The Older, the Richer? A Comparative Study of Tree-Related Microhabitats and Epiphytes on Champion and Planted Mature Oaks

Abstract

The common oak (Quercus robur L.), though ecologically important and long-lived, has declined in Northern Europe due to historical land use and conifer-dominated forestry. In Latvia, where its distribution is limited, oaks support a rich biodiversity through features like tree-related microhabitats (TreMs) and diverse epiphytic communities. This study compared TreM and epiphyte diversity between planted mature oaks and relict champion oak trees across 16 forest stands. Epiphyte species were recorded using fixed-area frames on tree trunks, and TreMs were categorized following a hierarchical typology. Champion trees hosted significantly more TreMs and a greater variety, including 10 unique TreMs. While overall epiphyte diversity indices did not differ significantly, champion trees supported more specialist and woodland key habitat indicator species. The findings underscore the ecological value of legacy trees, which provide complex habitats essential for specialist taxa and indicators of forest continuity. Conserving such trees is vital for maintaining forest biodiversity and supporting ecosystem resilience in managed landscapes.

1. Introduction

The common oak is found in the hemiboreal zone across various forest stand types [1]. The extent of common oak stands in Northern Europe is limited due to modern forest management practices, prioritizing conifer cultivation and converting formerly fertile forested areas into agricultural land [2]. However, oak stands are highly valuable for both forestry and conservation due to their production of high-quality timber and their role in supporting diverse and characteristic biodiversity [3]. Oak species have a naturally long lifespan, ranging from 300 to 900 years, and their wood remains highly durable even during the decay process [4]. Its long lifespan ensures stable habitats, particularly for specialist species [5] and those with limited dispersal potential [3].

Currently, oak is not a commercially significant species in Latvia due to its restricted distribution and the challenges involved in establishing plantations. However, with rising average temperatures and increased precipitation, its commercial importance is expected to increase in the future [6]. Historically, the common oak was widespread in Latvia, but intensive logging and land-use changes have significantly reduced its distribution [7]. According to the 2023 central statistical data from the State Forest Service, the total area of forest land in Latvia dominated by common oak was 9946.51 ha. This represents less than one percent of the country’s total forested area. Notably, there has been a significant increase in private land management over the past decade, indicating a growing interest in cultivating common oak within the private sector [8].

In many countries, the preservation of biodiversity has been established as a key principle and objective of forest policy [9]. A natural common oak forest is expected to feature diverse ecological structures, including old, large trees nearing their maximum age, dead wood, and shade-tolerant species in the understory [5]. A crucial structural feature of natural oak stands is the presence of mature or overmature oaks with rough bark, branched crowns, and diverse microhabitats [3]. Tree-related microhabitats (TreMs) are distinct structural features of trees that provide essential spaces for organisms to live, feed, or find shelter [10]. Their presence can signify habitat naturalness and reflect forest ecological complexity. TreMs play a crucial role in evaluating and supporting species diversity across multiple taxa, making them valuable indicators of biodiversity [11]. In this context, the vital role of oak, particularly ancient oak trees, in supporting groups such as lichens and fungi has gained increasing recognition [12]. With increasing age, its bark undergoes structural and chemical changes, creating suitable conditions for the colonization of rare and specialized lichen species [13], which serve as key indicators of biodiversity, reflecting forest continuity and management practices due to their physiological traits [14]. Age and continuity have a significant influence on the composition of epiphytic communities [15]. Their diversity and abundance are shaped by environmental factors, including light, moisture, and wind, as well as the species and size of host trees [16].

This study aims to explore how different origins and histories of oak trees—specifically, relict champion oaks and planted mature oaks—affect the diversity of TreMs and associated epiphyte communities. Champion oaks, often centuries old and shaped by natural growth processes, are structurally complex and ecologically valuable, potentially supporting a richer and more specialized set of organisms. In contrast, planted oaks are typically younger and more uniform, possibly hosting a different or less diverse set of TreMs and epiphytes. Effective management of mature oak stands requires balancing economic objectives with biodiversity conservation goals, as alternative tree species do not support a substantial proportion of the species that depend on oaks [17]. The primary objective of this study was to assess the differences in TreM diversity and epiphyte communities between champion oak trees and planted mature oak trees. We also aimed to investigate the specific sets of TreMs and epiphytes within each tree group to determine whether they function in a complementary manner, potentially contributing differently to biodiversity in forest landscapes.

2. Materials and Methods

2.1. Study Site Description

To compare epiphyte and TreM biodiversity between planted mature stands and old champion trees preserved as relics, 16 forest stands were selected (Figure 1). The mean annual temperature in the champion tree plots was 5.9 °C, compared to 5.6 °C in the planted stands. In January, the mean temperature was −4.7 °C in the champion tree plots and −5.4 °C in the planted plots. Both types had a mean July temperature of 17.0 °C. The total annual precipitation was 672 mm in the champion plots and 658 mm in the planted plots. In January, the mean total precipitation was 46.2 mm for the champion tree plots and 44.8 mm for the planted plots. In July, the mean total precipitation was 77.5 mm and 74.0 mm, respectively. Champion trees are designated as the tallest or largest-diameter individuals within their respective species. These trees are recognized as notable specimens, with some potentially classified as ancient, veteran, or heritage trees, depending on their age and ecological significance [18]. Previously established sampling plots were used to evaluate relict oaks. Approximately 20 years ago, halo thinning was conducted around half of these champion trees, while the other half served as controls. However, a previous study [19] found no significant differences between treated and control trees; therefore, they were analyzed as a single group. Within each stand, five to eight oak trees were examined, depending on the survival rate of the champion trees. In total, 56 trees across eight forest stands were analyzed, representing remnants of previous forest ecosystems. Not all selected stands were oak-dominated; they varied in age from young to overmature, ranging from 17 to 205 years, with an average stand age of 94 ± 44 years. The forest types where relict oaks were found—Hylocomiosa, Oxalidiosa, and Aegopodiosa—are among the most common in oak-dominated stands in Latvia. Across the country, 52% of these stands occur in Oxalidiosa, 24% in Hylocomiosa, and 18% in Aegopodiosa, with other forest types comprising the remaining 6% [8,20]. For comparison, eight mature planted oak-dominated stands were selected. The selection of planted stands was limited, as oak planting is still not a common practice in Latvia. Measurements were conducted in 23 sampling plots, with the number of plots determined by the size of each forest stand. The selected forest stands ranged in age from 123 to 185 years and belonged to the Oxalidiosa and Aegopodiosa forest types [21].

2.2. Data Collection and Measurements

For relict champion oaks within the stands, a circular sampling plot was set up around each tree (56 in total). In planted oak forests, sampling plots were established to cover the majority of the stand while avoiding canopy openings, wet areas, stand edges, and other atypical sections. Across the entire circular sample plot area (R = 12.62 m), all standing trees were measured (if DBH > 6.0 cm). Tree height (m) was recorded using a Vertex Laser 5 Class 1 altimeter (Haglöf Sweden AB, Långsele, Sweden) (accuracy ±1% of the measured height), while diameter (cm) was measured with a Mantax Blue 500 mm caliper (Haglöf Sweden AB, Långsele, Sweden) (accuracy ±1 mm). The inventory of epiphytic bryophyte and lichen species was conducted on the trunk of each champion oak tree. In planted stands, two to four oak trees closest to the center were assessed, with the sample size varying based on the total number of sampling plots at each location—the greater the number of sample plots, the fewer individual trees assessed per plot. First, the north, west, south, and east sides of the tree were designated. On each side, a 10 cm × 50 cm frame was installed, which was further divided into five 10 cm × 10 cm sections. The shorter side of the frame was attached horizontally to the tree at a height of 1.3 m above the root collar, with the longer side oriented downward. All moss and lichen species within each section were recorded, along with their percentage of coverage. For each tree, data on the occurrence of epiphytic bryophyte and lichen species were collected by evaluating the sample plots established on each side of the tree, resulting in a total of 20 plots, each measuring 10 cm × 10 cm. When bryophyte or lichen species could not be identified in the field, samples were collected for laboratory identification using a light microscope. Some specimens were only identified to the genus level—for example, Lecanora specimens lacking apothecia. However, in most cases, each genus identified represented a single species on a given tree. Lichen species nomenclature follows [20], bryophyte species nomenclature [22]. The evaluation of TreMs was conducted for all the relict champion trees (56 trees) and also all oak trees inside the circular sampling plots in planted stands (756 trees). For the assessment, we used hierarchical typology [10]. Microhabitats were divided into seven forms: (1) cavities, (2) tree injuries and exposed wood, (3) crown deadwood, (4) excrescences, (5) fruiting bodies of saproxylic fungi and fungi-like organisms, (6) epiphytic and epixylic structures, and (7) exudates. Each of the forms was divided into groups, a total of 15 groups, which were further divided into types of microhabitats—a total of 47. The presence or absence of observed microhabitats, as well as bryophyte and lichen species, was recorded for each analyzed tree during the leafless period in 2023.

To ensure that the two forest stand types were subject to comparable macroclimatic conditions, climatic data were analyzed. For each plot, data were obtained from the nearest point in a gridded dataset. Using the CRU TS 4.09 dataset [23], mean values were calculated across the entire available time frame for each forest type (champion and planted). First, the data for each plot were obtained. The variables included mean annual temperature, mean January temperature, mean July temperature, mean annual precipitation, and mean total precipitation for January and July.

2.3. Data Analysis

A linear mixed-effects model (using the lmer and lmerTest packages) [24] was used to compare the oak height and diameter among the two stand types [25]. Plot identification and location were included as random effects. For each tree selected for epiphyte assessment, the average cover for each epiphyte species was calculated. First, average coverage values for each cardinal direction were determined, and then an overall average was calculated for all directions of the tree. Species diversity indices were computed using the Shannon–Wiener [26] and Simpson index [27], and the total number of species present was recorded. Detrended correspondence analysis (DCA) was performed using the package vegan to assess patterns in species composition between planted and champion trees [28]. The total number of microhabitats was calculated for each tree. A Poisson generalized linear mixed-effects model (GLMM) was employed to assess whether the type of oak—champion or from mature planted forest—affects the total number of microhabitats [25]. A binary logistic GLMM was applied to examine the effect of oak type on the likelihood that a tree would have a particular microhabitat type. In both models, the plot identification was included as a random factor, as multiple plots were established at each location. To assess the significance of differences in the total number of microhabitats between forest stands, a Chi-square (χ²) test was used [29]. A proportion test was conducted to compare the proportions of unique and shared epiphyte species and TreMs. A t-test was then conducted to compare meteorological condition values between the two forest types and assess whether any significant differences existed. All statistical tests were performed with a significance level of p < 0.05, and all analyses were performed using R version 4.4.2 [30].

3. Results and Discussion

3.1. Stand Characteristics

The mean tree diameter was 31.1 ± 2.0 cm in champion tree plots and 26.0 ± 2.8 cm in planted mature stands. Tree height followed a similar trend, averaging 23.7 ± 1.6 m and 21.6 ± 2.2 m, respectively. Stands with relict champion trees exhibited greater overall structural heterogeneity, which is an essential driver of forest species richness as well as the regulation of microclimate [31]. The average tree diameter per plot ranged from 19.58 cm to 37.72 cm, while tree height varied from 12.69 m to 26.96 m. In contrast, planted oak stands were more uniform, with diameters ranging from 21.26 cm to 35.20 cm and heights from 16.34 m to 27.22 m. However, the two types had no statistically significant differences in diameter or height (p > 0.05). The average total stand basal area was 24.0 ± 9 m² ha¹ in champion tree plots and 28.6 ± 5 m² ha¹ in planted stands. No statistically significant differences were found in any of the meteorological variables between the two forest stand types. This includes mean annual temperature (p = 0.11), January temperature (p = 0.09), July temperature (p = 0.33), annual precipitation (p = 0.16), January precipitation (p = 0.38), and July precipitation (p = 0.23).

3.2. TreMs

Statistically significant differences (p < 0.0001) were found in the number of tree-related microhabitats between the two stand types. Champion trees had a significantly higher mean number of TreMs (4.16 ± 0.4) compared to the planted mature oak stands (1.53 ± 0.2). In terms of richness, champion trees supported 23 distinct TreM types, whereas planted stands hosted only 14 (Figure 2A). The diversity of microhabitats on trees increases ecological niches, thereby promoting species richness across multiple taxonomic groups, including bryophytes and lichens [10]. Other studies show that managed forest stands typically have lower TreM densities [32] and reduced structural diversity. Despite some champion trees having undergone halo thinning, the biological legacies preserved within these stands help maintain structural complexity, which in turn accelerates the recovery and development of TreMs [33]. Champion trees most frequently had three TreMs per tree, whereas planted trees typically had only one (Figure 3B). In planted mature stands, only one unique TreM type was identified (large woodpecker breeding cavity), while 13 TreM types were shared with the champion trees (Figure 2A). The presence of large woodpecker breeding cavities is particularly significant, as these structures serve as essential nesting and shelter sites for a wide range of secondary cavity-nesting species. Consequently, they have a direct and positive influence on the abundance and diversity of associated fauna [34]. In contrast, champion oaks contained 10 unique types of TreMs, a statistically significant difference (p = 0.04). Some of these unique TreMs are functionally interconnected—for instance, fork splits and dendrotelms often co-occur, as the formation of large forks promotes the development of water-filled tree cavities (dendrotelms) [35]. Other unique TreMs found in champion trees are the result of mechanical damage, such as bark pockets, cracks, and limb breakage. These features can accelerate wood decay processes, thereby facilitating the formation of additional microhabitats such as semi-open trunk rot holes and the presence of pulpy agaric fungi. Additional TreMs exclusive to champion trees include burrs, sap runs, and foliose and fruticose lichens. The occurrence of these lichens is likely linked to the deeply fissured bark of older trees, which creates a more humid and stable microhabitat. Such conditions favour the establishment and dominance of large foliose species that can outcompete smaller epiphytes by occupying the majority of the available surface area [16]. Several of these TreMs are particularly important for invertebrates. For example, sap runs provide a highly specialized microhabitat that supports sap-feeding and mycophagous beetle species [36] while pulpy agaric fungi serve exclusively as a food resource due to their rapid decomposition, which precludes use as larval habitat [37]. When the occurrence of TreM types was compared between the two forest types, it was found that several TreMs were significantly more likely to occur in champion tree stands than in planted stands (Figure 3A). These included dead branches, trunk rot holes, bryophytes, stem breakage, perennial polypores, annual polypores, remaining broken limbs, vertebrate nests, and trunk base rot holes (p < 0.05). These TreMs are of particular importance, as the highest diversity of oak-associated species has been recorded on oak bark, followed by dead wood and branches, including both limbs and twigs [17]. In planted mature oak stands, the occurrence of dead tops was higher, although this difference was not statistically significant. No significant differences were observed in the occurrence of epicormic shoots, bark loss, or bark shelters. For other TreM types, comparison was not possible as they were absent in planted stands. These findings highlight the importance of conserving mature, structurally complex oak trees—particularly relict champion oaks—as they offer a greater diversity and uniqueness of TreMs. From a forest management perspective, this highlights the need to integrate biodiversity considerations into planning, especially when replacing or supplementing oak stands with alternative species that may lack comparable ecological value. Given that TreMs support a wide range of organism groups, including epiphytes, and can serve as effective indicators of overall forest biodiversity [38], their preservation is crucial for maintaining ecological integrity in forest landscapes.

3.3. Epiphytes

A total of 68 epiphyte species were recorded on the champion trees, compared to 36 species on the planted stand oaks. Only 45.7% of the species were shared between both types (Figure 2A,B); however, this difference was not statistically significant (p = 0.6637). The higher proportion of the species was supported by the champion trees (48.6%), while the unique species for planted trees was low (5.7%). Champion and planted trees hosted a similar average number of epiphyte species, with eight and nine species per tree, respectively (Figure 3D), and these differences were not statistically significant. The four unique species found on planted trees included Bryoria sp., Chaenotheca chlorella (Ach.), Lecidella elaeochroma (Ach.), and Mycocalicium subtile (Pers.). Hair lichens of the genus Bryoria increase in abundance with greater canopy openness, likely due to their sensitivity to prolonged wetting in less ventilated conditions [39]. They can colonize suitable forests as young as 60 years [40]. The lower number of unique epiphytic species observed on planted oaks may be attributed to their less fissured bark, which provides less structural complexity and retains less moisture. As a result, epiphytes are likely subjected to more stressful conditions, including increased exposure to desiccation [16]. The shared component of the epiphyte species composition included Chaenotheca brachypoda (Ach.), Buellia griseovirens (Turner), and Plagiothecium laetum (Schimp.). Many species of Lepraria are widely distributed [41], similar to Buellia griseovirens. Although Buellia griseovirens has been reported to be absent on the smoother bark of younger trees [42], this pattern was not observed in our study. This discrepancy may be attributed to the fact that the managed, mature oaks in our sample already possessed relatively fissured bark. The most abundant epiphyte species in both stand types were Hypnum cupressiforme (Hedw.) and Lepraria sp., (Figure 3C), similar to studies in the United Kingdom [42], Ukraine [43] and Croatia [44]. Generalist species assessed include Amandinea punctata (Hoffm.), Bacidia sp., Physcia sp., and Xanthoria sp.—species that are often found in disturbed areas or across a variety of substrates [45]. Additionally, bryophytes such as Brachythecium rutabulum (Hedw.), Brachythecium salebrosum (Hoffm.), and Plagiomnium cuspidatum (Hedw.) are highly adaptable to different substrates [46]. Other species, such as Lecanora sp., Peltigera sp., and Riccardia sp., are characterized by broad ecological amplitudes and can thrive in diverse environments [46]. Species classified as generalists—characterized by broad ecological niches—are expected to occupy a greater number of habitat patches across the landscape than specialists, which are limited by narrower ecological requirements [47]. The unique species associated with champion trees include a range of specialist lichens, such as Acrocordia gemmata (Ach.) (an obligate epiphyte typically found in old-growth forests), Arthonia byssacea (Weigel) (commonly an epiphyte on old bark, demonstrating specialist tendencies), Calicium sp. (which includes various obligate epiphytic specialists, often serving as indicators of forest continuity), and several species within the genus Chaenotheca: Chaenotheca brachypoda (Ach.), Chaenotheca chrysocephala (Turner), and Chaenotheca trichialis (Ach.) [48,49]. Other notable specialists include Lecanactis abietina (Ach.), an indicator of old-growth and undisturbed forests, and Sclerophora sp., which are rare and linked with ancient trees and stable ecological conditions [50,51]. The greater number of unique species observed may be attributed to the coarse bark structure characteristic of champion oak trees, along with other tree traits associated with advanced age [4,52]. This may also be attributed to the larger size of the trees, which offer an increased surface area for colonization, as well as to the greater age of the trees, which allows for extended periods of establishment and growth [16]. Although the epiphyte species were assessed exclusively on champion trees, the forest structure in these stands is more heterogeneous, and the mixture of tree ages promotes colonization and ensures long-term substrate availability without temporal discontinuities [53].

Some epiphyte species were restricted to specific locations. Isothecium alopecuroides (Lam.) was observed on two trees at one site (champion trees). This species thrives in shady chasmophytic habitats, characterized by a narrow range of environmental conditions, typical of stenotopic species [54]. An exception was Anomodon longifolius (Schleich.), which covered the entire west side of a tree trunk (champion tree). The distribution of this species is shaped by microclimatic factors such as light availability, air humidity, and temperature. Structural components that alter the microclimate, such as canopy openness, the presence of a shrub layer, and vertical stratification of the canopy, play a critical role in influencing epiphytic communities [55] as well as habitat connectivity [56]. Along with Isothecium alopecuroides and Metzgeria furcata (L.), Anomodon longifolius was a woodland key habitat indicator species [57] observed exclusively on champion trees. In contrast, Neckera pennata (Hedw.) and Homalia trichomanoides (Sw.)—woodland key habitat indicator species—were found in both stand types. Similarly, seven lichen species identified as woodland key habitat indicators were detected in this study. Part of these species (Acrocordia gemmata (Huds.), Lecanactis abietina (Pers.), Arthonia byssacea (Ach.) were found exclusively on champion trees. These crustose lichen species exhibit a preference for humid, shaded environments [58]. Consequently, their occurrence may be associated with the deeply fissured bark of champion trees, which helps maintain elevated moisture levels and provides a suitable microhabitat [16]. Epiphyte occurrence is often related to tree characteristics such as architecture, bark structure, and the chemical composition of both bark and foliage. These factors influence microclimatic conditions, nutrient availability, and substrate stability [59]. Oak density is the primary factor influencing both the presence and diversity of red-listed lichens on oak trees [13]. There were no statistically significant differences in the Shannon–Wiener index for epiphytes between the two stand types (p = 0.79). The mean Shannon–Wiener index was 1.30 ± 0.01 for champion trees and 1.27 ± 0.10 for planted mature stands. Similarly, the Simpson index showed no significant difference (p = 0.67), with mean values of 0.63 ± 0.02 for champion trees and 0.61 ± 0.03 for planted trees. Although high proportions of the species are shared between the two forest stand types, the champion trees hosting specialist species are irreplaceable, also concluded in other studies [17]. These results underscore the importance of relict champion trees as providers of woodland key habitat and specially protected species. However, their value is likely not due to age and structural characteristics alone, but also to the specific conditions they create, such as humidity and light availability, as well as the ecological context of the surrounding forest stand.

Based on our findings, relict champion oaks play an important role in maintaining TreM diversity and supporting rich epiphyte communities. These trees should therefore be recognized not only as biologically valuable individuals but also as structural keystones within forest ecosystems. Forest management strategies should prioritize the protection of existing champion oaks and aim to extend the presence of structurally diverse trees within both natural and managed stands. Integrating such biodiversity-focused practices into oak forest management can enhance habitat quality and ensure the conservation of specialized species associated with champion trees.

4. Conclusions

The findings underscore the ecological importance of champion trees in supporting biodiversity within forest ecosystems. These trees harbour a significantly greater abundance and richness of TreMs and sustain a wider range of specialist and rare epiphyte species, many of which are indicators of ecological continuity and forest maturity. Although our results indicate a strong link between champion oaks and increased TreM and epiphyte diversity, we acknowledge that this pattern may be influenced by both the inherent characteristics of the tree and external environmental conditions. Oak planting can promote biodiversity, yet these trees reach their full ecological potential only when allowed to attain their maximum age. Although planted oak stands enhance forest structure, the diversity and uniqueness of species and TreMs they support are markedly lower than those found in champion trees. The presence of unique microhabitats and specialist species associated with champion trees highlights their irreplaceable role in maintaining structural heterogeneity. Conserving these legacy trees should therefore be prioritized in forest management strategies that aim to enhance biodiversity and ecosystem resilience.