Influence of Stand Age And Structure on the Epiphytic Lichen ...

Lichenologist 24(2): 165-180 (1992)
INFLUENCE OF STAND AGE AND STRUCTURE
ON THE EPIPHYTIC LICHEN VEGETATION IN
THE MIDDLE-BOREAL FORESTS OF FINLAND
M. HYVARINEN*, P. HALONEN* and M. KAUPPI*
Abstract: The epiphytic lichen vegetation on the trunks <strong>of</strong> Pinus sylvestris and Picea
abies was studied and analysed by canonical correspondence analysis in relation to a
number <strong>of</strong> environmental variables. The distribution and abundance <strong>of</strong> epiphytic
lichen species proved to be dependent on the age <strong>of</strong> the stand, showing divergent
responses in relation to phorophyte species and environmental variables such as
acidity <strong>of</strong> the bark and vertical location on the trunk. The importance <strong>of</strong> stand age in
the pattern <strong>of</strong> community variation is concluded to be an outcome <strong>of</strong> interaction
between changes in the structure <strong>of</strong> the tree canopy, microclimate and properties <strong>of</strong>
the bark. The responses <strong>of</strong> single lichen species to changes in the environment seem
to vary considerably, indicating differences in competitive ability and ecological
strategy between the species.
Introduction
The dependence <strong>of</strong> the distribution <strong>of</strong> epiphytic lichens on their habitat and on
other epiphytes has been discussed on numerous occasions, but the multitude
<strong>of</strong> factors that affect the succession <strong>of</strong> epiphytic lichens makes interpretation <strong>of</strong>
the changes difficult. Yarranton (1972) pointed out that changes in epiphytic
lichen communities are primarily dependent on changes in the environment
caused by growth <strong>of</strong> the trees (height-time interaction), and not on the internal
dynamics <strong>of</strong> the communities. He did not find any evidence <strong>of</strong> direct competition
between epiphytic species, although some kind <strong>of</strong> niche differentiation
clearly did exist. However, in studies dealing with succession <strong>of</strong> epiphytes on
deciduous trees it has sometimes mistakenly been taken as a rule that the
morphological lichen types succeed each other from crustose stages through
foliose to fruticose (Barkman 1958; Nakanishi 1960; Hale 1965). Although
succession requires competition between species, the larger, faster-growing
types suppressing the preceding stages, the succession <strong>of</strong> epiphytic lichens may
not correspond to a true autogenic succession as defined by Clements (1916).
Many authors consider interaction between the age and morphology <strong>of</strong> trees
(e.g. height and bark structure) to be the most important factor influencing
epiphytes (Adams & Risser 1971; Yarranton 1972; McCune & Antos 1982),
while Stone (1989), emphasizing the role <strong>of</strong> biotic factors, suggested that
autogenic factors influence the epiphyte succession within the framework <strong>of</strong>
allogenic factors.
The succession <strong>of</strong> epiphytic lichens is closely related to the vertical distribution
<strong>of</strong> species. Koskinen (1955) and Oksanen (1988), for example,
concluded that location on the tree bole was the most important environmental
•Department <strong>of</strong> Botany, University <strong>of</strong> Oulu, SF-90570 Oulu, Finland.
0024-2829/92/020165+16 803.00/0 © 1992 The British Lichen Society

166 THE LICHENOLOGIST Vol.24
factor for epiphytes. Barkman (1958) divided the whole forest stand vertically
into a number <strong>of</strong> microclimatic zones through which trees grow and which
govern the composition <strong>of</strong> the epiphytic vegetation in different parts <strong>of</strong> the tree,
while Kershaw (1964) indicated that the distribution <strong>of</strong> epiphytes on young
trees has the same kind <strong>of</strong> zonation as on older ones but in a more compressed
form. Yarranton (1972) observed that the epiphytic species on the black spruce
{Picea mariana (Mill.) BSP) fall into four main distributional types: (1) crown
and tree base; (2) base only; (3) lower part <strong>of</strong> crown; (4) branchless bole and
base. Generally the structure <strong>of</strong> the branches and the shape <strong>of</strong> the crown have a
considerable influence on the distribution <strong>of</strong> epiphytic lichens.
The aim <strong>of</strong> the present work was to determine the major environmental
factors influencing the distribution <strong>of</strong> epiphytic lichen vegetation on the trunks
<strong>of</strong> the two commonest conifers in the northern European boreal zone: the Scots
pine (Pinus sylvestris L.) and Norway spruce {Picea abies (L.) Karst.). Special
attention was paid to differences between' near natural' and' managed' forests
and to changes attributable to ageing <strong>of</strong> the forests.
Materials and Methods
Area studied
The research was carried out at Muhos in the central part <strong>of</strong> Finland, about 30 km SE <strong>of</strong> Oulu
and the same distance from the coast <strong>of</strong> the Gulf <strong>of</strong> Bothnia (64°45'N, 26°00'E, Fig. 1). The area is
located in the middle boreal subzone <strong>of</strong> Finland (see Ahti et al. 1968), where Scots pine dominates
the drier heath forests and Norway spruce is the main tree species in the mesic and moist forest
types. According to statistics supplied by the Meteorological Institute <strong>of</strong> Finland, the mean annual
temperature in Muhos for the decade 1980-1989 was 1 -7°C (range —0- TC in 1985 to 40°C in 1989)
and mean annual precipitation 549 mm, <strong>of</strong> which 311 mm fell during the growing season (for higher
plants) in May-September. The following climatic parameters are also considered important for
the ecology <strong>of</strong> epiphytic lichens: duration <strong>of</strong> the growing season with mean daily temperatures
exceeding 5°C (147 days), annual number <strong>of</strong> days with precipitation >01 mm (160 days), and
mean maximum snow depth in forests (60 cm). The climate <strong>of</strong> the area is oceanic in terms <strong>of</strong>
temperature, but less so regarding humidity conditions.
Sample plots
The 45 sample plots (see Table 1) make up four age series and were classified as open, managed
(i.e. thinned effectively) pine and spruce stands, and denser, near natural state pine and spruce
stands. The pine-dominated sites were mainly <strong>of</strong> the Empetrum-V'actinium type (EVT), two <strong>of</strong>
them belonging to the Empetrum-Calluna type (ECT) and the spruce sites to the Vaccinium-
Myrtillus type (VMT) or the intermediate type <strong>of</strong> EVT and VMT in the Finnish classification
(Kalela 1961). The main criterion for choice was sufficient homogeneity <strong>of</strong> the stand and its
surroundings (exposure, etc.). Furthermore, the managed stands selected were required to have
remained undisturbed for a period assessed to be sufficient for the epiphytic lichens to respond to
the microclimatic conditions <strong>of</strong> the environment (about 15-20 years).
The following variables were determined for each site: forest site type, canopy cover (scale: 1=0-
10%;2 = ll-20%;. .. 10 = 91-100°,,), basal area(m 2 ha ')<strong>of</strong> the trees (with a relascope, Bitterlich
1948), age <strong>of</strong> trees (with an increment borer), average height <strong>of</strong> trees (with a hypsometer) and the
diameter <strong>of</strong> the sample trees. The acidity <strong>of</strong> the bark at breast height on the trunks was analysed by a
method in which powdered bark was suspended in distilled water (1/10 v/v) for 24h, filtered and
measured with a pH meter. The pH value used was the average <strong>of</strong> the trees studied at each plot.
Five Scots pine trunks <strong>of</strong> medium diameter or three trunks <strong>of</strong> Norway spruce were examined at
each plot. The more heterogeneous epiphytic vegetation <strong>of</strong> pine was considered to need a bigger
sample intensity than spruce to reduce sample variance between the plots. The percentage cover <strong>of</strong>
the lichen species around the trunk was estimated on a five-pointscale (1 = < 3",,; 2 = 3-10° o ; 3 =
11-25%; 4 = 26-50%; 5= >50%) separately in two height classes, 0-0-7 m and 0-7-20 m. The

1992 Epiphytic lichens—Hyvdrinen et al.
167
26°
N
64 °45'
KILOMETRES
FIG. 1. Map <strong>of</strong> the area studied. The pine stands are indicated by dots and the spruce stands by filled
squares.
medians <strong>of</strong> the cover values for the various species on the trunks were used as values for the whole
plot, except in the case <strong>of</strong> a species occurring with the lowest degree <strong>of</strong> cover on less than half <strong>of</strong> the
trunks, when it was given a cover value <strong>of</strong> 0-5. The following cover percentages corresponding to
the estimates obtained in the fieldwere used for the ordination: 0-5 = 0-5; 1 = 1-5; 2 = 7; 3= 18; 4 =
38; 5 = 76. Species occurring on only one sample plot were omitted from the data matrix. The cover
<strong>of</strong> all the macrolichens {Cladonia at genus level only) were determined and also <strong>of</strong> those microlichens
that can be easily identified in the field. Consequently, some crustose groups and related
species, e.g. the order Caliciales, are treated in the ordination as if they were one species. The
species identifications (e.g. for the genus Usnea) were complemented with chemical methods such
as TLC in the laboratory (Culberson & Kristinsson 1970).
Data analysis
The modified data were analysed by canonical correspondence analysis (CCA), a technique for
direct gradient analysis proposed by ter Braak (1986,1987), which allows one to test whether all the
species simultaneously are linearly related to the environmental variables supplied. Consequently,
the direct use <strong>of</strong> environmental data makes it possible to combine the ordination and direct gradient

168 THE LICHENOLOGIST
Vol. 24
TABLE 1. Characteristics <strong>of</strong> the sample plots
Pine stands
Spruce stands
Variable
Managed
(» = 12)
Near natural
(71=13)
Managed
(71=10)
Near natural
(71=10)
<strong>Age</strong> <strong>of</strong> trees (years)
(range)
Canopy cover (%)
(range)
Average height (ra)
(range)
Bark pH
Basal area (m 2 ha~')
67 + 27-1*
(20-110)
58+16-4
(40-80)
13-7 + 41
(7-19)
3-73 + 010
25-3 + 6-9
91 + 36-9
(35-150)
73 + 8-5
(50-80)
15-5 + 4-2
(6-20)
3-75 + 0-13
28-9 + 5-9
75 + 33-7
(30-130)
65+14-3
(50-90)
16-1+5-5
(11-19)
3-48 + 014
23-1+8-3
103 + 41-4
(40-170)
80 + 9-9
(70-100)
15-3 + 5-7
(6-22)
3-36 + 0-17
23-8 + 9-3
*The figures are averages with standard deviations for the plots in each group.
analysis, and to observe the overall influence <strong>of</strong> the environment by approximating the fitting
Gaussian response surfaces to the species (ter Braak 1986).
In the present work certain environmental variables (Table 1) were chosen a priori according to
their assumed importance as factors influencing the epiphytic lichen vegetation. The multiple
correlations between environmental variables (i.e. multicollinearity) were controlled by a Variance
Inflation Factor given by CCA [VIF = (1—R 2 ,)" 1 , where R ; = multiple correlation between
explanatory variable j and other variables in the analysis]. Large values <strong>of</strong> VIF (>20) indicate
near linear dependences amongst variables and instability <strong>of</strong> canonical coefficients (for details see
Montgomery & Peck 1982; ter Braak 1988).
The regression coefficients for the environmental variables were tested by means <strong>of</strong> Student's
r-test, for which purpose the data matrix was also analysed by reciprocal averaging (Hill 1973), in
which the regression is calculated after extraction <strong>of</strong> the species and sample scores and not within
the iterative ordination algorithm as in CCA (ter Braak 1988). The direct use <strong>of</strong> Student's r-test
with canonical coefficients is not recommended because they have larger variances than regression
coefficients.
The CANOCO computer programme produces ordination plots in which the environmental
variables can be combined with species or study sites (ter Braak 1988). Continuous variables (e.g.
tree age) are shown as arrows, the length <strong>of</strong> which indicates the correlation between the variable and
the ordination axes, and the direction <strong>of</strong> which points to the maximum change in the variable.
Nominal variables (e.g. forest site type) are presented in terms <strong>of</strong> centroids showing the weighted
average for the species or sites belonging to that class in relation to the ordination axes.
Results
Sample plots
The ages <strong>of</strong> the trees in the stands varied from 20 to 170 years (Table 1). The
age gradient thus included stages from saplings to old forests. The variation in
stand age is likely to obscure much <strong>of</strong> the variation in other factors measured
between the pine and spruce stands, and to some extent between the classes
' managed ' and ' near natural'. The basal area was high in young stands (the
mean for the pine stands under 70 years was 29-9, n = 8), for example, even if
they had been subject to management. Canopy cover shows better the idea <strong>of</strong>
the original division into classes. The pH <strong>of</strong> the bark, which fitted into a normal
distribution (Wilk-Shapiro test for pH <strong>of</strong> pines W=0-953, P>0-31 and
spruces H^=0-936, P>0-22), varied to some extent between plots, but the
difference between the Scots pines (x = 3-74, S.D. 011) and Norway spruces

1992 Epiphytic lichens—Hyvdrinen et al. 169
TABLE 2. Pearson correlation coefficients for the environmental variables measured in pine and spruce
stands
Variable
<strong>Age</strong> <strong>of</strong>
trees
Canopy
cover
Average
height
BarkpH
Basal
area
Spruce stands
<strong>Age</strong> <strong>of</strong> trees (years)
Canopy cover (° 0 )
Average height (m)
Bark pH
Basal area (ra'ha" 1 )
-0042
0-805
-0-426
-0-333
^-0-114
-0-203
0062
0-683
0-601
-0-286
-0-315
-0173
-0-773
-0050
-0-463
0-265
-0076
0-534
0130
-0-208
Pine stands
(x = 3-42, S.D. 017) as a whole was rather small, albeit significant (ANOVA,
F, 44 = 61-099, P< < 0-001). Furthermore, the pH <strong>of</strong> the bark <strong>of</strong> the spruces
showed a close negative correlation with stand age (r= —0-773, F 219 = 25-741,
P= 0001) while that <strong>of</strong> the bark <strong>of</strong> the pines did so to a lesser extent (r = — 0-426,
F 424 = 5095, P = 0034, see Table 2). Accordingly, the environment <strong>of</strong> the
sample plots is heterogeneous within the framework <strong>of</strong> a few forest types.
Distribution <strong>of</strong> the species
A total <strong>of</strong> 58 lichen species was found on the bark <strong>of</strong> the conifers, 48 <strong>of</strong> them
occurring on pine and 38 on spruce (Table 3). The macrolichen vegetation on
the trunks <strong>of</strong> the pines and spruces was relatively uniform, while the crustose
lichens were found to be more phorophyte-specific, since ten out <strong>of</strong> the 13 pinespecific
species (excluding Cladonia species) and nine out <strong>of</strong> the ten sprucespecific
species were crustose. This is partly a consequence <strong>of</strong> the relatively low
frequency <strong>of</strong> microlichens present. Foliose and fruticose species were more
frequent than crustose species on both phorophytes, although some <strong>of</strong> them
(e.g. Cladonia and Cladina) represent epigeic lichens generally occurring only
on the bases <strong>of</strong> trunks. Some <strong>of</strong> the species are rare in the area and are more
likely to occur on pines, for example Alectoria sarmentosa, a common species on
both conifers in eastern Finland (Halonen et al. 1991). Species completely
absent from spruce were Evernia mesomorpha, Calicium parvum, Haematomma
elatinum, Hypocenomyce scalaris, and some species <strong>of</strong> the genus Lecanora,
whereas E. prunastri and the Caliciaceae, except for C. glaucellum and C.
parvum, were exclusive to spruce. The macrolichens tended to occur more
densely on pines.
The frequencies <strong>of</strong> occurrence on boles were used to analyse the vertical
distribution <strong>of</strong> species on different parts <strong>of</strong> the tree bole by testing for chisquare
goodness <strong>of</strong> fit. The null hypothesis was equal rate <strong>of</strong> occurrence on both
parts <strong>of</strong> the trunk, although the upper trunk was 1 1 times larger than the lower,
assuming that the tree has a conical shape. The shape <strong>of</strong> the lowest part <strong>of</strong> base,
however, equalizes the areas perceptibly. Hypogymnia tubulosa was more frequent
on the upper trunk <strong>of</strong> pine (x 2 = 4-45, P

170 THE LICHENOLOGIST Vol.24
TABLE 3. Percentage frequencies <strong>of</strong> the species occurring on the trunks <strong>of</strong> pine and spruce
Macrolichens
Pine
Spruce
Crustose lichens
Pine
Spruce
Alectoria sarmentosa
Bryoria capillaris
B. furcellata
B.fuscescens
Cetraria chlorophylla
C. islandica
C. pinastri
C. sepincola
Cladina arbuscula
C. rangiferina
C. stellaris
Cladonia bacilliformis
C. botrytes
C. carneola
C. cenotea
C. chlorophaea coll.
C. coniocraea
C. cornuta
C. crispata
C. digitata
C. fimbriata
Cladonia spp.
Evernia mesomorpha
E. prunastri
Hypogymnia physodes
H. tubulosa
Imshaugia aleurites
Parmelia sulcata
Parmeliopsis ambigua
P. hyperopta
Platismatia glauca
Pseudevernia furfuracea
Usnea hirta
U. filipendulaj subfloridana
No. <strong>of</strong> macrolichen species
0-8
920
51 2
91-2
64-8
10-8
92-8
17-6
1-6
8-8
10-8
1-6
40
—
9-6
6-4
1-6
3-2
0-8
9-6
40
73-6
5-6
—
1000
26-4
800
8-8
95-2
960
43-2
4-8
8-8
20-8
32
_
1000
26-7
950
1000
—
93-3
—
—
—
—
3-3
—
1-6
6-7
50
3-3
—
—
133
3-3
63-3
—
150
1000
23-3
Calicium glaucellum
C. parvum
C. trabinellum
C. viride
Chaenotheca chrysocephala
C. subroscida
C. trichialis
Cyphelium inquinans
Haematomnia elatinum
Hypocenomyce scalaris
Lecanora circumborealis
L.fuscescens
L. hypoptella
L. phaeostigma
L. pulicaris
L. symmicta
Lecidea aeruginosa
L. efflorescens
Lepraria incana
Micarea melanea
Microcalicium disseminatum*
Mycoblastus sanguinarius
Ochrolechia alb<strong>of</strong>iavescens
O. androgyna
Scoliciosporum chlorococcum
No. <strong>of</strong> crustose species
3-2
2-4
—
—
—
—
—
—
9-6
9-6
—
0-8
2-4
10-8
16-8
0-8
0-8
—
49-6
10-8
—
7-2
0-8
680
+
16
3-3
—
1-6
31-7
650
150
13 3
16
—
—
6-7
—
—
—
1-6
—
—
1-6
51-7
—
1-6
6-7
—
21-7
+
15
41-7
21-7
980
1000
600
—
78-3
150
23
Total no. <strong>of</strong> the species
48
38
Pine, n= 125; spruce, « = 60.
* = Non-lichenized species; + = common.
Nomenclature follows Santesson (1984).
androgyna (incl. O. alb<strong>of</strong>iavescens) (x 2 = 4-63, P < 0-1, df = 1) and Hypocenomyce
scalaris (x 2 = 2-88, P

1992 Epiphytic lichens—Hyvdrinen et al. 171
TABLE 4. Student's t-test values <strong>of</strong> regression coefficients (reciprocal averaging) and variance inflation
factors (VIF, canonical correspondence analysis) for environmental parameters in the pine, spruce and
combined ordinations
Pines (df= 14)
Spruces(df=
12)
Combined (df= 37)
Axl
Ax 2
VIF
Axl
Ax2
VIF
Axl
Ax 2
VIF
<strong>Stand</strong> age
Host tree
Bark acidity
Basal area
Canopy cover
Average height
Forest type
ECT
EVT
EVT/VMT
VMT
2-49*
—
0-59
012
0-46
0-83
1-44
0-38
0-38
—
0-93
—
0-58
0-95
100
0-74
002
006
006
—
5-36
—
1-81
3-50
3-07
3-87
1-46
2-42
2-22
—
006
—
1-51
0-63
1-40
002
—
—
0-65
0-65
002
—
0-33
005
0-29
0-25
—
—
0-60
0-60
7-32
—
3-80
2-24
1-92
4-72
—
—
2'22
2-22
2-62*
219*
1-24
0-64
0-74
0-60
—
—
—
—
203*
107
0-42
1-26
077
0-29
—
—
—
—
3-29
3-73
3-47
214
2-28
2-82
—
—
—
—
Degrees <strong>of</strong> freedom (df=n —q—1), where n = number <strong>of</strong> samples and q = number <strong>of</strong>
environmental variables.
* = Critical values <strong>of</strong> r-distribution between 005 and 001.
ECT = Empetrum—Calluna type; EVT = Empetrum— Vaccinium type; VMT = Vaccinium—Myrtillus
type; EVT/VMT = intermediate type <strong>of</strong> EVT and VMT. Forest site types according to Kalela
(1961).
spruces and pines to the age factor. In the combined pine-spruce ordination the
age <strong>of</strong> the stand contributes even more to the regression than does the host tree.
In general, the largely different r-values for age in the separate pine and spruce
ordinations indicate differential changes in the trees as substrata during their
growth and/or in pine and spruce stands as environmental entities.
It is also significant that the Variance Inflation Factors in all the ordinations
were fairly low (Table 4). The occurrence <strong>of</strong> the highest VIF values, which are
still well below the limit value <strong>of</strong> 20 proposed by ter Braak (1988), in the pine
and spruce ordinations for the age <strong>of</strong> the stand nevertheless do not show multicollinearity
with the other environmental variables included in the ordination.
Consequently, all the variables contribute to the regression equation and the
regression coefficients merit interpretation. The interactions <strong>of</strong> two pairs <strong>of</strong>
variables in the pine ordination (Fig. 2), stand age and height and basal area and
canopy cover, which seemed to form closely related factors (Table 2), were
tested by constructing product variables. These variables did not appreciably
affect the first eigenvalue (0127 versus 0131), and thus were not used in the
final ordination. In the ordination <strong>of</strong> the species living on pine (Fig. 2), the first
two CCA axes accounted for 74-3% <strong>of</strong> the variance in the weighted averages
with respect to each environmental variable used here.
The species <strong>of</strong> the pine stands could be classified by joint plot projection <strong>of</strong>
weighted averages as those more abundant in young forest and those favouring
old forests. Typical species <strong>of</strong> young forests are Cetraria sepincola, the genus
Lecanora (L. pulicaris and L. fuscescens being most frequent) and also

172
^r H. sea
THE LICHENOLOGIST
AX 2
Vol. 24
1 Calic.
Lecidea spp.
P. fur
-- 3.0
P. amb
Ochrol. spp.
• B. fur
# - I. ale
P. hyp
C. pin
VU. hir
• • P. sul
E. mes • H. tub
Lecanora spp.
3.0
C. sep
HEIGHT
Cladonia spp.
B. fus
P. gla
JD. chl
CANOPY
COVER
AX1
BASAL
AREA
--2.0 • B. cap
U. fil/sub
FIG. 2. Ordination <strong>of</strong> the species on pine by canonical correspondence analysis (CCA). The
eigenvalues <strong>of</strong> the first and second ordination axes are 0127 and 0033, respectively. B. cap =
Bryoria capillaris, B. fur = B. furcellata, B. fus = B. fuscescens, Calic. = Calicium glaucellumlC.
parvum, C. chl = Cetraria chlorophylla, C. pin = C. pinastri, C. sep = C. sepincola, E. mes = Evernia
mesomorpha, H. sea = Hypocenomyce scalaris, H. phy = Hypogymnia physodes, H. tub = H. tubulosa,
I. ale = Imshaugia aleurites, Ochrol. = Ochrolechia androgyna (incl. O. alb<strong>of</strong>lavescens), P. amb =
Parmeliopsis ambigua, P. hyp = P. hyperopta, P. gla = Platismatia glauca, P. fur = Pseudevernia
furfuracea, U. fil/sub = UsneafilipendulajU. subfloridana, U. hir= U. hirta.
Hypogymnia tubulosa. In contrast, Hypocenomyce scalaris, Lecidea species and
the genus Calicium (C. glaucellum and C. parvum) formed a distinct group
occurring more abundantly in old forests. Usneafilipendula (and U. subftoridana)
and Cladonia species on the upper trunk also favoured old forests, but seemed
to differ from the previous group in their responses to the other environmental
factors measured.

1992 Epiphytic lichens—Hyvdrinen et al.
173
AX 2
• 25
-- 0.75
24 10
• 6
EVT
• 14
5 V 7 13
2 H.o
CANOPY
COVER
AX1
18
BASAL
AREA
-. 0.75
FIG. 3. Site ordination <strong>of</strong> the pine stands by CCA. The centroids <strong>of</strong> the nominal variables are
indicated by squares. The ' managed ' stands are nos. 1-12 and the ' near natural' ones nos. 13-25,
the numbers running according to ascending age <strong>of</strong> the stands. The eigenvalues <strong>of</strong> the first and
second ordination axes are 0-127 and 0033, respectively. ECT = Empetrum-Calluna type; EVT =
Empetrum-Vactinium type; VMT = Vaccinium-Myrtillus type; EVT/VMT = intermediate type <strong>of</strong>
EVT and VMT.
Some difficulty is encountered in interpreting the effects <strong>of</strong> acidity <strong>of</strong> the bark
(presented in terms <strong>of</strong> pH values in the figures) and forest density (basal area
and canopy cover). Usneafilipendula could also be classified as a species typical
<strong>of</strong> dense, old forests and showed a preference for less acid bark, and Bryoria
capillaris seemed to act in the same way regarding pH. The high density <strong>of</strong> the
young, non-thinned forests markedly affects the distribution pattern. Cetraria
sepincola and the genus Lecanora, for example, which are common in young
forests, also tend to prefer a higher basal area and a larger canopy cover.
The young stands did not show any grouping into the classes' managed ' and
' near natural' in the ordination <strong>of</strong> the samples (Fig. 3), and the older dense
forests (stands 17-23) formed a cluster loaded close to the origin from which
stand 24, and above all stand 25, are distinct. The latter represents an extremely
old, naturally open stand surrounded by fens and the pines present had a bark <strong>of</strong>
very high acidity (pH = 3-43). The variation between the stands can also be
related to the different forest types to some extent, although much <strong>of</strong> this effect
is included in such stand characteristics as basal area.

174 THE LICHENOLOGIST Vol. 24
A> :2
- 1 0
# E. pru
pH
1.6
B. fur #
P. gla
B. fus
,U .hir
I. ale
C. chi/
P. hyp
P. amb \ .
Ochrol. spp.
HEIGHT
^ ^ ^
STAND AGE
Calic.
•
U. fil/sub
B. cap
X \ \
C. pin
P. sul
1.6
\
\
- 1
\
tub
\
BASAL
AREA
H*phy ^
Lecanora spp.
CANOPY
\. COVER
AX
1
FIG. 4. Ordination <strong>of</strong> the species on spruce by CCA. The eigenvalues <strong>of</strong> the first and second
ordination axes are 0187 and 0078, respectively. Calic. = Caliciales species {Chaenotheca
chrysocephala, C. subroscida and Calicium viride as the most frequent), E. pru = Evernia prunastri,
P. sul = Parmelia sulcata.
None <strong>of</strong> the environmental variables used in the CCA ordination <strong>of</strong> the
spruce data (Fig. 4) reached such a dominant position as did stand age with the
pines. Bark acidity and stand age showed the closest correlation with axis one
and basal area with axis two. These first two axes accounted for 72-9% <strong>of</strong> the
variance in the environmental variables used, with eigenvalues little higher
than in the pine ordination. The most interesting feature <strong>of</strong> the species distribution
was the position <strong>of</strong> the family Caliciaceae (Calicium viride, Chaenotheca
chrysocephala and C. subroscida as the most frequent species). This group,
characteristic <strong>of</strong> spruces, seemed to be more abundant on acid bark in the same
way as the two Calicium species in the pine ordination, but they also favoured
shady habitats, in contrast to the pine ordination.
The combined pine-spruce ordination enabled the epiphytic lichen species
to be grouped according to phorophyte specificity and their response to stand
age. Although the direction <strong>of</strong> the pH gradient in Fig. 5 indicates the division
between pines and spruces, the nominal variables ' spruce' and ' pine' (see
Table 4) were still included in the analysis. The centroids <strong>of</strong> these variables
are not presented because on this scale they would be situated near the centre
<strong>of</strong> the axes. The species occurring almost solely on pines were distributed all
along the age gradient. Thus Cetraria sepincola, Hypogymnia tubulosa, Evernia

1992 Epiphytic lichens—Hyvarinen et al. 175
P. sul
AX 2
_L 4.0
CANOPY
COVER
Calic.
• C.sep
Lecanoraspp.
BASAL
AREA
C. pin
B. cap
• C.chl
• E. pru
4.0
H. tub*
U. hir
H. phy
P. hy>-
I. ale
B. fur
B.fus
P. amb
P. gla
4.0
AX 1
• Ochrol. spp.
U. "/sub
Cladonia spp.
HEIGHT
Lecidea spp.
STAN D AG E
_. 4.0
H. sea
FIG. 5. Ordination <strong>of</strong> the species on pines and spruces combined by CCA. The eigenvalues <strong>of</strong> the
first and second ordination axes are 0-132 and 0090, respectively.
mesomorpha and Hypocenomyce scalaris formed a group characteristic <strong>of</strong> pines
with changing preference from young stands to old ones. Parmeliopsis ambigua,
Ochrolechia spp. and U. filipendula were more abundant in old stands and
slightly on pines, while Bryoria capillaris and C. chlorophylla are age generalists
with a slight preference for spruce. Bryoria fuscescens and Platismatia glauca
fall between these two groups. The core species <strong>of</strong> <strong>of</strong> the lichen vegetation <strong>of</strong> the
pines and spruces were Hypogymnia physodes, Parmeliopsis hyperopta, U. hirta,
C. pinastri, Imshaugia aleurites and B. furcellata, the last two being more
abundant on pines. The family Caliciaceae as a whole was more common in

176 THE LICHENOLOGIST Vol.24
older forest, phorophyte specificity being a more important factor for it than
stand age.
Discussion
Although the lichen vegetation <strong>of</strong> the boreal forests has been surveyed quite
extensively in Northern Europe (e.g. Ahlner 1948; Koskinen 1955; Somermaa
1972; Esseen 1981) and North America (e.g. Ahti 1964; Kalgutkar & Bird 1969;
Yarranton 1972; Jesberger & Sheard 1973; Eversman et al. 1987), floristic
research has mostly concerned the southern subzones <strong>of</strong> the boreal forests and
includes little data with which the present results can be compared. Esseen
(1981) found 24 macrolichens on Norway spruce and 18 on Scots pine in
Central Sweden (middle and southern boreal subzones), these figures being
comparable to the numbers <strong>of</strong> macrolichens observed here when the genus
Cladonia is excluded. Moreover, Somermaa (1972) surveyed the epiphytic
lichen vegetation <strong>of</strong> several forest types in Estonia (hemiboreal zone, Ahti et al.
1968), where the number <strong>of</strong> epiphytic lichen species on Scots pines varied from
33 to 50 depending on the forest type. The differences between the total
numbers <strong>of</strong> epiphytic lichen species found by Somermaa (69 on Scots pines and
74 on Norway spruces) and the present figures are surprisingly small considering
the much more favourable macroclimate <strong>of</strong> the hemiboreal zone and the
higher number <strong>of</strong> forest types surveyed by Somermaa.
The differences in lichen vegetation between the end-points <strong>of</strong> the age gradient
are based on differences in species abundance rather than species composition.
The species dominating young stages <strong>of</strong> the pine stands, other than those
mentioned in the results, seemed mostly to have wide ecological amplitudes and
occurred quite uniformly throughout the age series. A direct visual survey <strong>of</strong>
the abundance <strong>of</strong> the species revealed some interactions between age and other
environmental parameters that did not emerge from the species ordinations.
For example, the abundance <strong>of</strong> B. furcellata increased along the age gradient in
those stands classified as ' managed ' but decrease in the ' near natural' stands.
The position <strong>of</strong> B. furcellata in the pine ordination thus indicated indifference
rather than a preference for young stands. In general, the slightly increasing
total cover <strong>of</strong> the epiphytic lichens with age was mostly caused by the increasing
cover <strong>of</strong> P. ambigua, which was second in abundance to H. physodes on both <strong>of</strong>
the phorophytes.
The observed pattern <strong>of</strong> vertical distribution <strong>of</strong> some <strong>of</strong> the epiphytes can
best be explained by the properties <strong>of</strong> the bark. According to Koskinen (1955),
the bark at the base <strong>of</strong> the trunk is moister and less acid because <strong>of</strong> the proximity
<strong>of</strong> the soil, and it may have a greater water-holding capacity (Kalgutkar & Bird
1969). The leprose growth forms <strong>of</strong> Pertusariaceae at least are known to be
adapted to moist conditions (Halonen et al. 1991). Ochrolechia androgyna,
which was more frequent on the lower trunk and <strong>of</strong>ten grows on moss, provides
a good example <strong>of</strong> this feature. The winter snow cover, giving shelter from cold
temperatures, could be a further explanation (Barkman 1958). Wirth (1987)
argues that P. hyperopta, which is a relatively weak competitor on the upper
parts <strong>of</strong> the trunk, is highly abundant on the base because it is well adapted to

1992 Epiphytic lichens—Hyvdrinen et al. 177
snow cover. The closely related species P. ambigua did not show this kind
<strong>of</strong> vertical distribution in the present results, however, in contrast to the
observations <strong>of</strong> Somermaa (1972) in Estonia and Sonesson (1989) in Swedish
Lapland.
The influence <strong>of</strong> stand age on the epiphytic lichen vegetation on pines is
based not only on changes in microclimate but also on changes in the physical
and chemical properties <strong>of</strong> the bark. The scaly, peeling bark <strong>of</strong> young pines
changes to the thick, rough shield bark <strong>of</strong> old trees, providing sheltered microhabitats
(cracks, etc.), which are reported to be very important for trapping
lichen propagules prior to germination (Armstrong 1990). The bark <strong>of</strong> spruce
peels more easily and has a finer texture than that <strong>of</strong> pine, and it does not change
much with age, which could explain the more homogeneous epiphytic vegetation
on the spruces. According to Eversman et al. (1987) a scaly bark surface could
effectively prevent the attachment <strong>of</strong> diaspores to the trunk and thus be a major
reason for the differences in epiphyte vegetation observed between the three
conifer species they studied. Correspondingly, we have found a close negative
correlation between the growth rate <strong>of</strong> pine saplings and the number <strong>of</strong> epiphyte
species using them as a substratum, which is presumed to be due to the more
marked exfoliation <strong>of</strong> the bark <strong>of</strong> faster-growing saplings (Hyvarinen et al.
unpublished data). Kalgutkar & Bird (1969) also stated that the differences in
epiphyte succession between Larix lyallii and Pinus albicaulis are caused by
divergent changes in bark texture and water-holding capacity.
According to Barkman (1958) bark changes to become more acid during
stand succession. The bark <strong>of</strong> spruce seemed to act in a similar way, as can be
seen in the present spruce ordination, where the pH <strong>of</strong> the bark carries a higher
weighting than stand age as an environmental factor. The influence <strong>of</strong> the
higher acidity <strong>of</strong> the bark <strong>of</strong> spruce on the differences between the epiphytic
lichen vegetation <strong>of</strong> these two conifers seems to be obvious, however, especially
since those spruce stands with lichen vegetation most closely resembling that <strong>of</strong>
pine stands are the ones with the highest pH values measured. For example, the
family Caliciaceae, which is the key group differentiating between the lichen
floras on these two conifers, consistently occurs more frequently on acid bark.
This group, or at least some <strong>of</strong> its most abundant species (e.g. Chaenotheca
chrysocephala and C. subroscida), may have a good tolerance to acidity, which
may be a decisive factor in competition with macrolichens for space.
Shade tolerance could be another factor that makes it possible for crustose
lichens to receive more space on the trunks <strong>of</strong> spruces. The shape <strong>of</strong> the spruce
canopy causes quite different microclimatic conditions on its trunk from those
on the trunks <strong>of</strong> pines. Furthermore, the epiphyte lichen vegetation is known to
differ greatly between the branches and trunks <strong>of</strong> conifers (Pike et al. 1975,
1977). The trunks <strong>of</strong> spruces receive less light, which could be the main reason
for the greater abundance <strong>of</strong> macrolichens on their branches than on the trunk,
whereas, since the stem flow is presumed to depend on the structure <strong>of</strong> the tree
canopy (Seppanen 1964), the amount <strong>of</strong> water that reaches the bark <strong>of</strong> spruces
can be far less than in pines. However, the longer desiccation time after precipitation
may have a compensating effect. In addition, lichens can effectively gain
moisture by water vapour uptake (Kershaw 1985; Rundel 1988), and particularly
the species with green algae (all the species here) can maintain a positive

178 THE LICHENOLOGIST Vol.24
net photosynthesis even without liquid water (Lange et al. 1986,1988). Consequently
stem flow is likely to be <strong>of</strong> more importance for nutrient availability
than for the water balance <strong>of</strong> the lichen thallus. The occurrence <strong>of</strong> crustose
species more frequently on spruce trunks could be a compromise between
competitive pressure <strong>of</strong> faster-growing growth forms and unfavourable light
conditions, analogous to the observations <strong>of</strong> Jesberger & Sheard (1973) and
Kantvilas & Minchin (1989), who proposed the roughness and dryness <strong>of</strong> the
bark as environmental factors creating room for crustose species.
Time and height-time interaction were found to be consistently important
for the distribution <strong>of</strong> macrolichens on black spruce by Yarranton (1972), who
stated that the effect <strong>of</strong> absolute age is merely a function <strong>of</strong> the increasing height
<strong>of</strong> the trees, which alters the microclimate <strong>of</strong> the stand. In the present work the
average height <strong>of</strong> the stand, as indicated by the length and close proximity <strong>of</strong>
the arrow to the first axis in the pine ordination (Fig. 2), is closely related to the
pattern <strong>of</strong> community variation, although the distinction between the stand age
and the average height is too small to permit separation <strong>of</strong> the effects <strong>of</strong> these
variables on the distribution <strong>of</strong> individual species by visual interpretation <strong>of</strong>
the plot pattern. Overall, the r-values for the regression coefficients <strong>of</strong> these
variables (Table 4) clearly indicate that average height has only a small
independent function with respect to community variation and that it fuses into
the effect <strong>of</strong> stand age and other changes in the structure <strong>of</strong> the stand and
individual trees.
Interspecific morphological variability, especially in the surface area to
weight ratio, is known to be significant for the ecology <strong>of</strong> lichens through its
direct influence on water balance (Larson & Kershaw 1976; Kershaw 1985).
Usnea filipendula and B. capillaris, which represent slender and pendulous
growth forms, clearly prefer denser stands than the more shrub-like, robust
species B.furcellata and U. hirta. Bryoriafuscescens, which is quite common in
all kind <strong>of</strong> stands, could be considered indifferent in this respect. The taxonomy
<strong>of</strong> B. fuscescens is not clear, however, and it is considered to be a taxon
containing several forms (Brodo & Hawksworth 1977) that may have different
ecological demands.
The growth form <strong>of</strong> a species is closely linked to the concept <strong>of</strong> ecological
strategy among epiphytes. Rogers (1988,1990) classified lichen species according
to Grime's (1979) triangular ordination model, linking fruticose and foliose
growth forms with a competitive strategy and crustose ones with stress-tolerant
and ruderal strategies. As suggested by Rogers & Barnes (1986), the ecological
strategy <strong>of</strong> a lichen is related to the substratum type, with short-term substrata
open to colonization only by ruderal species. In the present material a ruderal
strategy concerning successional change in the epiphytic lichen communities
could only be associated with such species as Cetraria sepincola and Lecanora
spp., which give way to others after colonizing a new surface on the bark <strong>of</strong>
pines.
Overall, the mean strategy <strong>of</strong> the lichen species with increasing stability <strong>of</strong>
the substratum and environment during natural succession could be assumed
to shift slightly from ruderality towards the competitive pole (Rogers 1988).
Consequently, species such as Cladonia spp. and U. filipendula, which are
abundant in dense, old pine-stands, are considered to be good competitors

1992 Epiphytic lichens—Hyvdrinen et al. 179
owing to their growth form, while the crustose species preferring acidity, such
as the family Caliciaceae and Lecidea spp., could be classified as stress-tolerant.
Special thanks are extended to Mr O. Vitikainen and Dr L. Tibell for their help in identifying some
<strong>of</strong> the lichen specimens. We also wish to thank Dr J. Oksanen and Mr T. Muotka for reading the
manuscript and making constructive suggestions and Mr Malcolm Hicks, M.A. for revising the
language. The research was supported by the Academy <strong>of</strong> Finland.
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Accepted for publication 15 September 1991