Biodiversity and Conservation

, 18:105

Tree and stand level variables influencing diversity of lichens on temperate broad-leaved trees in boreo-nemoral floodplain forests

Authors

    • Institute of Ecology and Earth SciencesUniversity of Tartu
  • Jaan Liira
    • Institute of Ecology and Earth SciencesUniversity of Tartu
  • Jaanus Paal
    • Institute of Ecology and Earth SciencesUniversity of Tartu
  • Ave Suija
    • Natural History Museum of the University of Tartu
Original Paper

DOI: 10.1007/s10531-008-9460-y

Cite this article as:
Jüriado, I., Liira, J., Paal, J. et al. Biodivers Conserv (2009) 18: 105. doi:10.1007/s10531-008-9460-y

Abstract

Tree and stand level variables affecting the species richness, cover and composition of epiphytic lichens on temperate broad-leaved trees (Fraxinus excelsior, Quercus robur, Tilia cordata, Ulmus glabra, and U. laevis) were analysed in floodplain forest stands in Estonia. The effect of tree species, substrate characteristics, and stand and regional variables were tested by partial canonical correspondence analysis (pCCA) and by general linear mixed models (GLMM). The most pronounced factors affecting the species richness, cover and composition of epiphytic lichens are acidity of tree bark, bryophyte cover and circumference of tree stems. Stand level characteristics have less effects on the species richness of epiphytic lichens, however, lichen cover and composition was influenced by stand age and light availability. The boreo-nemoral floodplain forests represent valuable habitats for epiphytic lichens. As substrate-related factors influence the species diversity of lichens on temperate broad-leaved trees differently, it is important to consider the effect of each tree species in biodiversity and conservation studies of lichens.

Keywords

Bark pHBryophytesCircumferenceEpiphytesFloodplain forestSpecies richnessStand ageTemperate broad-leaved trees

Introduction

Epiphytic lichens represent an important component of the forest ecosystem and have proved to be sensible indicators of its functions (Will-Wolf et al. 2002), therefore, the lichen communities on deciduous and coniferous trees are intensively studied in regions of temperate and boreal forests (Culberson 1955; Barkman 1958; Yarraton 1972; Kuusinen 1996; Jüriado et al. 2003).

The processes underlying the formation of the epiphytic lichen communities are complex, as environmental factors at the tree and stand levels are inter-correlated (McCune 1993; Giordani 2006; Ellis and Coppins 2006, 2007a). At the tree level, occurrence of lichen species on trees depends first of all on the physical and chemical properties of the bark (Barkman 1958; Brodo 1973). The most highlighted physical characteristics of the substrate influencing the composition of epiphytic lichens are the roughness, thickness, hardness and water-holding capacity of bark (Culberson 1955; Mistry and Berardi 2005). From the chemical properties of the bark, bark acidity is considered to have the highest influence on the composition of lichen species (Bates and Brown 1981; Kuusinen 1996; Löbel et al. 2006). The identity of the tree species has been suggested as less important, mostly considering the fact that bark pH varies largely within tree species along the environmental gradients (Farmer et al. 1991; Gustafsson and Eriksson 1995). The composition of lichens and the effect of the bryophyte cover on epiphytic lichens depend also on the age, size, inclination and exposition of phorophytes (Sõmermaa 1972; Kantvilas and Jarman 2004; Belinchón et al. 2007; Johansson et al. 2007; Ranius et al. 2008).

Succession of lichen species on trees is induced both by tree and stand level effects: a change in the physical and chemical properties of the bark with tree ageing and a change in microclimatic conditions within a stand during its ageing cause the turnover of lichen species (Yarraton 1972; McCune 1993; Ellis and Coppins 2006). Therefore, in addition to stand age and historical continuity (Boudreault et al. 2000; Price and Hochachka 2001; Jüriado et al. 2003; Ellis and Coppins 2007a), stand moisture regime and habitat light availability can be considered the most influential factors for epiphytes at the stand level (Brodo 1961; McCune 1993; Burgaz et al. 1994). Soil nutritional conditions determine the diversity of lichens mainly indirectly, via the composition of tree species in a stand (Oksanen 1988; Jüriado et al. 2003).

The conditions in a forest stand are also influenced by large-scale processes such as air pollution and climate change (Hawksworth 2002; Insarov and Schroeter 2002). In addition, forest management severely affects the stand environment and communities of forest lichens (Aude and Poulsen 2000; Price and Hochachka 2001; Pykälä 2004). As the relative importance of local- and large-scale factors structuring the lichen communities on trees varies among geographical regions (McCune et al. 1997; Jovan and McCune 2004; Will-Wolf et al. 2006; Liira et al. 2007) and among forest types (Meier et al. 2005; Jüriado 2007), the respective studies can never be exhaustive.

In boreo-nemoral zone of Europe, man has had a tremendous impact on the tree species composition and structure of deciduous forests (Diekmann 1994). The modern forest stand has undergone homogenisation, simplification and fragmentation (Axelsson and Östlund 2001; Brown and Cook 2006). Among the other forest types, the area of floodplain forests frequently dominated by temperate broad-leaved trees (e.g. Acer platanoides, Fraxinus excelsior, Tilia cordata and Ulmus glabra) has decreased; the stands have been fragmented and heavily impacted by watercourse regulations, timber harvesting and other anthropogenic activities (Nilsson 1992a; Klimo and Hager 2001; Paal et al. 2007). Remaining stands represent part of the European natural heritage, and according to the Habitat Directive (EC 1992), floodplain forests belong to the habitats of great importance in nature protection.

In Estonia, floodplain forests are among main habitats for temperate broad-leaved trees (Paal et al. 2007). As considerable part of red-listed epiphytes in the boreal region depends on broad-leaved trees (Thor 1998; Berg et al. 2002), it is important to understand the processes influencing the species richness and composition on these tree species.

Due to the deficiency of comparative investigations of lichen species occurring on temperate broad-leaved trees in sub-natural forest (e.g. Löbel et al. 2006), the aim of the current study was to estimate the relative role of substrate properties and stand variables on the species richness and cover and composition of epiphytic lichens on five common temperate broad-leaved tree species. We tested whether the environmental factors affect the richness of lichen species uniformly for all tree species, i.e. if temperate broad-leaved tree species could be considered a homogenous group in biodiversity and conservation studies.

Materials and methods

Study sites and environmental variables

Estonia is located in the hemiboreal subzone of the boreal forest zone, i.e. in the transitional area where the southern boreal forest subzone changes into the spruce-hardwood subzone (Laasimer and Masing 1995). Floodplain forests with temperate broad-leaved tree species were chosen for the study of epiphytic lichen species communities on common ash (Fraxinus excelsior L.), common oak (Quercus robur L.), small-leaved lime (Tilia cordata Mill.), wych elm (Ulmus glabra Huds.) and spreading elm (Ulmus laevis Pall.). Floodplain forests are transitional habitats between terrestrial and aquatic ecosystems where the water table is usually at or near the surface and the land is covered periodically or at least occasionally by shallow water (Hager and Schume 2001). These forests are characterized by high species diversity (Paal et al. 2006, 2007), as well by high density and productivity of tree species (Nilsson 1992a; Mitsch and Gosselink 2000).

Field data were collected in 2002 as part of a project aimed to describe the typology and soils of Estonian floodplain forests (Paal et al. 2007). Sixteen stands scattered all over the distribution area of floodplain forests in Estonia were selected for lichenological study. The studied forests located in a continuous forest landscape near Laiksaare in southwestern Estonia (two stands between 58°05–07′ N and 24°38–41′ E, 25 sample trees), in the Soomaa National Park in central Estonia (six stands between 58°22–27′ N and 25°00–05′ E, 51 sample trees) and in the Alam-Pedja Nature Reserve in eastern Estonia (eight stands between 58°25–32′ N, and 26°09–17′ E, 52 sample trees). In Soomaa and Alam-Pedja, lichen communities on all five tree species were studied, while in Laiksaare only three tree species (Fraxinus excelsior, Tilia cordata and Ulmus glabra) were available for study. In every forest stand, five or six trees (with a diameter at least 20 cm) from each tree species were sampled. The circumference of each sample tree was measured at breast height (1.3 m above ground level) and the percentage of canopy cover was estimated near each sample tree (Appendix 1). Data about stand age (age of the oldest trees in the stand) was obtained from the State Forest Survey Database. The composition of the plant species of the tree and herb layers, and the mean basal area of the trees were described in a round 0.1 ha sampling area (Paal et al. 2007). For each sampling area, habitat light availability, and stand soil moisture and fertility conditions were evaluated using the weighted averaging algorithm and ecological indicator values of the herbaceous plant species (Ellenberg 1979).

Lichen sampling

We sampled epiphytic lichen communities on tree trunks using a 20 × 20 cm sample plot, setting the quadrat on the northern and the southern sides of the tree trunk, at a height of 1.3 m above ground level. To estimate the cover percentage of lichen species and the total cover of bryophytes, the sample plot was divided into 100 subplots. The specimens which we could not identify in the field were collected for laboratory identification. For identification of lichens in the laboratory, the stereomicroscope, the light microscope, ‘spot tests’, UV light and standardized thin-layer chromatography (TLC) were used. Owing to their difficult taxonomy, species of Arthopyrenia, small specimens of Lepraria and minute squamules of Cladonia were treated at the generic level. Melanelia spp. included tiny, unidentified specimens of either M. subaurifera or M. fuliginosa. Collective taxa (spp.) were excluded from the species list of a sample plot if any of the possible species within the genus were also found in the same plot. Reference materials are deposited in the lichen herbarium at the Natural History Museum of the University of Tartu (TU). Data about the species frequency in Estonia are derived from Randlane and Saag (1999) and updated according to the Database of Estonian lichens (eSamba). The list of protected lichen species is presented according to the official decrees (Keskkonnaministri määrus nr 51 2004; Vabariigi Valitsuse määrus nr 195 2004) and the red-listed lichen species are according to Randlane et al. (2008).

Measurement of bark pH

For measurement of pH of bark surface, two small samples of bark (ca. 1.5 cm2) were cut with a knife within each 20 × 20 cm sample plot on both sides of the tree trunk. Bark samples were air dried and stored in paper bags until laboratory analysis. To measure bark pH, a flathead electrode (Consort C532) was used applying a slightly modified technique suggested by Schmidt et al. (2001) and Kricke (2002). Of a solvent (0.01 M KCl), 0.5 ml was dropped in a small Petri dish and a bark sample was placed into the solvent with the outer surface downward to soak only its uppermost part. After a minute of floating, the bark sample was removed and the solvent was slightly shaken off. Then the flathead electrode was pressed against the bark, and the bark pH value was measured during 3 min. In statistical analyses the mean pH of two bark samples from one sample plot was calculated.

Statistical analyses

We used a non-parametric statistical method of the Multi-Response Permutation Procedure (MRPP; Mielke 1984), with a Euclidean distance, implemented in the program PC-ORD ver. 5 (McCune and Mefford 1999), to test differences in species composition among the regions, the tree species and the two side aspects of trees. The species occurring in 1–2 sample plots (1% of all plots) were removed from the data set. In MRPP tests the confounding effects of other factors were taken into account by using the data set of the residuals of the cover values produced with ANOVA models (implemented in the program package Statistica 7.1; StatSoft Inc 2005). For example, to test differences in species composition among the regions, the residuals of the ANOVA model, where the factor ‘Tree species’ was treated as the predictor variable, were used. For testing differences in species composition among the tree species, the factor ‘Region’ was applied as the predictor variable in ANOVA. In the MRPP test for the effect of the tree aspect on lichen composition, the residuals from ANOVA with the factors ‘Tree species’ and ‘Region’ as the predictor variables, were used. MRPP analysis yields an A-statistic, which is a descriptor of within-group homogeneity compared to random expectation (McCune and Mefford 1999).

We employed partial canonical correspondence analysis (pCCA) (ter Braak 1988) implemented in CANOCO ver. 4.5 (ter Braak and Šmilauer 2002) in order to examine relationships between species composition and the environmental variables. Variance in the composition of the epiphytic community, caused by the geographical location of the stands, was taken into account by setting geographical coordinates (continuous variables ‘Latitude’ and ‘Longitude’) as the covariables. The species occurring in 1–2 sample plots were removed from the data set prior to ordination. The forward selection procedure with randomization tests (Monte-Carlo permutation test, 1,000 unrestricted permutations) was used to select the most important environmental variables influencing species composition, retaining the variables with an independent significant contribution at the P < 0.05 level. The Monte-Carlo permutation test was also used to determine the statistical significance of the first and hereafter all canonical axes together. In the final model, all inflation factors were less than five, i.e. far below the suggested limit value of 20 (ter Braak and Šmilauer 2002).

We tested the response of species richness and cover of epiphytic lichens to the influence of the environmental variables using a general linear mixed model (GLMM; Littell et al. 1996) with the stepwise selection procedure, implemented in the program package SAS ver. 8.2 (proc MIXED, SAS Institute Inc. 1989). The categorical factors ‘Region’ and ‘Site’ nested in ‘Region’ were considered random factors and the sample plots on the northern and southern sides of a tree trunk (factor ‘Tree aspect’) were treated as repeated observations per sample tree. In the model, we also tested the interactions between the factor ‘Tree species’ and the continuous factors ‘Bryophyte cover’, ‘Circumference’ and ‘Bark pH’. We tested also non-linear relationships but as they were not significant, only a linear model is presented. For multiple comparisons between the tree species the Tukey-Kramer adjustment was used. Akaike’s information criterion (AIC; Akaike 1973) and the significance test of factors were used to identify optimal parameterisation of the models (Shao 1997). GLMM analysis was also applied to evaluate the influence of ‘Bryophyte cover’, ‘Circumference’ and tree species on bark pH using the same model settings as in the models described above.

In all statistical analyses, the cover values of lichens and bryophytes were square-root transformed (ter Braak and Šmilauer 2002), and the number of lichen species and variable ‘Circumference’ were log-transformed.

Results

Bark pH of temperate broad-leaved trees

The values of bark pH varied significantly between the tree species. The bark of Tiliacordata and Quercusrobur was more acid (mean pH = 4.58 ± 0.11 and 4.51 ± 0.15, respectively) than the bark of the other broad-leaved tree species (mean pH for Ulmus glabra, Fraxinus excelsior and Ulmus laevis being 4.96 ± 0.11, 5.11 ± 0.09 and 5.13 ± 0.11, respectively, Table 1). We observed also overall positive relationship between bark pH and cover of bryophytes, and tree-specific effects of tree circumference (Table 1), i.e. bark pH increased significantly with tree circumference for Fraxinus excelsior, Ulmus glabra and U. laevis.
Table 1

The results of general linear mixed model analysis (GLMM) for bark pH

Effect

df

P

Mean (±SE)

Slope

Tree species

4; 244

0.045

  

    Fraxinus excelsior

  

5.11 ± 0.09a

 

    Quercus robur

  

4.51 ± 0.15b

 

    Tilia cordata

  

4.58 ± 0.11b

 

    Ulmus glabra

  

4.96 ± 0.11a

 

    Ulmus laevis

  

5.13 ± 0.11a

 

Bryophyte cover

1; 244

<0.0001

 

0.044***

Bryophyte cover × Tree species

4; 244

0.977

  

Circumference

1; 244

<0.0001

  

Circumference × Tree species

4; 244

0.007

  

    Fraxinus excelsior

 

<0.0001

 

1.762***

    Quercus robur

 

0.660

 

−0.191

    Tilia cordata

 

0.360

 

0.441

    Ulmus glabra

 

0.008

 

1.285**

    Ulmus laevis

 

0.001

 

1.948**

Slope estimates are presented for continuous variables; within-group mean values are presented for categorical variables, letter labels denote homogeneity groups according to the results of Tukey-Kramer multiple comparison test. The significance test for the slope estimates different from zero: ** P < 0.01, *** P < 0.0001

Species composition of lichen communities

We found 104 corticolous lichen species on five broad-leaved tree species (Appendix 2). The highest number of lichens was recorded on Fraxinusexcelsior, 70 species; Ulmus laevis hosted 50 species, Quercus robur and Tilia cordata 49 species, and Ulmus glabra 45 species. Most of these lichen species are common in the Estonian lichen flora, except for six lichen species, which are considered rare having less than ten localities across the country (Appendix 2). From the total species list, seven lichen species belong to protected or red-listed species in Estonia (Appendix 2).

According to MRPP tests, there were significant differences in the lichen flora among all regions (A = 0.022, P < 0.0001) and among the pairs in different regions (P < 0.0001); as well as among all tree species (= 0.048, P < 0.0001) and among the pairs of the tree species (P < 0.01). Therefore, to reveal more specifically the effect of the substrate and site factors on the lichen community, regional parameters were used as the covariables in pCCA ordination. The eigenvalue of the first ordination axis was 0.35, of the second axis 0.26 and of the third axis 0.23. The first three axes described 55.2% of variation in the species–environment relationship. The Monte-Carlo permutation test confirmed that the relationship between the species data and the ordination axes is highly significant (P = 0.001). The variation patterns of the lichen assemblages on the trees can be largely explained by the host tree species, substrate related factors and stand age. Most of the environmental variables describing the site conditions of a stand gave a very low contribution to ordination results and were neglected from the analysis.

The gradient directed along the first ordination axis is mainly related to bark pH: the elm trees (Ulmus glabra and U. laevis) with a high cover of bryophytes show the strongest positive correlation with the first ordination axis while big oak trees in old stands with good light conditions are negatively correlated with the first axis (Fig. 1). Tree species with high bark pH (Ulmus glabra and U. laevis) have the most similar lichen flora in contrast with trees with a more acid bark (Quercus robur and Tilia cordata). The second axis reflects the gradient associated with tree circumference and with the cover of bryophytes; big mossy elm trees (Ulmus laevis) in stands of high soil fertility contrast with smaller ash and lime trees with a low cover of bryophytes on the tree trunk. Variation along the third axis revealed the difference between the lichen assemblages occurring on trunks of those lime and ash trees, which have low cover of bryophytes (not shown).
https://static-content.springer.com/image/art%3A10.1007%2Fs10531-008-9460-y/MediaObjects/10531_2008_9460_Fig1_HTML.gif
Fig. 1

Lichen species and the environmental variables on the biplot of partial canonical correspondence analysis (pCCA) of the first and the second axes. The tree species (dummy variables) are represented by their centroids (Fra exc, Fraxinus excelsior; Que rob, Quercus robur; Til cor, Tilia cordata; Ulm gla, Ulmus glabra; Ulm lae, Ulmus laevis). Bry cover, cover of bryophytes in a sample plot on the bole; Circumference, circumference of a sample tree; Light, habitat lightness; Soil fert, soil fertility; Tree sp no, number of tree species in a stand. For abbreviations of lichen species see Appendix 2

The variable ‘Tree aspect’ (location of sample plots on the northern or southern side of the tree trunk) was insignificant in pCCA ordination, although in the MRPP test where the effects of ‘Region’ and ‘Tree species’ were taken into account, a significant difference was revealed between the lichen communities on northern and southern sides of the trees (A = 0.001, P = 0.028).

According to the ordination scores of the lichen species, the lichens associated with the trees with the acid bark and with a low cover of bryophytes are located in the negative side of the first axis (e.g. Evernia prunastri, Hypogymnia physodes and Pertusaria amara) (Fig. 1). In the upper positive side of the biplot are the lichens associated with the trees with the subneutral bark (e.g. Phaeophyscia orbicularis) or with the high cover of bryophytes on the tree bole (e.g. Bacidia subincompta, Biatoridium monasteriense and Mycobilimbia epixanthoides). In the upper left part of the biplot are the species restricted mainly to large trees (e.g. Arthonia byssacea, Opegrapha varia and Pertusaria flavida), while the species preferring younger trees (e.g. Arthonia radiata, Pertusaria leioplaca and Phlyctis agelaea) are on the lower side of the biplot (Fig. 1).

Species richness and cover of lichens

In the stepwise building of the general linear model, most of the variables characterizing the general ecological conditions of a stand (Appendix 1) turned out to have a weak predictive power on species richness or cover of lichens on trees and were therefore excluded from further analysis. In the final model, the number of lichen species in the sample plots is significantly different for the tree species. The mean number of lichen species is highest on Quercus robur (ca. 11 species), being significantly higher compared with Fraxinus excelsior, Ulmus glabra and U. laevis (on average six species). Species richness on Tilia cordata is intermediate with an average value of eight species (Table 2). Species richness has overall negative correlation with cover of bryophytes (Table 2). We also observed the host tree-specific effects: taking into account the significant interaction term between the variables ‘Tree species’ and ‘Bryophyte cover’, the species richness of lichens decreases particularly drastically with increasing cover of bryophytes for Fraxinus excelsior, Ulmus glabra and U. laevis (Table 2, Fig. 2).
Table 2

The results of general linear mixed model analysis (GLMM) for number of lichen species (log-transformed)

Effect

df

P

Mean

Slope

Tree species

4; 219

0.002

  

    Fraxinus excelsior

  

5.7c

 

    Quercus robur

  

10.7a

 

    Tilia cordata

  

7.8a,b

 

    Ulmus glabra

  

6.0b,c

 

    Ulmus laevis

  

5.8b,c

 

Bryophyte cover

1; 219

<0.0001

  

Bryophyte cover × Tree species

4; 219

0.104

  

    Fraxinus excelsior

 

0.011

 

−0.038*

    Quercus robur

 

0.523

 

−0.008

    Tilia cordata

 

0.646

 

−0.004

    Ulmus glabra

 

0.024

 

−0.024*

    Ulmus laevis

 

0.018

 

−0.025*

Circumference

1; 219

0.063

  

Circumference × Tree species

4; 219

0.014

  

    Fraxinus excelsior

 

<0.0001

 

−0.703***

    Quercus robur

 

0.172

 

−0.242

    Tilia cordata

 

0.521

 

0.117

    Ulmus glabra

 

0.328

 

−0.207

    Ulmus laevis

 

0.181

 

0.328

Bark pH

1; 219

0.386

  

Bark pH × Tree species

4; 219

0.002

  

    Fraxinus excelsior

 

0.353

 

−0.036

    Quercus robur

 

0.012

 

0.251*

    Tilia cordata

 

0.765

 

0.024

    Ulmus glabra

 

0.004

 

−0.194**

    Ulmus laevis

 

0.003

 

−0.191**

The significance test for the slope estimates different from zero: *P < 0.05, ** P < 0.01, *** P < 0.0001. Other notations as in Table 1

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Fig. 2

Relationship between number of lichen species and cover of bryophytes for different tree species according to the general linear mixed model (see Table 2). The scale ‘Number of lichen species’ is log-transformed and the scale ‘Bryophyte cover’ is square-root transformed. F.e., Fraxinus excelsior; Q.r., Quercus robur; T.c., Tilia cordata; U.g., Ulmus glabra; U.l., Ulmus laevis. Significance: * P < 0.05; ns, not significant

Considering the significant interaction term between the variables ‘Tree species’ and ‘Circumference’, the significant negative effect of ‘Circumference’ on the species richness of lichens is revealed only for Fraxinus excelsior (Table 2, Fig. 3). We also observed tree species-specific variation in the effects of bark pH on the species richness of lichens (Table 2). On Quercus robur, species richness increases with increasing bark pH, while lichen richness decreases on both Ulmus species with increasing bark pH (Table 2, Fig. 4).
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Fig. 3

Relationship between number of lichen species and circumference of tree for different tree species according to the general linear mixed model (see Table 2). The scale ‘Number of lichen species’ and the scale ‘Circumference’ are log-transformed. F.e., Fraxinus excelsior; Q.r., Quercus robur; T.c., Tilia cordata; U.g., Ulmus glabra; U.l., Ulmus laevis. Significance: *** P < 0.0001; ns, not significant

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Fig. 4

Relationship between number of lichen species and bark pH for different tree species according to the general linear mixed model (see Table 2). The scale of ‘Number of lichen species’ is log-transformed. F.e., Fraxinus excelsior; Q.r., Quercus robur; T.c., Tilia cordata; U.g., Ulmus glabra; U.l., Ulmus laevis. Significance: * P < 0.05, ** P < 0.01; ns, not significant

The total cover of lichens differs significantly for the tree species and shows general negative relationship with ‘Bryophyte cover’ and ‘Bark pH’ (Table 3). The host tree-specific effects are observed as well. Regarding the significant interaction term between ‘Tree species’ and ‘Bark pH’ the cover of lichens decreases noticeably with increasing bark pH for Fraxinus excelsior, Ulmus glabra and U. laevis (Table 3, Fig. 5). Although the main effect of ‘Tree species’ on lichen species cover in the model is significant, multiple comparison tests did not reveal any significant tree species-specific differences, as the effects of other factors were overwhelming. Besides the substrate-specific effects, also light conditions in a stand determined the cover of lichens on broad-leaved trees: the total cover of lichens increased with increasing light availability of the habitat. The cover of lichens was also dependent on the geographical location of the stand, i.e. the variable ‘Latitude’ in the model is significant.
Table 3

The results of general linear mixed model analysis (GLMM) for cover of lichens (square-root transformed)

Effect

df

P

Mean

Slope

Tree species

4; 223

0.029

  

     Fraxinus excelsior

  

64.8

 

     Quercus robur

  

54.6

 

     Tilia cordata

  

54.7

 

     Ulmus glabra

  

64.7

 

     Ulmus laevis

  

67.1

 

Bryophyte cover

1; 223

<0.0001

 

−0.243***

Bryophyte cover × Tree species

4; 223

0.139

  

Bark pH

1; 223

0.001

  

Bark pH × Tree species

4; 223

0.039

  

     Fraxinus excelsior

 

0.001

 

−1.129**

     Quercus robur

 

0.438

 

0.711

     Tilia cordata

 

0.067

 

−1.350

     Ulmus glabra

 

<0.0001

 

−2.452***

     Ulmus laevis

 

0.006

 

−1.315**

Habitat lightness

1; 223

0.009

 

0.521**

Latitude

1; 223

0.001

 

−5.264**

Notations as in Table 1

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Fig. 5

Relationship between total cover of lichens and bark pH for different tree species according to the general linear mixed model (see Table 3). The scale of ‘Lichen cover’ is square-root transformed. F.e., Fraxinus excelsior; Q.r., Quercus robur; T.c., Tilia cordata; U.g., Ulmus glabra; U.l., Ulmus laevis. Significance: ** P < 0.01, *** P < 0.0001; ns, not significant

Discussion

Both the tree and stand level environmental variables determined the diversity of lichen species on temperate broad-leaved trees, however, the effect of tree species and substrate characteristics was more pronounced than the effect of the environmental conditions of the stand. The results of our study are in good agreement with the conclusions made by Löbel et al. (2006) and Belinchón et al. (2007) who also found that substrate characteristics are crucial for the richness of epiphyte species at the tree level. The importance of habitat characteristics is expected to be more obvious when lichen diversity is measured at the stand level or in different forest site types (Oksanen 1988; Humphrey et al. 2002; Jüriado et al. 2003).

Our observations demonstrate that there are small but significant differences in the species richness, composition and cover of lichens among temperate broad-leaved tree species. The greatest difference in lichen species composition was found between fairly acid-barked trees (Quercusrobur and Tilia cordata) and moderately acid to subneutral-barked trees (Ulmusglabra and U. laevis). Similar results were also obtained by Sander (1999) who analysed the diversity of lichens on temperate broad-leaved trees in rural parks of Estonia.

The studied tree species showed tree-specific peculiarities in relation to the evaluated substrate characteristics. We found that the bark pH of moderately acid to subneutral-barked trees (Fraxinusexcelsior and Ulmus spp.) increased with the circumference of tree. Still, the effects of tree ageing and/or tree size on bark acidity are hard to generalize as reverse effects have been observed depending on analysed tree species (Bates and Brown 1981; Bates 1992; Hyvärinen et al. 1992; Ellis and Coppins 2007b). We also noted that bark pH is higher in the case of trees with a more extensive cover of bryophytes. This relationship can be considered indicative correlation as, generally, bryophytes favour high bark pH and can even alter it (Barkman 1958). Inter-correlation among the studied substrate characteristics was revealed also from ordination analysis. Changes in the composition of lichen communities on broad-leaved trees are mainly due to the covariation of several environmental variables combined, i.e. covariation of cover of bryophytes with bark pH or with tree size (circumference).

The relationships of richness and cover of lichen species on trees with the studied environmental characteristics showed also tree-specific effects. The contradictory results regarding the relationship of richness of lichen species with bark pH observed in this study and in other studies (Du Rietz 1945; Culberson 1955; Kuusinen 1995; Löbel et al. 2006; Cáceres et al. 2007) are apparently due to the comparatively small variation in the bark pH of the analysed tree species. A hump-back relationship has been revealed in the case of a sufficiently long gradient of bark pH as an extremely acid or alkaline bark is unsuitable for lichens (Brodo 1973; Mistry and Berardi 2005).

For trunks of Fraxinus excelsior, we observed a negative effect of tree circumference on richness of lichen species. Several studies have shown that peak species richness on the tree bole is associated with intermediate age of trees: for younger trees species richness has positive relationship with tree age (size) while further on richness of epiphytes decreases with tree age (size) (Adams and Risser 1971; Ellis and Coppins 2006; Johansson et al. 2007). Our observation of the negative relationship between tree size and species richness of lichens fits the described pattern as we studied only mature and over-mature trees.

The negative influence of cover of bryophytes on richness and cover of lichen species occurring on trunks of broad-leaved trees was clearly evident. However, in a similar study conducted in boreo-nemoral forests of the same bio-geographical region and focusing on almost the same trees species, no significant relationship was found between the above parameters (Löbel et al. 2006). This supports the widespread opinion that dominance of either lichens or bryophytes on the tree bole depends greatly on habitat conditions, particularly stand humidity and shade of the habitat (Hong and Glime 1997; Frahm 2003). Apparently, periodical flooding of floodplain forests creates favourable conditions for the epiphytic bryophyte vegetation and, consequently, lichen diversity decreases on the lower part of trunks.

We found that in floodplain forest the composition of lichen species is different on the northern side and on the southern side of the tree trunk, while, the richness and cover of lichen species did not show any significant response to the side aspect of the tree trunk. This result is consistent with that of Sõmermaa (1972) who found a distinct difference in the composition of lichen species on different sides of the tree trunk in various forest types of Estonia. Usually, in forests with a closed canopy, the effect of the cardinal aspect on lichen diversity is found to be nonsignificant (Pharo and Beattie 2002; Coote et al. 2007), or has remained unnoticed due to the overwhelming effects of other factors. The effect of the aspect on lichen communities on the bole is known to be more marked for stands where light exposure is higher (Belinchón et al. 2007) or for solitary trees (Moe and Botnen 1997).

The environmental gradients of habitat availability and soil fertility revealed from ordination analysis indicate the ecological optima for the studied tree species: Quercus robur is the most demanding species with respect to light and Ulmus species are the most shade-tolerant, and in contrast, Q. robur and Tilia cordata prefer less fertile sites than Ulmus glabra (Diekmann 1996). In the studied floodplain forests, the light availability inside the forest stand is apparently a limiting factor for growth of lichens on the tree bole as we found positive relationship between cover of epiphytic lichens and habitat lightness. However, many epiphytes of deciduous trees require the shelter of an unbroken but not too densely shady forest environment (Burgaz et al. 1994; Belinchón et al. 2007). In general, the natural forest ecosystem creates a mosaic of patches with different light conditions (Emborg 1998) and offers optimum habitat lightness for the variety of lichen species (Rose 1992; Esseen et al. 1997).

As a result of the human impact, old-growth deciduous forests are particularly scarce in the region of boreal forests (Nilsson 1992b; Esseen et al. 1997). Although the studied stands were all natural forest communities located in a continuous forest landscape, they have undergone clear-cutting at least once during the past 200 years (Lõhmus 2002). In the forest community, high stand age implies longer colonization time for the species, which is crucial for late-successional lichens characterized by poor dispersal and colonization ability (Hedenås and Ericson 2000). In this study, we established the effect of stand age on composition of lichen species but not on species richness of lichens. This is probably due to the low representation of old-growth stands among floodplain forests or the focus of attention on the small observation scale (tree level).

In conclusion, our observations demonstrate that there are small but significant differences in the species richness, cover and composition of lichens among temperate broad-leaved tree species. The tree-scale effects on the diversity of lichen species are the most pronounced; however, stand characteristics are also crucial for epiphytic diversity in floodplain forests. As substrate-related variables do not affect the richness, cover, and composition of lichen species uniformly for all tree species, the temperate broad-leaved tree species can not be considered a homogenous group in biodiversity and conservation studies. We suggest that deciduous floodplain forests are also a valuable habitat for lichens in the boreal forest region, representing a great diversity of corticolous species and being a substantial habitat for rare, protected and red-listed epiphytic lichens which depend on temperate broad-leaved trees. The maintenance of the tree species diversity and spatial and temporal continuity of those habitats should be the main objective in forest conservation.

Acknowledgements

The authors are thankful to the administration of the Alam-Pedja Nature Reserve, to M. Suurkask from the Soomaa National Park, and to the family Kose for kind help during field work. Special thanks belong to M. Otsus, E. M. Jeletsky, T. Niitla and K. Sasi for the assistance in field work, and to L. Saag and P. Lõhmus for determining and verifying some of the specimens. We are grateful to T. Randlane and anonymous reviewers for valuable comments to the manuscript. We thank E. Jaigma for improving the English text of the manuscript. Financial support was received from the Estonian Science Foundation (grants No. 5494) and from the Estonian Ministry of Education and Research (targeted financing Nos. SF0182639s04, SF0180153s08 and SF0180098s08). This research was also supported by the European Union through the European Regional Development Fund and by the Archimedes Foundation (grant RLOOMTIPP).

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© Springer Science+Business Media B.V. 2008