Biodivers Conserv (2009) 18:105–125
DOI 10.1007/s10531-008-9460-y
ORIGINAL PAPER
Tree and stand level variables influencing diversity
of lichens on temperate broad-leaved trees
in boreo-nemoral floodplain forests
Inga Jüriado Æ Jaan Liira Æ Jaanus Paal Æ Ave Suija
Received: 8 January 2008 / Accepted: 28 August 2008 / Published online: 24 September 2008
Ó Springer Science+Business Media B.V. 2008
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 pH Bryophytes Circumference Epiphytes Floodplain forest Species richness Stand age Temperate broad-leaved trees
Nomenclature Randlane et al. (2007) for lichens; Leht (2007) for vascular plants.
I. Jüriado (&) J. Liira J. Paal
Institute of Ecology and Earth Sciences, University of Tartu, 40 Lai St., 51005 Tartu, Estonia
e-mail: [email protected]
J. Liira
e-mail: [email protected]
J. Paal
e-mail: [email protected]
A. Suija
Natural History Museum of the University of Tartu, 38 Lai St., 51005 Tartu, Estonia
e-mail: [email protected]
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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
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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°05–070 N and 24°38–410 E, 25 sample trees), in the Soomaa
National Park in central Estonia (six stands between 58°22–270 N and 25°00–050 E, 51
sample trees) and in the Alam-Pedja Nature Reserve in eastern Estonia (eight stands
between 58°25–320 N, and 26°09–170 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
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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 9 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 9 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
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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 MonteCarlo 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 Tilia
cordata and Quercus robur 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
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Table 1 The results of general linear mixed model analysis (GLMM) for bark pH
Effect
df
Tree species
4; 244
P
Mean (±SE)
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
Bryophyte cover 9 Tree species
4; 244
0.977
Circumference
1; 244
\0.0001
Circumference 9 Tree species
4; 244
Fraxinus excelsior
Slope
0.044***
0.007
\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
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.
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 Fraxinus excelsior, 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 (A = 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
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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
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).
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
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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).
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).
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 treespecific 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.
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
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Table 2 The results of general linear mixed model analysis (GLMM) for number of lichen species (logtransformed)
Effect
df
Tree species
4; 219
P
Mean
Slope
0.002
5.7c
Fraxinus excelsior
10.7a
Quercus robur
Tilia cordata
7.8a,b
Ulmus glabra
6.0b,c
Ulmus laevis
5.8b,c
Bryophyte cover
1; 219
\0.0001
Bryophyte cover 9 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
Circumference 9 Tree species
4; 219
0.063
0.014
\0.0001
Fraxinus excelsior
-0.703***
Quercus robur
0.172
Tilia cordata
0.521
0.117
Ulmus glabra
0.328
-0.207
0.181
0.328
Ulmus laevis
Bark pH
1; 219
0.386
Bark pH 9 Tree species
4; 219
0.002
-0.242
Fraxinus excelsior
0.353
Quercus robur
0.012
-0.036
Tilia cordata
0.765
0.024
Ulmus glabra
0.004
-0.194**
Ulmus laevis
0.003
-0.191**
0.251*
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
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 (Quercus robur and Tilia cordata) and moderately acid to subneutralbarked trees (Ulmus glabra 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
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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 logtransformed 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
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
Table 3 The results of general linear mixed model analysis (GLMM) for cover of lichens (square-root
transformed)
Effect
df
Tree species
4; 223
P
Mean
Slope
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
Bryophyte cover 9 Tree species
4; 223
0.139
Bark pH
1; 223
0.001
Bark pH 9 Tree species
4; 223
-0.243***
0.039
Fraxinus excelsior
0.001
Quercus robur
0.438
0.711
Tilia cordata
0.067
-1.350
Ulmus glabra
\0.0001
-2.452***
0.006
-1.315**
Ulmus laevis
-1.129**
Habitat lightness
1; 223
0.009
0.521**
Latitude
1; 223
0.001
-5.264**
Notations as in Table 1
123
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Biodivers Conserv (2009) 18:105–125
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
subneutral-barked trees (Fraxinus excelsior 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.
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Biodivers Conserv (2009) 18:105–125
117
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 broadleaved 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
123
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Biodivers Conserv (2009) 18:105–125
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).
Appendices
Appendix 1 Environmental variables employed in data analysis
Variables
Comments
Bryophyte cover
Total cover of bryophytes in a 20 9 20 sample plot on the bole (15%; 0–99%)
Bark pH
Bark pH of a sample plot on the bole (4.89; 3.68–6.46)
Tree aspect
Location of a 20 9 20 sample plot on the northern or on the southern side of a sample
tree
Circumference
Circumference of a sample tree at a height of 1.3 m above ground (135 cm; 63–
360 cm)
Tree species
Tree species under study: Fraxinus excelsior (n = 41), Quercus robur (n = 20), Tilia
cordata (n = 25), Ulmus glabra (n = 20) and Ulmus laevis (n = 22)
Canopy cover
Percent of canopy cover on the scale zero to one near each sample tree (0.8; 0.5–1)
Basal area of treesa Mean basal area of trees in a stand (28.1 m2/ha; 19.6–42 m2/ha)
Number of tree
speciesa
Number of tree species per 0.1 ha sampling area (6; 3–9)
Habitat lightnessa
Mean of respective indicator values per 0.1 ha sampling area according to Ellenberg
(1979), (4.99; 3.45–6.97)
Soil fertilitya
Mean of respective indicator values per 0.1 ha sampling area according to Ellenberg
(1979), (5.54; 4.17–6.99)
Soil moisturea
Mean of respective indicator values per 0.1 ha sampling area according to Ellenberg
(1979), (6.5; 5.54–9.17)
Stand ageb
Age of the oldest trees in a stand (95; 70–140)
Region
The study regions in Estonia (eastern part of Estonia, central part of Estonia and
southwestern part of Estonia)
Site
Study stand within a region
Latitude and
longitude
Geographical co-ordinates of each study stand were recorded by means of GPS
Average values and minimum–maximum range of the variables are presented in brackets
a
The variables were described from 0.1 ha sampling area (Paal et al. 2007)
b
The value of the parameter was obtained from the Forest Survey Database
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Biodivers Conserv (2009) 18:105–125
119
Appendix 2 List of the recorded lichen species
Species
Fra exc Que rob Til cor Ulm gla Ulm lae
Acrocordia cavata (Ach.) R. C. Harris
?
Acrocordia gemmata (Ach.) A. Massal. (Acr gem)
?
Anaptychia ciliaris (L.) Körb.
?
?
?
?
Anisomeridium polypori (Ellis & Everh.) M. E. Barr**
?
Arthonia byssacea (Weigel) Almq. (Art bys)*, NT
?
?
Arthonia didyma Körb. (Art did), NT
?
?
Arthonia mediella Nyl.
?
Arthonia radiata (Pers.) Ach. (Art rad)
?
Arthonia spadicea Leight. (Art spa)
?
?
?
?
?
Arthonia vinosa Leight. (Art vin)
?
?
?
?
?
Arthopyrenia spp. (Arto sp.)
?
?
?
?
Arthothelium ruanum (A. Massal.) Körb. (Arth ru)
?
?
?
?
Bacidia arceutina (Ach.) Arnold (Bac arc)
?
?
Bacidia beckhausii Körb. (Bac bec)
?
Bacidia fraxinea Lönnr. (Bac fra)
?
Bacidia globulosa (Flörke) Hafellner & V. Wirth (Bac glo) ?
?
?
?
?
?
?
?
?
Bacidia incompta (Borrer ex Hook.) Anzi**
?
Bacidia polychroa (Th. Fr.) Körb.
?
Bacidia rubella (Hoffm.) A. Massal. (Bac rub)
?
Bacidia subincompta (Nyl.) Arnold (Bac sub)
?
Bacidina arnoldiana (Körb.) V. Wirth & Vĕzda
?
?
?
?
?
?
Biatora efflorescens (Hedl.) Räsänen
?
?
?
?
?
Biatora helvola Körb. (Bia hel)
?
?
?
?
?
Biatora ocelliformis (Nyl.) Arnold (Bia oce)
?
?
?
?
Biatoridium monasteriense J. Lahm ex Körb. (Biat mo)*, NT ?
?
Buellia disciformis (Fr.) Mudd. (Bue dis)
?
Buellia erubescens Arnold
Buellia griseovirens (Turner & Borrer ex Sm.) Almb.
?
?
Buellia schaereri De Not. (Bue sch)
Candelariella xanthostigma (Ach.) Lettau
?
?
?
?
?
Chaenotheca chrysocephala (Turner ex Ach.) Th. Fr.
?
Chaenotheca furfuracea (L.) Tibell
?
Chaenotheca subroscida (Eitner) Zahlbr.
?
Chaenotheca trichialis (Ach.) Th. Fr.
?
Chaenothecopsis rubescens Vain.**
?
Chrysothrix candelaris (L.) J. R. Laundon
?
Cladonia coniocraea (Flörke) Spreng. (Cla con)
?
?
?
Cladonia fimbriata (L.) Fr.
?
?
?
?
?
?
?
Dimerella pineti (Ach.) Vĕzda (Dim pin)
Evernia prunastri (L.) Ach. (Eve pru)
?
?
Cladonia sp.
Cliostomum griffithii (Sm.) Coppins
?
?
?
?
123
120
Biodivers Conserv (2009) 18:105–125
Appendix 2 continued
Species
Fra
exc
Que
rob
Til
cor
Ulm
gla
Ulm
lae
Graphis scripta (L.) Ach. (Gra scr)
?
?
?
?
?
Gyalecta truncigena (Ach.) Hepp (Gya tru)
?
Haematomma ochroleucum (Neck.) J. R. Laundon (Hae och)
?
?
Hypogymnia physodes (L.) Nyl. (Hypo ph)
?
?
Hypogymnia tubulosa (Schaer.) Hav.
?
?
?
?
Lecania cyrtella (Ach.) Th. Fr. (Len cyr)
Lecania naegelii (Hepp) Diederich & Van den Boom
?
Lecanora allophana Nyl.
?
Lecanora argentata (Ach.) Malme (Leca ar)
?
?
?
Lecanora carpinea (L.) Vain. (Leca ca)
?
?
?
Lecanora chlarotera Nyl. (Leca ch)
?
Lecanora expallens Ach.
?
Lecanora leptyrodes (Nyl.) Degel. (Leca le)
?
Lecanora pulicaris (Pers.) Ach. (Leca pu)
Lecanora rugosella Zahlbr.
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
?
Lecanora symmicta (Ach.) Ach.
?
Lecidea albohyalina (Nyl.) Th. Fr. (Leci al)**
?
Lecidea erythrophaea Flörke ex Sommerf. (Leci er)*, NT
?
?
?
?
?
?
?
Lecidella elaeochroma (Ach.) M. Choisy (Led ela)
?
?
?
Lepraria eburnea J. R. Laundon (Lep ebu)
?
?
?
Lepraria incana (L.) Ach. (Lep inc)
?
Lepraria jackii Tønsberg
?
Lepraria lobificans Nyl. (Lep lob)
?
Lepraria sp.
?
Leptogium lichenodes (L.) Zahlbr.
?
Lobaria pulmonaria (L.) Hoffm.*, NT
?
?
?
?
?
?
?
?
?
?
?
?
Loxospora elatina (Ach.) A. Massal.
?
Melanelia fuliginosa (Fr. ex Duby) Essl. (Mel ful)
?
?
?
?
?
Melanelia sp.
?
?
?
?
?
Melanelia subaurifera (Nyl.) Essl.
?
?
?
?
Micarea prasina Fr. (Mic pra)
?
?
?
?
?
?
?
?
Melanelia subargentifera (Nyl.) Essl.
?
Mycobilimbia epixanthoides (Nyl.) Vitik. Ahti, Kuusinen, Lommi & ?
T. Ulvinen (Myc epi)
Mycobilimbia sabuletorum (Schreb.) Hafellner
?
Mycoblastus fucatus (Stirt.) Zahlbr.
?
Ochrolechia androgyna (Hoffm.) Arnold
?
Ochrolechia arborea (Kreyer) Almb.
?
Opegrapha rufescens Pers. (Ope ruf)
?
?
Opegrapha varia Pers. (Ope var)
?
?
?
?
?
?
?
?
Pachyphiale fagicola (Hepp) Zwackh**
?
?
Parmelia sulcata Taylor
?
?
Parmeliopsis ambigua (Wulfen) Nyl.
?
?
123
?
?
?
?
Biodivers Conserv (2009) 18:105–125
121
Appendix 2 continued
Species
Fra
exc
Peltigera praetextata (Flörke ex Sommerf.) Zopf
?
Pertusaria albescens (Huds.) M. Choisy & Werner
Que
rob
Til
cor
Ulm
gla
Ulm
lae
?
?
Pertusaria amara (Ach.) Nyl. (Per ama)
?
?
?
Pertusaria coccodes (Ach.) Nyl. (Per coc)
?
?
?
?
Pertusaria flavida (DC.) J. R. Laundon (Per fla)**
?
?
?
Pertusaria hemisphaerica (Flörke) Erichsen (Per hem)
?
Pertusaria leioplaca DC. (Per lei)
?
Pertusaria leucostoma A. Massal. (Per leu)
?
?
?
?
Phaeophyscia nigricans (Flörke) Moberg
?
Phaeophyscia orbicularis (Neck.) Moberg (Pha orb)
?
?
Phlyctis agelaea (Ach.) Flot. (Phl age)
?
?
?
?
?
Phlyctis argena (Spreng.) Flot. (Phl arg)
?
?
?
?
?
Physcia adscendens (Fr.) H. Olivier
Physcia tenella (Scop.) DC.
?
?
Pseudevernia furfuracea (L.) Zopf
?
Pyrrhospora quernea (Dicks.) Körb.
?
Ramalina baltica Lettau
?
Ramalina farinacea (L.) Ach. (Ram far)
?
?
Ramalina pollinaria (Westr.) Ach.
?
Sclerophora coniophaea (Norman) J. Mattsson & Middelb.*,
NT
?
Sclerophora nivea (Hoffm.) Tibell*
Tephromela atra (Huds.) Hafellner ex Kalb
Xanthoria parietina (L.) Th. Fr.
?
?
?
?
?
?
The abbreviations of species names are presented in brackets. Species under protection in Estonia are
marked with an asterisk (*), and rare species are marked with two asterisks (**). Red-listed lichen species
are assigned with abbreviation of red-list category (NT, near threatened). Fra exc, Fraxinus excelsior; Que
rob, Quercus robur; Til cor, Tilia cordata; Ulm gla, Ulmus glabra; and Ulm lae, Ulmus laevis
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