Interacting effects of tree characteristics on the occurrence of rare epiphytes in a Swedish beech...

Interacting effects of tree characteristics on the occurrence of rare

epiphytes in a Swedish beech forest area

ORJAN FRITZ AND JORG BRUNET

Southern Swedish Forest Research Centre, Swedish University of Agricultural

Sciences, Box 49, SE-230 53 Alnarp, Sweden

e-mails: orjan.fritz@ess.slu.se; jorg.brunet@ess.slu.se

MAYRA CALDIZ

Environmental Department, The County Administrative Board of Scania,

Kungsgatan 13, SE-205 15 Malmo, Sweden

e-mail: mayra.caldiz@lansstyrelsen.se

ABSTRACT. Many epiphytes in Swedish beech forests are associated with old and damaged trees.

In this study we examined the impact of bark, soil and stemflow pH, water-holding capacity

and bark structures on this association. We also analyzed whether the influence of these factors

differed between species of conservation concern (red-listed and indicator species of woodland

key habitats) and species not of conservation concern. One hundred and one age-determined

living beech trees (range 58–277 yrs) in 13 beech-dominated stands were surveyed in a forest

landscape in southern Sweden. We recorded 119 species in total (76 lichens, 43 bryophytes) of

which 21 were red-listed and 17 indicator species (26 lichens, 12 bryophytes). NMS ordination

showed that the species composition of lichens changed primarily with tree age and along the

gradient of smooth bark versus moss cover. Bark pH and tree vitality were the most important

gradients for bryophyte composition. The combination of old damaged beech trees and high

bark pH resulted in the highest mean number of species of conservation concern for both

lichens and bryophytes. The link between these factors is partly explained by a positive effect of

tree age on the stemflow pH. Species number of bryophytes not of conservation concern

increased with bark pH, whereas the corresponding group of lichens was favored primarily by

increased light availability. Neither the water-holding capacity of bark nor soil pH affected

patterns of species number. The results from this study show that old beech trees infected by

fungi, with a higher bark pH, are the most valuable trees for epiphytes of conservation concern.

KEYWORDS. Bark pH, Biskopstorp, bryophytes, Fagus sylvatica, indicator species, lichens,

red-listed species, stemflow, tree age, tree vitality, Sweden, epiphytes.

¤ ¤ ¤

Beech (Fagus sylvatica) is a dominant tree species in

temperate forests across Europe, and another twelve

species in the genus occur worldwide in the Northern

Hemisphere (Peters 1997). However, due to human

activities the area of natural temperate forests has

decreased dramatically and the remaining parts have

been fragmented and degraded substantially

(Hannah et al. 1995). In Sweden, the existing beech

The Bryologist 112(3), pp. 488–505 0007-2745/09/$1.95/0Copyright E2009 by The American Bryological and Lichenological Society, Inc.

forests are concentrated in the three southernmost

provinces, Scania, Blekinge and Halland, in the

nemoral zone. In this area, beech is the main

phorophyte for many epiphytic species, in particular

for a set of lichens (Almborn 1948). The epiphytic

communities on beech have been adversely affected

by habitat loss, forestry activities and acid deposition

(Arup et al. 1997). This has resulted in decreasing

populations of many bryophytes and lichens that are

now red-listed (Gardenfors 2005; Hallingback 1992).

In order to make appropriate conservation measures,

it is crucial to understand the environmental factors

limiting the distribution of these species on beech.

The occurrence of epiphytes of conservation

concern, here defined as red-listed species and

indicator species of woodland key habitats, in beech

forest has recently been found to be closely associated

with old trees (Fritz et al. 2009). However, not all old

trees host such species, even when growing in close

proximity to trees with source populations. In

addition, species of conservation concern were found

mainly on old, damaged trees, and these species were

therefore hypothesized to depend on the formation

of certain age-related substrate qualities (Fritz et al.

2009).

The physical and chemical properties of the bark

are partly dependent on age and can influence

epiphyte communities to a large extent (Bates 1992;

Boudreault et al. 2008; Farmer et al. 1991a, b;

Gauslaa & Holien 1998; Goward & Arsenault 2000;

Herk 2001; Hyvarinen et al. 1992; Juriado et al. 2009;

Larsen et al. 2007; Mitchell et al. 2005; Schmidt et al.

2001). By regulating nutrient availability, bark pH is

one such chemical factor (Nash 2008). In parts of

southern Scandinavia, bark pH was predicted to be

particularly important in structuring epiphytic

communities, because of the low impact from

mineral-rich dust impregnation and a moderately

humid to moderately dry climate (Barkman 1958).

Variations in bark pH of otherwise comparable

trees of the same species have been attributed to

small scale differences in soil mineral status and

chemical microhabitat differences (Gauslaa 1985,

1995) or dripzone effects (Goward & Arsenault

2000). The potential impact of soil mineral status on

bark pH, and indirectly to the occurrence of different

epiphytic communities, has long been discussed.

Barkman (1958) considered this link ‘‘highly

unlikely.’’ However, Gauslaa (1985) found

correlations between bark chemistry, epiphyte

community and small scale variations in soil mineral

status. Farmer et al. (1991b) hypothesized that bark

pH could be explained by the combination of tree

species, atmospheric chemistry and soil nutrient

status, and Purvis et al. (2008) argued that there is a

connected flow of nutrients between soil, tree and

epiphytes. Bates (1992), however, found only a

limited correlation between chemical soils and bark

attributes, and commented that ‘‘…soil chemistry

has, at most, a modest role in determining bark

chemistry and epiphyte community on a single tree

species.’’ In addition, despite finding significant

correlations between bark and soil chemistry,

Gustafsson and Eriksson (1995) were not able to find

any significant correlation between bark pH and

soil Ca.

Enhanced bark pH has been measured around

stem wounds where nutrient leakage occurs (Gauslaa

1995). Bark around where the stem has been

damaged may maintain a high pH on beech trees

otherwise influenced by acidic stemflow. Due to the

erect-positioned upper branches and smooth bark,

beech has one of the highest amounts of stemflow

from precipitation among European tree species

(Falkengren-Grerup 1989). Beech bark has only a

moderate buffering capacity (Barkman 1958).

Stemflow collects acid compounds from dry and wet

atmospheric deposition, and may thus acidify the

beech bark. Beech bark microhabitats with a high pH

may therefore play an important role for the

occurrence of sensitive epiphytic species.

Water-holding capacity is another bark

property, which together with precipitation, air

humidity and evaporation determines water supply

to epiphytic species (Hauck et al. 2000). The

moisture retention ability of the bark has the

potential to be an important variable for epiphytes

because of their poikilohydric nature, making them

susceptible to drought (Barkman 1958).

In this paper, we studied the combined impact

of soil, tree and bark variables on the occurrence of

epiphytic lichens and bryophytes on age-determined

trees in beech stands. We addressed the following

questions. Is there a link between soil pH, bark pH

Fritz et al.: Rare Swedish epiphytes 489

and the occurrence of particular epiphyte species?

How do bark pH and water-holding capacity interact

with tree age and bark structure in affecting

composition and number of epiphytic lichens and

bryophytes? Which tree characteristics affect the

number of species of conservation concern? What are

the implications of the patterns observed for

conservation of epiphytes in managed beech forests?

MATERIALS AND METHODS

Study area. Data were collected in the proposed

nature reserve of Biskopstorp (56u489050N,

12u539470E) in the province of Halland, southwest

Sweden (Fig. 1). Biskopstorp (ca. 900 ha, of which

190 ha are beech forest) is one of the core areas for

biodiversity associated with beech forests in Sweden

(Fritz 2006).

The altitudes range from about 25 m to 170 m.

Mean annual precipitation is 1100–1200 mm, with

rainfall (of . 1 mm) on more than 130 days per year.

Mean annual temperature is 7uC (Raab & Vedin

1995). The bedrock is dominated by Precambrian

granites. Glacial moraine deposits dominate the soils

(Freden 1994), which are podzolic with raw humus,

resulting in a sparse to absent field layer and where

the ground is commonly covered only by litter. All

the stands studied were beech-dominated, with only

very low proportions of other trees, such as Norway

spruce (Picea abies), Scots pine (Pinus sylvestris),

birch (Betula spp.), oak (Quercus spp.) and rowan

(Sorbus aucuparia). The beech stands are all high

forests and located in a matrix of spruce plantations,

originating from previous management (Lindbladh

et al. 2008).

The province is exposed to predominantly

southwesterly winds, bringing up air pollution from

the European continent and the British Isles.

However, long-term monitoring in the province

shows that sulphur deposition in spruce forests has

decreased from about 25 kg/ha yr21 in 1988 to about

5 kg/ha yr21 in 2007. During the same period the pH

of rainfall on open areas has increased from about

pH 4 to almost 5 (Karlsson et al. 2008).

Study sites. A total of 101 cored and age-

determined living beech trees within 13 stands were

included in this study (Fig. 1). We used a sample of

beech trees from 15 circular sample plots of 7 m

radius (157 m2) (Fahlvik 1999). The sample plots

were located in parts typical of each stand. In two of

the 13 studied stands more than one plot was

surveyed because of obvious heterogeneity in the

stand with respect to the age of the dominating

cohort.

Sampling of variables. Twenty environmental

variables were collected in all, mostly during 2005

and at 0–2 m in height (Table 1). Data on tree age

and diameter at breast height (dbh) were provided

from a previous study (Fahlvik 1999). The age of the

cored beech trees was 58–277 years (mean 175 6 SD

65 yrs). The diameter at breast height for those trees

was 8–103 cm (mean 40 6 14 cm). There was a

positive correlation (R2 5 0.16, p , 0.001, n 5 101,

Linear regression) between age and dbh, and almost a

linear growth with age, but with a large variation.

Tree vitality was divided into either vital healthy trees

or ‘‘damaged’’ trees with visible rot-inflicted wounds

on the stem. Bark recovery was measured in mm and

analyzed as the proportion of regrowth from 2000 to

2006 of the bark pH sample (see below). Bark

recovery is used as expression for tree and bark

vitality of the individual beech tree. Bark diversity

refers to the number of the bark texture types

smooth, rough and cracked on the tree stem.

Bark pH. Bark pieces were systematically

collected at breast height on the north-and south-

facing part on every beech in August 2000. The

collection consisted of pieces cut with chisel and

Figure 1. The location of the study area in southwest Sweden

and the distribution of the 15 plots within the beech-

dominated stands (thin lines) in Biskopstorp (thick line).

490 THE BRYOLOGIST 112(3): 2009

hammer of around 40 cm2 of the bark into the

cambium. The bark samples were air dried at room

temperature, and then cleaned of epiphytes with a

strong brush. The bark was cut into smaller pieces,

and the inner and outer bark were separated with a

chisel or knife. Pieces of outer bark, the hard surface

periderm and the inner bark, the softer and humid

‘‘bast’’ (Braun 1976), were ground separately with a

coffee mill to a powder. For each sample, 1 g of

powder was placed in a 50 ml container with 10 ml

of deionized water. The container was closed to

prevent CO2 contamination, and then shaken for

2 hrs. After that, the pH of the solution was

measured twice for each stem (north, south aspect)

and bark layer (outer, inner) with a digital pH meter.

The average value, separated for outer and inner bark

pH, was used for the analysis. There were data

missing for inner bark pH from seven trees, all from

one stand. In analyses with both outer and inner bark

pH we used 94 samples, and in analyses with only

outer bark pH we used all 101 trees. Because of the

logarithmic scale of pH, all values in this study were

transformed to H+ concentrations in calculations of

means or medians in analyses.

Soil pH. Soil samples (5–15 cm depth, excluding

leaf litter) were taken on October 26, 2005, using a

soil corer (stainless steel cylinder) with a diameter of

7 cm, about one meter from the tree base in a

southerly direction. Soil samples were sieved using a

mesh size of 6 mm, and 5 g of the soil were put in a

50 ml container with 20 ml deionized water. After

stirring the solution for 2 hrs, the pH was measured

with a digital glass electrode pH meter.

Stemflow pH. Stemflow water was collected

during heavy rainfall on October 5, 2008, when most

of the beech leaves still were green, and on October

26, when most leaves had fallen. Water was sampled

in total at 52 beech trees, of which 38 were identical

at both occasions, from 11 plots among 10 stands in

the full data set. Water running down the stem was

collected in small containers generally at the bark pH

sample sites at breast height (one sample for each

stem). To measure the pH of the rain, an open

container collected rainwater in a small gap in the

beech forest canopy in the center of the study area

during the days. The containers were closed and

brought to the lab, where stemflow pH was measured

with a digital glass electrode pH meter. The average

pH-value was used in the analyses.

Bark water-holding capacity. The remnant

pieces from the bark pH samples, with a minimum

surface of 15 cm2, were used to determine the water-

holding capacity. The 61 trees tested were a subset of

the full data set and the sampled trees were

distributed in 11 plots among 10 stands. The pieces

were oven dried for 24 h at 60uC and then weighed

immediately (Dry weight 5 Dw). Pieces of intact

outer bark were placed on absorbent paper and

sprayed 50 times from a height of 50 cm and weighed

(W0). After 2 h of air-drying (+20uC), the bark pieces

were weighed again (W1). Two samples per tree were

measured and the mean was used in the analyses. An

index (WHCIndex) was calculated for each bark piece

using the weights, where the air-dried weight was

subtracted from the wet weight, expressing the

evaporation as the percentage of the dry weight: To

express the remaining water amount in the bark

pieces, the water-holding capacity, the opposite of

the percentage was used: WHCIndex5 1 2 (W0–W1/

Species survey. For every beech tree all species of

epiphytic lichens and bryophytes on the stem to 2 m

height were surveyed using a hand lens (103). Cover

was estimated for each species recorded on a 3-

graded scale: 1 5 rare, , 1 dm2; 2 5 sparse to

moderate, 1–3 dm2; 3 5 abundant, . 3 dm2. Time

spent on each tree was normally about ten minutes,

but varied with trunk size, bark structural complexity

and species number. Unidentified species were

collected and later determined by chemical spot tests

or under the microscope (stereo 20–603 and light

100–6603). However, for the difficult genus

Lepraria, records were included in either Lepraria

incana coll. or the more easily recognized L.

membranacea.

Species groups. We divided all species into eight

groups (Table 1). Red-listed species according to

Gardenfors (2005). The classification of indicator

species for the nature conservation value of

woodland sites, follows Nitare (2000) and Fritz et al.

(2008), but red-listed indicator species were excluded

from this group. These two species groups are

considered as species of conservation concern (CC)

in this paper. Species that are not red-listed or

indicators were lumped in the group ‘‘species not of

conservation concern’’ (NCC), lichens and

bryophytes respectively. The latter grouping consists

mostly of widespread generalists but may include a

few rarer species that could be of conservation

interest. The nomenclature follows Santesson et al.

(2004) for lichens and Hallingback et al. (2006) for

bryophytes.

ANALYSES

Correlation between variables. Spearman

correlation coefficients were calculated between the

variables in the data sets. For highly significantly inter-

correlated variables the threshold value was set to 0.8.

The variables that were kept showed the highest

correlation with the species groups. Thus the variable

crown projection was omitted in further analysis as it

correlated strongly to dbh. For comparing the

stemflow pH on the beech trees sampled at both

occasions a correlation analysis was made. Statistical

analyses, unless otherwise stated, were carried out in

MINITAB (Minitab Inc. 1972–2008).

Species composition. Variables in the full data

set were analyzed by non-metric multidimensional

scaling (NMS) using PC-Ord 5.15 (McCune &

Mefford 1999) in order to describe the species

community and the relation between environmental

variables and community structure. The variables (94

trees 3 17 variables) were related to the abundance

of each single species, i.e., the species composition,

and separated between lichens (94 trees 3 76 species)

and bryophytes (94 trees 3 43 species) (Table 1). In

the final analysis all species and untransformed data

were used. The NMS ordinations were done in auto-

pilot mode comparing 1–6-dimensional solutions.

Sørensen distance measure was used with 250 runs

with the real data compared with 250 runs of

randomized data with 500 iterations each. The run

with the lowest final stress was used. In the final

ordinations stress levels differed significantly (p ,

0.01) from the randomized Monte Carlo tests.

Correlations between the ordination axes and the

variables and species groups respectively were

calculated with Pearson Correlation. Cumulative

correlations (R2) between distances in the original n-

dimensional space and distances on the ordination

axes were also calculated in PC-Ord.

Species number. Spearman Rank Correlations

were used to analyze the correlation between the

variables studied and species number in the eight

species groups. Multiple linear regressions were used

to analyze the relation between the most correlated

variables from the correlation analysis and species

number. The three most important variables

emerging from the analyses of species composition

and species number were divided in two classes each:

tree age (younger or older than 180 yrs) (cf. Fritz et

al. 2009); tree vitality (damaged or vital) and outer

bark pH (lower or higher than the median 5.96). This

resulted in eight exclusive combinations with 8–20

trees per combination (n 5 101). For each

combination the mean number of species recorded

for lichens and bryophytes of conservation concern

were calculated to illustrate interacting effects of age,

vitality and pH. A Mann-Whitney test was used to

analyze potential differences in median numbers of

species between the combinations.

Bark pH-ranges of individual species. The outer

bark pH distribution for each species with at least

five records was calculated. In addition, the outer

bark pH of the beech trees on which the species was

found was tested against the bark pH of all trees from

which it was not recorded (Mann-Whitney test).

RESULTS

Species survey. A total of 119 species were

identified, 76 lichens and 43 bryophytes (Appendix

1). Lepraria incana coll. and Hypnum cupressiforme

were the most frequent species in each organism

group. As many as 61 species had a frequency lower

than 5%. In total we found 38 species of conservation

concern of which 26 were lichens; 21 nationally red-

listed and 17 indicator species.

pH. The outer bark pH (median 5.96) was not

significantly different from the inner bark pH

(median 5.95) (paired t-test, n 5 94, p 5 0.78).

However, the outer bark pH values showed

considerably more variation (range 5.31–7.03) than

the more stable inner bark pH values (range 5.31–

6.25). Up to about pH 6, the bark values on both

sides of the stem correlated strongly. At higher bark

pH on the northern side of the stem the pH values on

the southern side levelled off for the outer as well as

the inner bark. Outer bark pH did not correlate

positively with any other variable than inner bark pH

(Table 2). Inner bark pH correlated positively with

tree age. Both outer and inner bark pH were

negatively correlated to bark recovery (Table 2).

Soil pH was generally low, showed little

variation (median 3.94, range 3.48–4.70), and was

correlated only (negatively) to stemflow pH

(Table 2).

Stemflow pH was high, and varied considerably

(median 6.20, range 5.25–7.25, n 5 52). However,

stemflow pH was very similar at both occasions and

the correlation between the two data sets was highly

significant (R2 5 0.65, r 5 0.806***, n 5 37, one

extreme outlier excluded). The rainfall pH was high

at both occasions and also very similar (pH 1 5 5.7

and pH 2 5 5.8, median 5.77). The high rainfall pH

is probably influenced by either canopy leaching of

neighboring deciduous trees or sea spray, due to the

strong southwesterly wind during sampling. Because

of the similar pH in rain and stemflow at both

occasions, we used a data set of stemflow pH

consisting of median pH-values from trees sampled

at both occasions and single pH-values from trees

sampled once. Stemflow pH correlated positively

mostly with tree age, bark thickness and moss cover,

and negatively mostly with bark recovery, smooth

bark and tree vitality (Table 2).

Bark water-holding capacity. The capacity of

the beech bark pieces studied for storing water was

limited. After two hours almost all the water applied

had evaporated from the bark. However, the index of

WHC correlated positively to several

(intercorrelated) tree variables, such as dbh, bark

fissure depth and bark thickness (Table 2).

Species composition. The ordination of lichen

species cover on beech trees resulted in a three-

dimensional solution with rather equal importance

between the gradients, in total accounting for 70%

of the variance (Fig. 2). The most important

gradient, axis 3 (r2 5 0.30), was mainly correlated to

tree age, whereas moss cover and smooth bark were

the most important variables that correlated to the

second most important gradient, axis 1 (r2 5 0.24)

(Fig. 2). Light was the most important variable on

axis 2 (r2 5 0.16). Of the common lichens, many

species, for example Graphis scripta and Phlyctis

Table 2. Significant Spearman correlations between the beech tree predictors (n 5 94; * p , 0.05; ** p , 0.01 and *** p , 0.001).

Correlation coefficients for the variables stemflow pH and water-holding capacity were calculated from subsets of the full data set.

Only significant correlations are shown.

cracked

diversity

recovery

smooth

thickness

Bark pH

Bark cracked 1

Bark depth 0.477*** 1

Bark diversity 0.524*** 1

Bark recovery 20.246* 1

Bark rough 0.365*** 1

Bark smooth 20.471*** 0.384*** 20.280** 1

Bark thickness 0.322** 0.727*** 0.396*** 20.441*** 1

Bark pH inner 20.265* 1

Bark pH outer 20.293* 0.509***

DBH 0.377*** 0.578*** 0.233* 0.270** 0.691***

Light 0.250*

Moss cover 0.414*** 0.338** 20.456*** 0.396***

Soil pH

Stem inclination

Stemflow pH 20.443** 20.400** 0.526*** 0.329*

Tree age 0.415*** 20.360*** 20.237* 0.704*** 0.332**

Tree height 0.291** 0.338** 0.223*

Tree vitality 20.259* 0.210*

Water-holding capacity 0.344* 0.353**

Table 2. Extended.

Bark pH outer DBH Light Moss cover Soil pH

inclination

Stemflow

height

vitality

0.281** 1

0.271** 1

0.327* 0.345* 0.412** 20.291* 1

0.352** 0.282** 0.219* 0.645*** 1

0.377*** 20.327** 1

20.237* 20.343* 0.243* 1

0.401***

Figure 2. NMS ordination of trees (N) based on species abundance. Bryophytes to the left and lichens to the right. Correlations

with environmental variables for the two most important axes in the three-dimensional solution are shown with a joint plot. Only

variables with r2 . 0.100 (5 significant with the axis) and species of conservation concern are shown. For explanation of species

abbreviations, see Appendix 1.

argena, were ordered along the smooth bark

gradient, and few along the gradients of moss cover

and bark fissure depth, i.e., the lichens were

negatively correlated to increasing moss cover. Along

the tree age and light gradients many common light-

demanding species, such as Parmelia sulcata and

Hypogymnia physodes, were found. The rare lichens,

such as Megalaria laureri and Pachyphiale carneola,

were related to increasing tree age and bark pH

(Fig. 2).

The ordination of bryophyte species cover on

beech trees resulted also in a three-dimensional

solution accounting for 80% of the variance (Fig. 2).

Outer bark pH was positively and tree vitality

negatively related to the most important gradient,

axis 3 (r2 5 0.64), whereas tree age was the variable

that correlated most to the second gradient, axis 1 (r2

5 0.09). Axis 2 was of less importance (r2 5 0.07).

High outer bark pH and tree age favored several

bryophytes of conservation concern, i.e., Antitrichia

curtipendula, Neckera complanata and Porella

platyphylla. On the contrary, the common

bryophytes Dicranum montanum, Dicranum

scoparium and Hypnum cupressiforme, were positively

correlated to tree vitality.

Species number. Outer bark pH, tree age, tree

vitality and stemflow pH were the variables most

strongly correlated to the number of species in the

different groups (Table 3). In the subset of stemflow

data (n 5 52 trees) a multiple regression analysis of

these four most important variables against species

number in groups showed a rather high degree of

explanation, particularly for the number of lichens of

conservation concern (total model R2 (adj) 5 48%)

as well as for bryophytes of conservation concern (R2

(adj) 5 36%). In the full data set (n 5 101 trees) tree

age, outer bark pH and tree vitality were the three

most important for these species groups. Old

damaged beech trees with high bark pH had

significantly more species of lichens (Mann-Whitney

test, p , 0.05) as well as bryophytes (p , 0.05) of

conservation concern than any other combination of

tree age, vitality and bark pH (Fig. 3). For the large

group of lichens not of conservation concern light

was the single most important variable together with

the abundance of smooth bark area, whereas outer

bark pH was the single most important variable for

bryophytes not of conservation concern (Table 3). In

a separate correlation analysis, water-holding

capacity of the bark did not contribute significantly

to the number of species in any group.

pH-ranges for bryophytes and lichens. For

bryophytes as well as lichens there were gradients in the

single species outer bark pH-ranges (Fig. 4).

Particularly for many bryophytes, the median bark pH

on the beech trees from which they were recorded was

significantly different (p , 0.05, Mann-Whitney test)

from the median bark pH on the stems from which

they were not recorded. Often the median bark pH was

higher from the trees with records of these bryophytes,

but a selection of species, e.g., Dicranum montanum, D.

scoparium and Hypnum cupressiforme, were recorded

from trees with a significantly lower median bark pH

than the trees without these species. Most species of

conservation concern were associated with higher

median bark pH than the median pH of all sampled

beech trees (Fig. 4).

DISCUSSION

Species groups and bark properties. This study

confirms that bark pH is a crucial factor among the

variables studied for species number and

composition of epiphytes on beech trunks (Almborn

1948; Studlar 1982). The effect of bark pH was

stronger for lichens and bryophytes of conservation

concern and for bryophytes not of conservation

concern, than for lichens not of conservation

concern.

Low pH can damage lichens by H ion toxicity to

the algal photobiont (Tarhanen 1998), for example

reducing the photosynthesis for Lobaria pulmonaria

(Gauslaa et al. 1996) and limiting nitrogenase activity

in cyanobacterial photobionts (for references, see

Goward & Arsenaud 2000). High bark pH and/or

high moisture content of the substrate can facilitate

spore germination in bryophytes (Wiklund & Rydin

2004).

Beech bark recovery, a measure of tree vitality,

was negatively correlated to both the inner and outer

bark pH, suggesting that growth generates hydrogen

ions that lower the pH. A site with low productivity,

indicating slow tree growth, favored higher bark pH

on aspen (Populus tremuloides) in Canada

(Boudreault et al. 2008). The lichens not of

conservation concern were positively correlated with

bark recovery, possibly because of a general rapid

growth of such vital trees and the subsequent

formation of new smooth bark areas suitable for

colonization, initially with low competition from

bryophytes. This group of lichens was also favored by

increased light availability, which was in accordance

with an earlier study in managed beech forests in

southern Sweden (Olsson 1995), suggesting that the

bulk of species in this group of lichens primarily

requires space and favorable photosynthetic

conditions, not a specific microhabitat quality.

Table 3. Significant Spearman correlation coefficients (rs) between predictors and the number of species in eight groups (n 5 94

trees; * p , 0.05; ** p , 0.01 and *** p , 0.001). Correlation coefficients for the variables stemflow pH and water-holding capacity

were calculated from subsets of the data set. Only significant correlations and variables are shown. For explanation of the

abbreviation of species groups, see Table 1.

Lichens

Bryophytes

Bark pH outer 0.315** 0.357** 0.353** 0.226* 0.354*** 0.427*** 0.321**

Tree age 0.664*** 0.216* 0.624*** 0.497*** 0.388**

Tree vitality 20.317** 20.245* 20.320** 20.403*** 20.391***

Stemflow pH 0.663*** 0.609*** 0.614*** 0.547***

Bark thickness 0.417*** 0.364*** 0.361*** 0.251*

Stem inclination 0.304** 0.223* 0.316** 0.236* 0.214*

Light 0.248* 0.217* 0.357*** 0.224*

Tree height 20.258* 20.235* 20.247* 20.208*

Bark pH inner 0.251* 0.217* 0.225* 0.250*

Bark recovery 20.209* 0.210* 20.204* 20.222*

Bark diversity 0.267** 0.255*

Bark smooth 0.348**

Moss cover 20.223*

Bark depth 0.205*

Figure 3. Mean (6 SE) number of species of conservation concern, lichens and bryophytes, respectively, on surveyed beech trees

(n 5 101) for combinations of tree age (low , 180 yrs; high . 180 yrs), tree vitality (damaged; vital) and outer bark pH (low ,

5.96; high . 5.96).

Interacting effects on species number. Our

results also demonstrate that a single factor, such as

bark pH, is not enough to explain species number on

beech trees. The number of species of conservation

concern was due to the interacting effects of high

outer bark pH, high tree age and low tree vitality.

Nutrient/base cation leakage from wounds and rot

holes may increase the bark pH of the stem

(Barkman 1958; Gauslaa 1985, 1995; Staxang 1969).

This is probably the reason for the positive

Figure 4. Distributions of outer bark pH (min, median, max) for lichens and bryophytes with at least five records. CC marks

species of conservation concern. * Species with a pH-distribution significantly different from the trees from where it was not

recorded. Significance levels: * p , 0.05; ** p , 0.01 and *** p , 0.001.

interacting effect of tree damage and outer bark pH

on species number observed in our study. However,

damaged trees can also have a lower bark pH than

healthy trees (Mikhailova et al. 2005), probably

depending on, e.g., the pH-value in wet deposition,

the tree species involved and the type of damage. In

turn, the number of lichens recorded may correlate

negatively to bark pH (Hyvarinen et al. 1992).

Contradicting responses of lichens to bark pH may

be a result of small variation in the bark pH of the

tree species analysed (Juriado et al. 2008), but could

also depend on competition from bryophytes.

Bark pH is reported to decrease with tree age

because of leaching of the bark (Barkman 1958),

which could be further enhanced in a tree species like

beech because of the substantial stemflow. This was,

however, not observed in our data, and different

relationships between tree age and bark pH have been

reported from different phorophytes (Juriado et al.

2008).

Beech stemflow is produced in precipitation

events exceeding 5 mm (Chang & Matzner 2000),

and is affected not only by wet deposition

composition per se, but also from leaching of living

tissues (leaves, bark) and dry deposition, that can

result in an altered pH of the stem than the pH of the

precipitation (Bergkvist & Folkeson 1995;

Falkengren-Grerup 1989). Acidic stemflow in

combination with a restricted buffering capacity of

the beech bark could result in acidification of large

stem areas. In our study, however, bark pH did not

decrease with increasing tree age. On the contrary,

outer bark pH was almost positively correlated to

tree age. This may be an effect of the higher pH-

values in stemflow on old beech trees measured in

this study. Stemflow pH varies seasonally (Farmer et

al. 1991b), so that during the season with leaves on

the trees there is a canopy release of Ca, K and Mg

ions, whereas during the leafless period there is an

enrichment of H ions and lower pH values in the

stemflow (Staelens et al. 2007); i.e., a leafed-out

canopy of deciduous species neutralizes the acidity of

incident precipitation by ion exchange (Andre et al.

2008a). The stemflow pH at the two different

occasions in our study was, however, high and very

similar, contradicting the literature. The explanation

may be that the sampling begun after .30 mm of

rain already had fallen, and that accumulated acid

compounds as well as neutralizing base cations might

have been washed away from the beech leaves and

stems at an initial stage of the rainfall. Thus, the

explanation for a higher stemflow pH on old trees may

be due to nutrient leakage from stem wounds or from

frost-related bark lesions (Jonsson 1998), which will

favor epiphytes associated with high bark pH on old

trees. The epiphytes, in turn, may reinforce the process

by increase the bark pH by ionic exchange to improve

growth conditions even more (Barkman 1958; Gauslaa

& Holien 1998). Further studies, e.g., on the effects of

nutrient leakage from different types of damage at

different spatial levels, are required to understand the

relationship between tree age and bark pH.

Air pollution and the subsequent acidification of

bark are known to negatively affect epiphytes

(Farmer et al. 1991b), e.g., the red-listed beech moss

Neckera pumila (Hallingback 1992). The long-term

effects of air pollution may be one important reason

why species of conservation concern are concentrated

on old damaged beech trees with high bark pH in our

study area. Historical data indicate that, e.g., Lobaria

pulmonaria was much more common during the 18th

century than today (Tidstrom 1891).

The water-holding capacity of beech bark did

not have a major impact on the number of species,

corresponding with other studies on lichen diversity

(Hauck et al. 2000; Studlar 1982). The water-holding

capacity of bark is considered to increase with age as

the bark of the phorophyte becomes thick and rough

(Barkman 1958). In our study the water-holding

capacity increased significantly with tree size, as

rough bark structures mainly develop on large trees.

Humidity and light are generally referred to as the

main limiting factors for lichens and bryophytes

(Barkman 1958). The low importance of water-

holding capacity of the beech bark to species number

in this study may be due to the closed canopy,

maintaining a rather humid microclimate, and the

high stemflow on beech trees. However, in exposed

situations beech bark may be unsuitable for

desiccation-sensitive epiphytes, because of the low

capacity of beech bark to store water, and a low

adaptation to withstand overheating of the cambium

(Nicolai 1986), making the beech bark a very dry

habitat.

Linking of soil, bark and epiphytes. In this

study soil pH correlated only (negatively) with

stemflow pH, whereas outer bark pH was almost

positively correlated to stemflow pH, suggesting tree

characteristics more important than soil for outer

bark pH (cf. Andre et al. 2008b). This study was

conducted on generally acidic and nutrient-poor soils

with low variation in pH, which probably increases

the relative importance of stemflow in influencing

bark pH. Although pH is a good measure of the acid-

base status, further analyses of base cation

concentrations and base saturation are needed to

understand the relationship between stemflow, soil

and bark chemistry.

Conservation and management implications.

The results from this study show that old beech trees

infected by fungi with a higher bark pH are most

valuable for epiphytes of conservation concern.

Although more species were recorded from older

beech trees, younger damaged stems with high outer

bark pH had more species of conservation concern

than vital stems of the same age. This result bears

promise with respect to artificially reducing the time

for substrate formation and increasing substrate

quality in some homogenous younger-mature

previously managed stands for the benefit of certain

species of conservation concern. This could be done by

using chainsaws or axes to induce damage and thus

fungal colonization that may eventually create

attractive sites for establishment of epiphytic species of

conservation concern. Field experiments are, however,

needed to develop recommendations for active habitat

restoration to favor epiphytes in beech forests.

ACKNOWLEDGMENTS

Valuable comments on the manuscript have been provided by

Ulf Arup, Nils Cronberg and Nele Ingerpuu. Mats Niklasson

assisted in the bark sampling and in the laboratory measuring

bark pH and water-holding capacity. Erik Ockinger assisted

with water-holding capacity measurements. Vikki Bengtsson

has made linguistic corrections and Nils Fahlvik has provided

data from cored beech trees. WWF Sweden funded the bark

sampling. The study is part of the research program

‘‘Sustainable Management of Hardwood Forests’’ at the

Swedish University of Agricultural Sciences.

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Appendix 1. List of lichens (n 5 76) and bryophytes (n 5 43) recorded and their frequency on 101 surveyed beeches in the study

area of Biskopstorp, Sweden. Red-listed species and indicators are species of conservation concern. NCC 5 species not of

conservation concern.

Scientific name Abbreviation Species group Frequency

Lichens (n = 76)

Lepraria incana Lep_inca NCC 0.93

Pertusaria pertusa Per_pert NCC 0.64

Phlyctis argena Phl_arge NCC 0.63

Graphis scripta Gra_scri NCC 0.51

Cladonia coniocraea Cla_coni NCC 0.37

Pyrenula nitida Pyr_nita Red-listed 0.33

Melanelia fuliginosa Mel_fuli NCC 0.29

Pertusaria hemisphaerica Per_hemi NCC 0.29

Parmelia sulcata Par_sulc NCC 0.24

Cladonia digitata Cla_digi NCC 0.23

Lecanora chlarotera Lec_chla NCC 0.20

Pertusaria amara Per_amar NCC 0.20

Lecanora glabrata Lec_glab Red-listed 0.15

Normandina pulchella Nor_pulc Red-listed 0.13

Anisomeridium polypori Ani_poly NCC 0.10

Ropalospora viridis Rop_viri NCC 0.10

Micarea prasina Mic_pras NCC 0.09

Parmelia saxatilis Par_saxa NCC 0.09

Agonimia allobata Ago_allo Red-listed 0.08

Arthonia spadicea Art_spad Indicator 0.08

Dimerella pineti Dim_pine NCC 0.08

Opegrapha varia Ope_vari NCC 0.08

Arthonia radiata Art_radi NCC 0.07

Buellia griseovirens Bue_gris NCC 0.07

Evernia prunastri Eve_prun NCC 0.06

Opegrapha viridis Ope_viri Indicator 0.06

Thelotrema lepadinum The_lepa Indicator 0.06

Bacidia rubella Bac_rube Indicator 0.05

Haematomma ochroleucum Hae_ochr NCC 0.05

Lecanora expallens Lec_expa NCC 0.05

Arthonia didyma Art_didy NCC 0.04

Biatora efflorescens Bia_effl NCC 0.04

Megalaria laureri Meg_laur Red-listed 0.04

Mycobilimbia piluliferum Myc_pilu Red-listed 0.04

Pachyphiale carneola Pac_carn Red-listed 0.04

Parmeliella hyperopta Par_hype NCC 0.04

Bacidina phacodes Bac_phac Red-listed 0.03

Fuscidea cyathoides Fus_cyat NCC 0.03

Hypogymnia physodes Hyp_phys NCC 0.03

Lecidella elaeochroma Lec_elae NCC 0.03

Lecanora intumescens Lec_intu NCC 0.03

Ochrolechia subviridis Och_subv NCC 0.03

Opegrapha vulgata Ope_vulg NCC 0.03

Peltigera praetextata Pel_prae Indicator 0.03

Pertusaria albescens Per_albe NCC 0.03

Arthonia vinosa Art_vino Indicator 0.02

Biatora chrysantha Bia_chry NCC 0.02

Candelaria concolor Can_conc NCC 0.02

Cladonia polydactyla Cla_poly NCC 0.02

Cladonia squamosa Cla_squa NCC 0.02

Lepraria membranacea Lep_memb NCC 0.02

Leptogium lichenoides Lep_lich Indicator 0.02

Lobaria pulmonaria Lob_pulm Red-listed 0.02

Micarea peliocarpa Mic_peli NCC 0.02

Ochrolechia androgyna Och_andr NCC 0.02

Parmeliopsis ambigua Par_ambi NCC 0.02

Phlyctis agelaea Phl_agae Indicator 0.02

Pseudosagedia aenea Pse_aene NCC 0.02

Thelopsis rubella The_rube Red-listed 0.02

Bacidia incompta Bac_inco Red-listed 0.01

Bacidia rosella Bac_rose Red-listed 0.01

Bacidia viridifarinosa Bac_viri NCC 0.01

Biatoridium monasteriense Bia_mona Red-listed 0.01

Cladonia fimbriata Cla_fimb NCC 0.01

Gyalecta flotowii Gya_flot Red-listed 0.01

Lecania cyrtellina Lec_cyrt NCC 0.01

Lecanora allophana Lec_allo NCC 0.01

Menegazzia terebrata Men_tere Red-listed 0.01

Mycobilimbia epixanthoides Myc_epix NCC 0.01

Ochrolechia turneri Och_turn NCC 0.01

Opegrapha ochrocheila Ope_ochr Red-listed 0.01

Opegrapha rufescens Ope_rufe NCC 0.01

Opegrapha sorediifera Ope_sore Indicator 0.01

Pertusaria flavida Per_flav NCC 0.01

Phaeophyscia endophoenicea Pha_endo Indicator 0.01

Pyrrhospora quernea Pyr_quer NCC 0.01

Bryophytes (n = 43)

Hypnum cupressiforme Hypn_cup NCC 0.86

Dicranum scoparium Dicr_sco NCC 0.61

Metzgeria furcata Metz_fur NCC 0.57

Mnium hornum Mniu_hor NCC 0.47

Isothecium myosuroides Isot_myo NCC 0.40

Plagiothecium denticulatum Plag_den NCC 0.38

Dicranum montanum Dicr_mon NCC 0.33

Frullania dilatata Frul_dil NCC 0.33

Isothecium alopecuroides Isot_alo NCC 0.32

Polytrichastrum formosum Poly_for NCC 0.31

Frullania tamarisci Frul_tam NCC 0.25

Neckera complanata Neck_com Indicator 0.25

Ulota crispa Ulot_cri NCC 0.23

Radula complanata Radu_com NCC 0.21

Dicranum majus Dicr_maj NCC 0.16

Zygodon rupestris Zygo_rup Indicator 0.16

Orthotrichum stramineum Orth_str NCC 0.14

Homalothecium sericeum Homa_ser Indicator 0.13

Porella platyphylla Pore_pla Indicator 0.10

Frullania fragilifolia Frul_fra NCC 0.09

Appendix 1. Continued.

Rhytidiadelphus loreus Rhyt_lor NCC 0.09

Brachythecium rutabulum Brac_rut NCC 0.08

Neckera pumila Neck_pum Red-listed 0.08

Zygodon conoideus Zygo_con Red-listed 0.08

Plagiochila asplenioides Plag_asp NCC 0.07

Antitrichia curtipendula Anti_cur Indicator 0.06

Bryum moravicum Bryu_mor NCC 0.06

Lejeunea cavifolia Leje_cav NCC 0.05

Bryum capillare Bryu_cap NCC 0.04

Dicranum fulvum Dicr_ful Red-listed 0.03

Metzgeria fruticulosa Metz_fru Red-listed 0.03

Homalia trichomanoides Homa_tri Indicator 0.02

Lepidozia reptans Lepi_rep NCC 0.02

Lophocolea heterophylla Loph_het NCC 0.02

Nardia scalaris Nard_sca NCC 0.02

Sciuro-hypnum reflexum Sciu_ref NCC 0.02

Campylopus flexuosus Camp_fle NCC 0.01

Leucobryum glaucum Leuc_gla NCC 0.01

Neckera crispa Neck_cri Indicator 0.01

Orthotrichum pulchellum Orth_pul Red-listed 0.01

Plagiomnium cuspidatum Plag_cus NCC 0.01

Plagiothecium undulatum Plag_und NCC 0.01

Thuidium tamarisci Thui_tam NCC 0.01

Appendix 1. Continued.

Interacting effects of tree characteristics on the occurrence of rare epiphytes in a Swedish beech...

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Temporal effects of focus in Swedish

4x2 chassis for Swedish truck

Genetic signatures of divergent selection in European beech

Identification of drought-sensitive beech ecotypes by physiological parameters

"Challenging Swedish Exceptionalism? Teaching while Black"

Effects of herbivores on a Posidonia oceanica seagrass meadow: importance of epiphytes

2013.pdf - Swedish Chamber of Commerce

Helios (Swedish Naturist Magazine)

The carbon balance of a young Beech forest

A First Quantitative Census of Vascular Epiphytes in Rain forests of Colombian Amazonia

Forest Health Pest Alert - Beech Leaf Disease - New York