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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: [email protected]; [email protected]
MAYRA CALDIZ
Environmental Department, The County Administrative Board of Scania,
Kungsgatan 13, SE-205 15 Malmo, Sweden
e-mail: [email protected]
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
Tab
le1.
Des
crip
tio
no
fp
red
icto
ran
dre
spo
nse
vari
able
su
sed
inth
ean
alys
es.
Pre
dic
tors
Sca
leD
escr
ipti
on
Bar
kcr
ack
edO
rdin
alF
req
uen
cy(0
–3
):0
5n
oo
ccu
rren
ce;
15
,1
dm
2;
25
1–
3d
m2;
35
.3
dm
2
Bar
kd
epth
Co
nti
nu
ou
sA
vera
ged
epth
of
fiss
ure
of
the
bar
km
easu
red
atfo
ur
card
inal
dir
ecti
on
sat
bre
ast
hei
ght.
Bar
kd
iver
sity
Ord
inal
Nu
mb
er(0
–3
)o
fth
eb
ark
typ
essm
oo
th,
rou
ghan
dcr
ack
ed.
Bar
kp
Hin
ner
Co
nti
nu
ou
sA
vera
geva
lue
of
the
inn
erb
ark
sam
ple
dat
bre
ast
hei
ght
on
sou
than
dn
ort
hsi
de
of
each
stem
.
Bar
kp
Ho
ute
rC
on
tin
uo
us
Ave
rage
valu
eo
fth
eo
ute
rb
ark
sam
ple
dat
bre
ast
hei
ght
on
sou
than
dn
ort
hsi
de
of
each
stem
.
Bar
kre
cove
ryC
on
tin
uo
us
Bar
kre
gro
wth
(%)
atth
ep
Hsa
mp
les.
Ave
rage
valu
eo
fn
ort
han
dso
uth
sid
eo
fth
est
em.
Bar
kro
ugh
Ord
inal
Fre
qu
ency
(0–
3):
05
no
occ
urr
ence
;1
5,
1d
m2;
25
1–
3d
m2;
35
.3
dm
2
Bar
ksm
oo
thO
rdin
alF
req
uen
cy(0
–3
):0
5n
oo
ccu
rren
ce;
15
,1
dm
2;
25
1–
3d
m2;
35
.3
dm
2
Bar
kth
ick
nes
sC
on
tin
uo
us
Ave
rage
bar
kth
ick
nes
s(e
pid
erm
toca
mb
ium
)m
easu
red
atfo
ur
card
inal
dir
ecti
on
sat
bre
ast
hei
ght.
Cro
wn
pro
ject
ion
Co
nti
nu
ou
sM
axim
um
can
op
yle
ngt
hin
aS
E-N
Wd
irec
tio
n(p
erp
end
icu
lar
toth
ep
reva
ilin
gw
ind
dir
ecti
on
).
DB
HC
on
tin
uo
us
Dia
met
erat
bre
ast
hei
ght,
cm.
Lig
ht
Co
nti
nu
ou
sC
ano
py
sco
pe
met
ho
d(B
row
net
al.
20
00),
valu
em
easu
red
on
sou
than
dn
ort
hst
emsi
de
(bh
),av
erag
eu
sed
.
Mo
ssco
ver
Co
nti
nu
ou
sE
stim
ated
per
cen
tage
cove
ro
fm
oss
esin
10
%-c
lass
eso
nst
emfr
om
0–
2m
hei
ght.
So
ilp
HC
on
tin
uo
us
pH
inh
um
us
laye
rca
1m
fro
mb
ase
of
stem
faci
ng
sou
th.
Ste
min
clin
atio
nC
on
tin
uo
us
Incl
inat
ion
of
stem
mea
sure
din
deg
rees
atth
eh
eigh
to
f1
mw
ith
acl
ino
met
er.
Ste
mfl
ow
pH
Co
nti
nu
ou
sS
tem
flo
ww
ater
pH
sam
ple
dat
bre
ast
hei
ght.
Ave
rage
of
two
sam
ple
s.
Tre
eag
eC
on
tin
uo
us
Act
ual
calc
ula
ted
age
of
bee
ch,
yrs.
Tre
eh
eigh
tC
on
tin
uo
us
Mea
sure
of
tree
hei
ght
(Sil
va6
5).
Tre
evi
tali
tyN
om
inal
05
dam
aged
,w
ith
dec
ay;
15
no
rmal
,h
ealt
hy
tree
Wat
er-h
old
ing
cap
acit
yC
on
tin
uo
us
Mea
sure
das
the
wei
ght
loss
of
the
bar
ksa
mp
les
afte
r2
hr
of
evap
ora
tio
nfr
om
wat
ertr
eatm
ent.
Res
po
nse
s
Sp
ecie
sgr
oup
s(8
)
Lic
hen
sR
Co
nti
nu
ou
sN
um
ber
of
red
-lis
ted
spec
ies
of
lich
ens.
Lic
hen
sI
Co
nti
nu
ou
sN
um
ber
of
ind
icat
or
spec
ies
of
lich
ens
no
tre
d-l
iste
d.
Lic
hen
sC
CC
on
tin
uo
us
Nu
mb
ero
fli
chen
so
fco
nse
rvat
ion
con
cern
(red
-lis
ted
and
ind
icat
or
spec
ies)
.
Lic
hen
sN
CC
Co
nti
nu
ou
sN
um
ber
of
lich
ensp
ecie
sn
ot
red
-lis
ted
or
con
sid
ered
asin
dic
ato
rs.
Bry
op
hyt
esR
Co
nti
nu
ou
sN
um
ber
of
red
-lis
ted
spec
ies
of
bry
op
hyt
es.
Bry
op
hyt
esI
Co
nti
nu
ou
sN
um
ber
of
ind
icat
or
spec
ies
of
bry
op
hyt
esn
ot
red
-lis
ted
.
Bry
op
hyt
esC
CC
on
tin
uo
us
Nu
mb
ero
fb
ryo
ph
ytes
of
con
serv
atio
nco
nce
rn(r
ed-l
iste
dan
din
dic
ato
rsp
ecie
s).
Bry
op
hyt
esN
CC
Co
nti
nu
ou
sN
um
ber
of
bry
op
hyt
esp
ecie
sn
ot
red
-lis
ted
or
con
sid
ered
asin
dic
ato
rs.
Sin
gle
spec
ies
(118
)O
rdin
alA
bu
nd
ance
on
each
stem
:0
5n
oo
ccu
rren
ce;
15
,1
dm
2;
25
1–
3d
m2;
35
.3
dm
2
Fritz et al.: Rare Swedish epiphytes 491
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/
Dw).
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
492 THE BRYOLOGIST 112(3): 2009
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
Fritz et al.: Rare Swedish epiphytes 493
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.
Bark
cracked
Bark
depth
Bark
diversity
Bark
recovery
Bark
rough
Bark
smooth
Bark
thickness
Bark pH
inner
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**
494 THE BRYOLOGIST 112(3): 2009
Table 2. Extended.
Bark pH outer DBH Light Moss cover Soil pH
Stem
inclination
Stemflow
pH
Tree
age
Tree
height
Tree
vitality
1
1
0.281** 1
0.271** 1
1
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.
Fritz et al.: Rare Swedish epiphytes 495
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
496 THE BRYOLOGIST 112(3): 2009
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
R
Lichens
I
Lichens
CC
Lichens
NCC
Bryophytes
R
Bryophytes
I
Bryophytes
CC
Bryophytes
NCC
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).
Fritz et al.: Rare Swedish epiphytes 497
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.
498 THE BRYOLOGIST 112(3): 2009
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.
Fritz et al.: Rare Swedish epiphytes 499
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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502 THE BRYOLOGIST 112(3): 2009
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
Fritz et al.: Rare Swedish epiphytes 503
Scientific name Abbreviation Species group Frequency
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.
504 THE BRYOLOGIST 112(3): 2009
Scientific name Abbreviation Species group Frequency
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.
Fritz et al.: Rare Swedish epiphytes 505