (L—light, T—temperature, M—moisture, pH—soil reaction, N—nutrients); Country codes: CRO—Croatia, HU—Hungary, B&H—Bosnia and Hercegovina, SRB—Serbia; Symbols indicate silver lime presence in communities (▲ > 50%, ∆ < 50%, ⃝ < 10%); Red represents Western Balkan communities, blue represents communities from Zrinska Gora Mt.
Forests 16 00438 g003
Table 1. Average Ellenberg-type indicator values and Tilia tomentosa frequency in forest communities of Zrinska Gora Mt (L—light, T—temperature, M—moisture, pH—soil reaction, N—nutrients).
Table 1. Average Ellenberg-type indicator values and Tilia tomentosa frequency in forest communities of Zrinska Gora Mt (L—light, T—temperature, M—moisture, pH—soil reaction, N—nutrients).
GroupCommunityNo of RelevésTilia tomentosa Frequency (%)Average Ellenberg-Type Indicator Values
TotalTree LayerShrub LayerLTMpHN
ICephalanthero-Fagetum circetosum lutetianae (Galio-Fagenion)386632 (+–4)66 (+–3)4.805.745.546.225.78
Festuco-Carpinetum (Carpinion betuli)107020 (+–2)70 (+–2)4.785.785.405.965.20
Polysticho-Tilietum (Tilio-Acerion)109090 (1–4)70 (+–1)4.545.265.706.215.87
IIAposeridi-Castaneetum (Aremonio-Fagion)540-40 (+–1)5.785.955.125.854.53
Castaneo-Fagetum (Luzulo-Fagenion)63317 (+)33 (+–1)5.526.285.055.704.49
Cephalanthero-Fagetum typicum (Galio-Fagenion)125025 (+)33 (+)5.105.885.355.945.12
Potentillo-Quercetum (Quercion robori-petraeae)17406 (2)41 (+–2)5.926.214.855.723.91
Pteridio-Betuletum (Quercion robori-petraeae)520-20 (+)6.325.715.535.864.88
IIILuzulo-Fagetum (Luzulo-Fagenion)7---5.485.925.065.203.85
Querco-Castaneetum (Quercion robori-petraeae)6---5.566.265.265.874.81
Table 2. Synoptic table with percentage frequency and modified fidelity phi-coefficient for three groups based on silver lime presence (I > 50%, II < 50%, and III = 0). Layers: A—tree layer; B—shrub layer; C—herb layer; D—bryophytes.
Table 2. Synoptic table with percentage frequency and modified fidelity phi-coefficient for three groups based on silver lime presence (I > 50%, II < 50%, and III = 0). Layers: A—tree layer; B—shrub layer; C—herb layer; D—bryophytes.
Group No. IIIIII
No. of Relevés 584513
Fagetalia sylvaticae
Fagus sylvatica L.(A)1003264---85---
Fagus sylvatica L.(B)973080---62---
Sambucus nigra L. 7654.224---15---
Lamium galeobdolon (L.) Crantz(C)8161.320---15---
Galium odoratum (L.) Scop. 7149.540---.---
Cardamine bulbifera (L.) Crantz 8364.724---8---
Anemone nemorosa L. 38512---.---
Mycelis muralis (L.) Dumort. 5344.324---.---
Symphytum tuberosum L. 4049.84---.---
Actaea spicata L. 5244.67---15---
Pulmonaria officinalis L. 5740.727---8---
Viola reichenbachiana Jord. ex Boreau 533924---8---
Asplenium scolopendrium L. 1932.92---.---
Geranium robertianum L. 3341.17---.---
Carex sylvatica Huds. 6228.733---31---
Brachypodium sylvaticum (Huds.) P. Beauv. 3---2941.3.---
Tilio-Acerion
Ulmus glabra Huds.(A)1633.---.---
Ulmus glabra Huds.(B)2818.52---23---
Polystichum setiferum (Forssk.) Woyn.(C)8862.529---15---
Lunaria rediviva L. 1633.---.---
Aruncus dioicus (Walter) Fernald 1633.---.---
Aremonio-Fagion
Cardamine waldsteinii Dyer(C)3349.5.---.---
Cardamine kitaibelii Bech. 2946.5.---.---
Cardamine trifolia L. 1229.---.---
Adenostyletalia
Athyrium filix-femina (L.) Roth(C)8853.224---38---
Dryopteris filix-mas (L.) Schott 8437.544---46---
Doronicum austriacum Jacq. 2131.44---.---
Galio-Urticetea
Urtica dioica L.(C)2224.14---8---
Alliaria petiolata (M. Bieb.) Cavara et Grande 2838.74---.---
Alnion incanae
Carex pendula Huds.(C)3343.74---.---
Chrysosplenium alternifolium L. 2441.8.---.---
Circaea lutetiana L. 7227.740---46---
Cardamine impatiens L. 1431.---.---
Rubus caesius L. .---1127.7.---
Vaccinio-Picetalia
Oxalis acetosella L.(C)2643.4.---.---
Hieracium murorum L. .---3820.138---
Solidago virgaurea L. 3---2217.615---
Luzula pilosa (L.) Willd. 10---4---4645.4
Quercetalia robori-petraeae
Betula pendula Roth(A)2---1832.3.---
Castanea sativa Mill.(B)12---7118.19248.5
Chamaecytisus supinus (L.) Link .---2240.---
Festuca heterophylla Lam.(C)2---4233.823---
Luzula forsteri (Sm.) DC. 3---4424.538---
Dianthus barbatus L. .---1633.1.---
Veronica officinalis L. 3---2234.5.---
Hieracium racemosum Willd. .---4421.946---
Pteridium aquilinum (L.) Kuhn 38---9127.992---
Quercetalia pubescentis
Tilia tomentosa Moench(A)4042.911---.---
Tilia tomentosa Moench(B)6749.136---.---
Fraxinus ornus L. 16---582254---
Sorbus torminalis (L.) Crantz 7---3613.738---
Potentilla micrantha DC.(C)5---5840.531---
Lathyrus niger (L.) Bernh. ---2442.1.---
Viola alba Besser 3---1829.5.---
Viola hirta L. 14---3334.2.---
Querco-Fagetea
Quercus petraea (Matt.) Liebl.(A)38---8234.754---
Quercus petraea (Matt.) Liebl.(B)7---3333.58---
Moehringia trinervia (L.) Clairv.(C)34482---.---
Cruciata glabra (L.) Ehrend. 5---2223.28---
Galium sylvaticum L. 9---3612.738---
Trifolio-Geranietea
Genista tinctoria L.(B)5---5823.462---
Clinopodium vulgare L.(C).---3138.38---
Hypericum perforatum L. .---1127.7.---
Molinio-Arhenatherretea
Dactylis glomerata L.(C).---2442.1.---
Agrostietea
Carex hirta L.(C).---1633.1.---
Erico-Pinetea
Chamaecytisus hirsutus (L.) Link(B).---1127.7.---
Galium lucidum All.(C).---1633.1.---
Bryophyta
Plagiochila porelloides (Torr. ex Nees) Lindenb.(D)1936.7.---.---
Conocephalum conicum (L.) Dumort. 1633.---.---
Hylocomium splendens (Hedw.) Schimp. 1229.---.---
Dicranella heteromalla (Hedw.) Schimp. 12---24---5436.6
Other species
Populus tremula L.(B).---1330.5.---
Frangula alnus Mill. .---1127.7.---
Stellaria media (L.) Vill.(C)2429.79---.---
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MDPI and ACS Style

Šapić, I.; Vukelić, J.; Alegro, A.; Mikac, S.; Ugarković, D.; Poljak, I.; Baričević, D. Silver Lime (Tilia tomentosa Moench) in Forest Vegetation at the Western Edge of the Natural Distribution. Forests 2025, 16, 438. https://doi.org/10.3390/f16030438

AMA Style

Šapić I, Vukelić J, Alegro A, Mikac S, Ugarković D, Poljak I, Baričević D. Silver Lime (Tilia tomentosa Moench) in Forest Vegetation at the Western Edge of the Natural Distribution. Forests. 2025; 16(3):438. https://doi.org/10.3390/f16030438

Chicago/Turabian Style

Šapić, Irena, Joso Vukelić, Antun Alegro, Stjepan Mikac, Damir Ugarković, Igor Poljak, and Dario Baričević. 2025. "Silver Lime (Tilia tomentosa Moench) in Forest Vegetation at the Western Edge of the Natural Distribution" Forests 16, no. 3: 438. https://doi.org/10.3390/f16030438

APA Style

Šapić, I., Vukelić, J., Alegro, A., Mikac, S., Ugarković, D., Poljak, I., & Baričević, D. (2025). Silver Lime (Tilia tomentosa Moench) in Forest Vegetation at the Western Edge of the Natural Distribution. Forests, 16(3), 438. https://doi.org/10.3390/f16030438

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