Journal of Vegetation Science 17: 195-206, 2006

© IAVS; Opulus Press Uppsala.

- Variables influencing the distribution of epiphytic lichens in heterogeneous areas - 195

Variables influencing the distribution of epiphytic lichens in

heterogeneous areas: A case study for Liguria, NW Italy

Giordani, Paolo

DIP.TE.RIS., University of Genova, corso Dogali 1M, I-16136, Genova, Italy; E-mail giordani@dipteris.unige.it

Abstract Introduction
Questions: What are the most relevant environmental vari-
ables influencing the distribution and the species richness of The search for conceptual schemes of interactions
epiphytic lichens in heterogeneous areas of the Mediterranean among organisms and environmental factors is a com-
region? What is the relative importance of substrate- vs.
mon tool in ecology, regardless of the specific study
environmental-related variables? How do climatic and distur-
bance factors interact? organisms; several have been developed especially for
Location: The study was carried out in the Liguria region vascular plants (Austin 1980; Austin & Smith 1989;
(northwestern Italy). This is a complex region where steep Guisan & Zimmermann 2000). Nevertheless, many au-
environmental gradients occur over a few kilometres of longi- thors have reported the difficulty of generalizing phe-
tude and latitude. nomena observed in local case-studies (see e.g. Levins
Methods: Data on lichen species frequencies, collected on the 1966). Some critical points concern the spatial scale of
basis of stratified random sampling, were analyzed using non- action of environmental factors (regional vs. local gra-
metric multidimensional scaling (NMS) and DCA. Indicator dients) (Økland & Bendiksen 1985), difficulty in esti-
Value Analysis (IVA) analysis was used to find indicator
mating some complex interactions (e.g. historical fac-
species for the environmental predictors.
Results: In the survey area, epiphytic lichen distribution de- tors) that may account for a considerable part of vari-
pends on both substrate- and environment-related factors. ability (Økland 1996) or, lastly, the natural variability of
Climatic variables (in particular average yearly temperature the effects. Indeed, in different ecological conditions,
and rainfall), anthropogenic pressures (particularly harvesting limiting factors (and explanatory variables in general)
and atmospheric pollution), bark pH and texture were associ- may be different for the same response variable, they
ated with the main axes of variability in the dataset. Mean may relate to different synergistic or antagonistic proc-
annual rainfall is the best predictor for epiphytic lichen rich- esses or they may have a different minimum – maximum
ness in the survey area. The particular effects of the Mediterra- range of both impact and effect (Økland 1992).
nean region (e.g. the influence of forest fires) and of heteroge-
Most of these aspects, recently investigated in vascu-
neous areas (the variability of diversity in relation to habitat)
were pointed out. Several indicator species, closely linked to lar plants (Økland 1992), are still little known for epiphytic
particular ecological conditions, were found for both substrate- lichens. These organisms represent only a very small part
and environment-related variables. of the biomass in most temperate ecosystems (Lang et al.
Conclusions: The main variables involved seemed to be the 1980). Nevertheless, they play some important roles, e.g.
same reported for other areas, but their relative importance in nitrogen fixation (Kershaw 1985), nesting for several
and their spatial scale of action were in some cases different, invertebrates (Aptroot & Berg 2004) and nutrient cy-
probably due to the geomorphological and climatic heteroge- cling. Because of their poikilohydric nature and their
neity of the survey area. The significant influence of climatic close dependence on the atmosphere for their metabolic
predictors and disturbance factors on epiphytic lichens was
processes (Rundel 1988; Nash 1996), epiphytic lichens
confirmed, suggesting that these organisms may be used suc-
cessfully to describe ecological trends in natural environ- are strongly influenced by both macro- and micro-
ments, also providing practical information at ecosystem level. environmental variables, which affect their richness, abun-
dance, and distribution on different spatial scales, from
Keywords: Climate; Disturbance; Indicator Value Analysis; substrate- to regional level (McCune et al 1997; Kantvilas
Non-parametric multivariate analysis; Stratified random sam- & Minchin 1989; Will-Wolf et al. 2002). The first con-
pling; Substrate. ceptual models describing the relationships among fac-
tors influencing epiphytic lichen distribution (and epiphytic
Nomenclature: Nimis (2003). organisms in general) were proposed by Hilitzer (1925),
who defined direct (or primary) and indirect (or second-
Abbreviations: NMS: Non-metric Multidimensional Scal- ary) factors, based on an approach similar to that pro-
ing. IVA = Indicator Value Analysis. posed for vascular plants. Subsequently, Barkman (1958)
described the relationship among epiphytes vs. environ-
196 Giordani, P.

mental (including insolation, geographical and lected by means of stratified random sampling, are ana-
orographical position of the site and anthropogenic influ- lysed using a non-parametric multivariate technique to
ence), physical and chemical factors. Physical factors obtain information on interactions of factors (Table 1,
include light, temperature and water, while chemical App. 3) thought to influence the distribution and the
factors, e.g. the pH and the elemental composition of the abundance of epiphytic lichens. More focused analysis
bark, relate to both substrate influence and nutrient sup- addresses interpretation of predictors that covary. Two
ply of the lichen. According to this author, a fine and sets of predictors were distinguished: substrate- and envi-
complete series of transitions occurred between direct ronment-related, these latter being further broken down
and indirect factors: e.g. the environmental factor ‘water’ into climatic, disturbance and habitat subsets.
presents several aspects (rainfall, inundation, atmospheric This paper suggests improved methods, based on the
humidity, water capacity and evaporation) that influence distribution of epiphytic lichens, for assessing environ-
epiphytic organisms to different extents and on different mental quality in heterogeneous areas subjected to an-
spatial and time scales. Many later studies confirmed the thropogenic pressure, including monitoring of the ef-
relevance of these factors for lichen ecology (Seaward fects of atmospheric pollution (Nimis et al. 2002), as-
1977; Nash 1996) and physiology (Galun 1988). Several sessing ecological continuity in forest ecosystems (Rose
investigations have focused on different disturbances that 1976; Will-Wolf et al. 2002), and improving knowledge
showed a strong limiting effect on lichen communities in of ecological trends in natural environments, with re-
different areas or periods: e.g. nitrogen compounds in the gard not only to lichens but to habitat as a whole.
Netherlands (van Dobben et al. 2001; van Herk 2002),
SO2 in the 1970s in Great Britain (Hawksworth & Rose
1970) and dust (Loppi & De Dominicis 1996,) or fires Methods
(Garty 1992; Longán et al. 1999) in Mediterranean areas.
For Mediterranean and tropical areas (Saipunkaew et al. Survey area
2005), and more heterogeneous regions in general, inter-
actions among lichens and environment are still poorly The Liguria region, in northwestern Italy, has a
known (Brunialti & Giordani 2003). Apart from investi- surface area of 5314 km2. To the south, it borders on the
gations of flora and vegetation, only a few papers deal Ligurian Sea. A continuous mountainous ridge (Ligurian
explicitly with multivariate analysis of factors influenc- Alps and Ligurian Apennines) separates the Tyhrrenian
ing lichen distribution in Mediterranean areas (see e.g. slopes from the Po Valley basin. Liguria was selected as
Fos 1998; Zedda 2002; Brunialti & Giordani 2003), the study area because of the occurrence of significant
whereas more data are known from temperate regions of environmental gradients for both natural and anthropo-
Central Europe and North America (Degelius 1935; genic variables (Table 1, App. 3). Six main bioclimatic
Barkman 1958; Mc Cune et al. 1997). This is probably regions can be distinguished in the survey area, follow-
due to two main reasons: 1) in Mediterranean areas, ing the classification by Nimis (2003): (a) a narrow
overlapping of different environmental gradients seems Humid Mediterranean region ( < 10 km from the sea),
to be particularly significant, making it difficult to discern limited to some coastal districts mostly to the east of
effects of one factor from another (e.g. co-presence of Genoa, ranging from 0 to 800 m a.s.l.; (b) a Humid Sub-
climatic and anthropogenic factors); 2) the high variabil- Mediterranean region occuring both in the Tyhrrenian
ity both of predictive factors and of lichen distribution and Po valley hinterland to the east of Genoa and to the
and abundance at very large spatial scales make it diffi- extreme west of Genoa near the French border, ranging
cult to generalize the results of more local case studies for from 400 to 1000 m a.s.l. and characterized by decidu-
larger areas. ous Quercus-Carpinus forests; (c) a Dry-Mediterranean
The aim of this paper is to explore environmental region, limited to lowlands and hills close to the sea to
factors correlated to epiphytic lichens in a heterogeneous the west of Genoa; (d) Dry Sub-Mediterranean area
area, as a basis for developing predictive models for occurring mainly in the valleys of the River Po in the
lichen diversity and abundance in Mediterranean regions. western part of the region; (e) a Montane region, includ-
As a contribution towards this goal, I am presenting the ing some areas of the Alps and Apennine hinterlands
results of a case-study carried out in the Liguria region above 1000 m a.s.l., characterised by Fagus forests and
(NW Italy), a climatically heterogeneous Mediterranean (f) a Sub-Alpine region, restricted to areas above the
area. This paper presents an investigation of the interac- tree-line of the highest mountains of the Ligurian Alps.
tions of factors at plot-level, focusing on the interpreta- About 1.5 million inhabitants are concentrated in the
tion of complex gradients of variability and on distin- regional capital, Genoa, and in coastal areas (~2000
guishing effects of different groups of factors that co-vary persons/km2), where high levels of atmospheric pollu-
for this study. Data on epiphytic lichen abundance, col- tion occur, due mainly to traffic and industry. On the
 - Variables influencing the distribution of epiphytic lichens in heterogeneous areas - 197

Table 1. Response (a-c) and predictor (1-18) environmental variables considered in this work and associated indicator species (* p
< 0.05; ** p < 0.01). SA = subset affiliation: R = response variable, S = substrate-related, EC = environmental related – climate, ED
= environment-related – disturbance, EH = environment-related – habitat. See App. 3 for details on environmental variables and
categories.

No. Code Variable SA Categories and Species Indicator Values

a M n Sp Mean number of species R -

b M LAV Mean Lichen Abundance Value R -
c Tot sp Total number of species R -
1 Tr Sp Tree species S Abies alba: Scoliciosporum umbrinum 36.0**; Hypogymnia physodes 34.3**;
Parmeliopsis ambigua 32.9**. Olea europaea: Leprocaulon microscopicum 32.1**;
Heterodermia obscurata 31.5**; Punctelia subrudecta 28.5**; Hyperphyscia
adglutinata 25.1**; Fagus sylvatica: Arthonia radiata 26.8**; Lecanora pulicaris
22.7**; Lecanora intumescens 20.7**.
2 Dec Ev Deciduous vs. evergreen S Deciduous: Physcia adscendens 35.8**; Flavoparmelia caperata 34.4**; Parmelia
sulcata 28.0**; Hyperphyscia adglutinata 25.1**; Amandinea punctata 23.8**;
Candelariella xanthostigma 21.8**. Evergreen: Scoliciosporum umbrinum 25.0**.
3 M Circ Mean Circumference of the trunks S > 100 cm: Lepraria incana 25.9*.
4 pH Bark pH S Basic: Hyperphyscia adglutinata 26.2*. Neutral: Candelariella xanthostigma 34.2**;
Lepraria incana 24.2*. Acid: Scoliciosporum umbrinum 28.2**.
5 Text Bark texture S Smooth: Arthonia radiata 25.9**; Lecanora pulicaris 21.8**; Buellia griseovirens 20.5**.
Medium: Parmelia sulcata 24.9**. Rough: Hyperphyscia adglutinata 25.2**. Very rough:
Flavoparmelia caperata 22.6**; Physcia adscendens 22.6**; Parmotrema chinense 21.3**.
6 Wat Ret Bark water retention S Low: Scoliciosporum umbrinum 23**. Medium: Physcia adscendens 30.8**; Flavoparmelia
caperata 28*; Lepraria incana 25.5*. High: Phaeophyscia orbicularis 49.2**; Xanthoria
parietina 27.6**; Hyperphyscia adglutinata 27.5**.
7 Exf Bark exfoliation S Low: Buellia griseovirens 21.4**. Medium: Leprocaulon microscopicum 20.5**.
High: Melanelia fuliginosa ssp. glabratula 25.1**; Parmelia sulcata 24.1**; Candelariella
xanthostigma 20.8**. Very high: Parmeliopsis ambigua 21.1**.
8 Exp Cardinal exposure of the plot EC No indicator species
9 Long Longitude EC No indicator species
10 Lat Latitude EC No indicator species
11 Elev Elevation above sea level EC < 400 m: Hyperphyscia adglutinata 36.2**; Physcia adscendens 30.8**; Phaeophyscia
orbicularis 28.9**; Leprocaulon microscopicum 24.4**. 400 - 800 m: Flavoparmelia
caperata 21.4*; 800 - 1200 m: Parmelia sulcata 30.3**; Melanelia fuliginosa ssp. glabratula
28.1**; Cladonia parasitica 23.8**; Naetrocymbe punctiformis 21.4**; Phlyctis argena
21.3*; Buellia griseovirens 21.2 ** >1200 m: Scoliciosporum umbrinum 46**; Lecanora
pulicaris 32.9**; Arthonia radiata 29.1**.
16 MA Rain Mean annual rainfall EC Cold humid: Buellia griseovirens 54.1**; Scoliciosporum umbrinum 44.6*; Lecanora
pallida 32.4**; Parmelina pastillifera 28.9**; Pertusaria leioplaca 25.3*; Cladonia parasitica
23.1*. MesoT humid: Parmelia saxatilis 26.2*; Tephromela atra 22.5*. Warm humid:
Leprocaulon microscopicum 31.6*; Parmotrema reticulatum 31**; Normandina pulchella
26.7*. Warm dry: Physcia adscendens 21.5*.
17 MA Temp Mean annual temperature EC
12 Harv Harvesting ED Old coppicewood: Phlyctis argena 26.5*; Parmelina tiliacea 23.7*; Pertusaria pustulata
23.6*; Lecanora strobilina 20.8*. Coppicewood: Physcia adscendens 40.2*.
13 Atm Poll Atmospheric pollution ED Low: Parmelia sulcata 32.1*. Medium: Hyperphyscia adglutinata 28.7*; Phlyctis argena
23.7*. High: Phaeophyscia orbicularis 35.7**; Physcia adscendens 34.6*.
14 For Fir Occurrence of forest fires ED Unburnt: Parmotrema chinense 27.1**. Burnt: Lecanora chlarotera 77.1**; Parmelia
sulcata 56.1*; Parmelina tiliacea 51.6*; Hyperphyscia adglutinata 47.9*; Candelariella
xanthostigma 47.2*; Lecanora expallens 41.9*; Candelariella reflexa 40.1*; Physcia
tenella 36.4*; Physconia grisea 31.7*; Parmelia saxatilis 28.8*; Caloplaca pyracea 28.6*;
Xanthoria parietina 28.2*; Caloplaca pollinii 27.6*; Flavoparmelia soredians 26.8*;
Pertusaria leioplaca 26.5*; Pertusaria pertusa 26.2*; Parmelina quercina 22.2*.
15 Agr Pract Agricultural practices ED Treated: Hyperphyscia adglutinata 79.3**; Punctelia subrudecta 46.4*; Pertusaria amara
43.4*; Collema furfuraceum 21.7*.
18 Hab Habitat EH Olive groves: Punctelia subrudecta 56.8*; Heterodermia obscurata 46*; Collema
furfuraceum 37.1*; Hyperphyscia adglutinata 32.1*; Pertusaria amara 30.5*; Leprocaulon
microscopicum 25.2*; Phaeophyscia orbicularis 24*; Schismatomma decolorans 22.7*;
Punctelia borreri 22.1*. Conifers: Parmeliopsis ambigua 51.4*; Hypogymnia physodes
45.7*; Evernia prunastri 28*. Beechwood: Buellia griseovirens 41.9*; Scoliciosporum
umbrinum 28.7*; Lecanora intumescens 27.2*. Rural areas: Parmelia sulcata 30.7*.
Thermophilous oak woods > 400 m: Lecanora chlarotera 27.3*; Parmotrema chinense
25.3*. Urban areas: Phaeophyscia orbicularis 23.8*. Chestnuts and mesophilous oak
woods < 400 m: Flavoparmelia caperata 20.4*.
198 Giordani, P.

Table 2. Strata with % coverage and number of sampling plots Datasets and data transformation
(N) and size of the adjusted data set (Nadj.); low = < 400 m
a.s.l.; high = > 400 m a.s.l. A total of 196 epiphytic lichen species were col-
Stratum cov N Nadj
lected from the 165 sampled plots. Two matrices were
considered in analysing the data: (1) a matrix of sam-
Olive groves
Thermophilous Quercus woods - low
6.4
2.1
16
16
13
9
pling plots × species abundances and (2) a matrix of
Thermophilous Quercus woods - high 0.3 13 10 sampling plots × environmental factors. To detect and
Chestnut and mesophilous Quercus woods - low) 17.4 19 13 exclude possible outliers from the analysis, an explora-
Chestnut and mesophilous Quercus woods - high 37.4 41 37
Fagus woods 1.6 14 13
tory multivariate analysis was carried out using PCORD
Urban and suburban areas 18.5 20 6 (McCune & Mefford 1999). Outlier sampled plots, plots
Non-forested rural areas 15.2 18 9 with < 3 sampled trees, rare species (occurring in < 5%
Montane conifers 1.3 8 6
Total 100.0 165 116
of sampling plots) and plots containing more than one
tree species were excluded, yielding an adjusted dataset
of 74 species × 116 plots (Table 2; Apps. 1 and 2).
other hand, many mountainous areas are scarcely popu- Eighteen predictor variables, both substrate- and envi-
lated (~10 persons/km2) and have no local sources of air ronmental-related, were considered; see App. 3 for de-
pollution. However, in these latter areas, harvesting of tails of data collection.
wood and forest fires exert significant and increasing To reduce the effect of the high variability and the
environmental pressures. different orders of magnitude within variables on the
final model, quantitative variables in matrix 2 were log-
transformed (McCune et al. 2002).
Sampling design

All the 5420 kilometric UTM intersections within the Ordination

survey area were systematically selected and classified
into nine strata, based on habitat type and altitude (Table I used two different ordination techniques in order to
2). A number of intersections proportional to the surface detect the main factors of variability of epiphytic lichen
occupied by each stratum within the survey area were in the survey area: global Non-metric multidimensional
selected with a stratified random sampling design, using scaling (NMS) (Shepard 1962a, b; Kruskal 1964) with
the ‘random sampling’ option in the software package Sørensen distance, and, for comparison, Detrended Cor-
Statistica 6.0 (StatSoft Italia, Anon. 2001). The sample respondence Analysis (DCA) (Hill & Gauch 1980).
included 165 intersections, corresponding to about 3% of Both analyses were performed with PCORD version
the statistical population. In the field, each intersection 4.25 (McCune & Mefford 1999). I chose unconstrained
selected was positioned using a GPS and a 30 m radius ordinations for my analysis tool because my main goal
plot was installed, centred on the selected coordinates. was to explore relation of lichen communities to exter-
nal variables without making a priori assumptions about
either variables or relationships (Økland 1996). Pearson
Lichen sampling
correlation of quantitative predictor variables (Table 1)
Within each plot, all trees conforming to minimum with ordination axes was used to interpret relationships
standards (circumference > 60 cm; inclination of the bole of these variables to lichen community composition.
< 10°; absence of damage and of decorticated areas on the Variables with r = 0.182 to 0.299 are described as
trunk) within the 30 m radius plots were considered. weakly correlated, those with r ≥ 0.300 are described as
For each tree, the abundance of each lichen species was correlated. For comparison, a Pearson r of 0.182 with N
releved using a sampling grid consisting of a 10×50 cm = 116 is significant at p = 0.05.
ladder divided into 5 10×10 cm quadrants. This ladder grid
was placed systematically on the N, E, S and W side of the Indicator Value Analysis (IVA)
bole of each tree (4 per tree), with the top edge 1.5 m above
ground, following the standards suggested by Asta et al. Indicator Value Analysis (IVA - Dufrêne & Legendre
(2002). Summary measurements of species richness and 1997) was used (PC-ORD - McCune & Mefford 1999)
abundance were calculated for each plot (Apps. 1, 3): to determine indicator species corresponding to various
mean number of species per tree; total number of species ecological conditions at plot level. This method com-
releved within the plot; mean Lichen Diversity Value bines information on species abundance and the reliabil-
(LDV – Asta et al. 2002) calculated as the sum of the ity of occurrence of a species in a given ecological
abundance of each species within the sampling grids on a group. For each species i in each plot group j, the
tree, averaged for all trees within a plot. product of Aij (mean abundance of the species i in the
 - Variables influencing the distribution of epiphytic lichens in heterogeneous areas - 199

plots of group j compared to all groups in the study) by and distances on the three ordination axes is 0.742. Axes
Bij (relative frequency of occurrence of species i in the were rotated by 90°, so that the axis with the highest r2
plots of group j) was calculated as follows: (0.332) was labeled Axis 1, followed by Axis 2 (0.248) and
Axis 3 (0.162) (Figs. 1 & 2 and Table 3).
IVij = Aij * Bij * 100 (1)
Environment-related factors
where IVij is the indicator value of the species i in the
group j. Environment-related factors are those most strongly
The statistical significance of the maximum IVij correlated with ordination axes (Fig. 1 and Table 3). Axis
observed for each species was tested by means of a 1 and Axis 2 represented two climatic gradients: Axis 1
Monte Carlo test, based on 1000 randomizations. from the montane areas of the hinterland to the coast, with
For IVA, quantitative climatic variables were trans- increasing MA Temp and decreasing Elev and Lat; Axis
formed into categorical variables, on the basis of the 2 from the western dry part to the eastern more humid part
range of values observed in the survey area, with the of the survey area, with increasing Long and MA Rain.
following classes: (1) dry and cold; (2) dry and warm; Gradients for the main disturbances influencing epiphytic
(3) mesophilous; (4) humid and cold; (5) humid and lichens covaried with environment-related factors on these
warm (ranges of values for each class in App. 3). axes. Positive scores on Axis 1 were in general associated
with human-disturbed sites, including a composite group
of categories for several variables (Fig. 1a-d). The Non-
Results forest category under ‘Harv’ corresponds with Urban,
Non-forested rural areas and olive groves categories un-
Ordination results: NMS der ‘Habitat’ (Fig. 1d), and Treated category under ‘Agr
Pract’ (Fig 1b); For Fir also overlaps this group. This
NMS analysis was run in autopilot mode, comparing 1- entire group of categories is associated with positive
to 6-dimensional solutions. The best solution was a three- values of axis 1 along with higher impact of Atm Poll
dimensional configuration (maximized difference between (Fig. 1a, Medium and High categories). Positive values
the best of 40 runs of real data and 50 randomized runs, p < on Axis 2 were associated mainly with decreasing Harv
0.05 from Monte Carlo test; average stress = 19.3). Cumu- (Fig. 1c, forested categories) and partially with lower
lative Pearson r2 between distances in the original space Atm Poll. The occurrence of For Fir (mainly positively
related to Axis 1) was also partially negatively associated
with Axis 3 (Table 3).
Table 3. NMS ordination: correlation (r Pearson) of factors Habitat groups on the ordination reflected the two
with three axes. Relations with positive (+), negative (–)
strong environmental gradients along Axis 1 and Axis 2
values of the given axis or a weak relationship (±) were
reported for categorical predictors. See Table 1 for explana- (Fig. 1d). Olive groves and thermophilous oakwoods
tion of SA and factor codes. *M n Sp represents lichen species were associated with positive values of Axis 1, sites
diversity for analyses. with higher temperature and lower elevation. Beech and
conifer woods had negative values along Axis 1, associ-
SA Code Axis1 Axis 2 Axis 3
ated with the highest elevations. Plots in urban areas had
Total axis r2 0.332 0.248 0.162 negative values on Axis 2 and were characterized by a
M n Sp* 0.226 0.663 –0.358 very low species richness. Broadleaf forests (mainly
S Tr Sp + ± ±
chestnuts and mesophilous oaks) and non-forested rural
Dec Ev ±
M Circ –0.158 0.13 –0.074 areas, on the contrary, were associated with positive
pH + values of Axis 2, with mostly higher species richness.
Text +
Wat Ret +
Exf ± Substrate-related factors
EC Exp ±
Long 0.026 0.382 0.064 Tree size (M Circ) showed weak correlations with
Lat –0.349 0.152 0.073
Elev –0.639 0.164 –0.104 all three axes, whereas patterns of several categorical
MA Rain –0.204 0.483 0.001 variables were detected (Table 3). In particular, positive
MA Temp 0.493 –0.023 0.159 values on Axis 1 were associated with increasing rough-
ED Harv -
Atm Poll + ± ness (Fig. 1e), water retention and pH of bark (Table 3),
For Fir + - whereas evergreen tree species were weakly associated
Agr Pract + with positive values of Axis 3.
EH Hab + ±
200 Giordani, P.

Fig. 1. NMS ordination of plots based

on lichen species composition.
Lengths of arrows for predictive fac-
tors represent strength of correlations;
directions represent signs. The arrow
labelled Species Richness is variable
M n Sp; see Table 1 for other variable
codes. Symbols in the charts repre-
sent plots grouped by categorical vari-
ables displaying strong pattern: a.
Atmospheric pollution; b. Agricultural
practices; c. Harvesting; d. Habitat
type; e. Bark texture.

Species richness adscendens and Lecanora chlarotera). Only two species

were correlated with Axis 3 (App. 2): Lepraria incana
M n Sp was chosen to represent species richness in was associated with positive values and unburned sites,
the ordination, because it had stronger correlations than whereas Parmelia sulcata was negatively correlated
Tot Sp with axes (App. 3). It was correlated mostly with and associated with burned sites.
Axis 2 and to a minor extent on Axis 3 (Species Rich-
ness, Figs. 1 & 2 and M n Sp, Table 3). Important Ordination results: DCA
differences in species richness were detected in relation
to habitat (App. 1). In particular, plots in urban areas had As a comparison, a DCA ordination was performed on
very low Tot n sp (5), M n sp of species (4) and M LAV the same dataset (Table 4), obtaining a very similar 3-
(32). Also beechwoods and Thermophilous oakwoods dimensional solution, with Axis 1 showing r2 = 0.316,
showed low values for these parameters, whereas other followed by Axis 2 (0.113) and Axis 3 (0.109). The main
habitats showed high and comparable species richness. ecological gradients along the axes were quite similar to
the NMS analysis, though a lower proportion of variation
Lichen species abundance was displayed in the DCA ordination (total r2 = 0.538):
Axis 1 corresponded to a gradient of increasing elevation
Most of the species showed correlation (r > 0.300) and latitude and decreasing MA Temp, whereas longitude
with Axis 2 (Fig. 2a, b; App. 2). In particular, and MA Rain were correlated with Axis 2. Species rich-
Flavoparmelia caperata, Melanelia fuliginosa and ness was preferentially partitioned along Axis 2 > Axis 3 >
Parmotrema chinense showed a strong positive correla- Axis 1. Categorical factors showed similar trends to those
tion (at more humid sites farther east), whereas only observed in the NMS analysis: Agr Pract and Atm Poll
Pyrenula nitida showed a negative correlation (at drier showed gradients along Axis 1, whereas Harv was nega-
sites farther west). Fourteen species showed correlation tively correlated with Axis 2. Note that DCA Axes 1 and 3
> 0.300 with Axis 1: most of them were positively are reversed from NMS Axes 1 and 3 (i.e. high elevation
associated (e.g. Hyperphyscia adglutinata, Physcia sites have positive values on DCA Axis 1).
 - Variables influencing the distribution of epiphytic lichens in heterogeneous areas - 201

IVA

Fifty-nine species showed statistically significant

IVs (p < 0.05; IV > 20) for different substrate- and
environmental-related factors (Table 1). More than 18%
of the sampled epiphytic lichen species were indicators
of specific climatic conditions, while nearly 15% of
species were closely related to habitat. A considerable
number of them indicated effects of various anthropo-
genic pressures: especially forest fires (10.7% of the
species) and forest management (7.7%). A few species
were associated with substrate-related factors: 4.0%
were associated with bark surface and one species was
found preferentially in a particular interval of trunk
circumferences. Species associated with particular ex-
treme ecological conditions had the highest IVs: e.g.,
Hyperphyscia adglutinata indicated plots subjected to
intense agricultural practices (79.3), Lecanora chlarotera
indicated recently burnt plots (77.1) and Phaeophyscia
orbicularis was associated with bark with high water
retention (49.2). All the climatic features of the survey
area were well represented by their indicator species:
e.g., Buellia griseovirens (54.1) for cold and humid
areas and Parmotrema reticulatum (31) for warm and
humid conditions. Lastly, reliable indicator species were
found for specific habitats, such as Punctelia subrudecta
(56.8) for olive groves or Parmeliopsis ambigua for
conifer forests (51.4). Fig. 2. NMS ordination of plots based on lichen species
composition, showing weighted mean score on axis for each
species. Lengths of arrows for predictive factors represent
Table 4. DCA ordination: correlation (r Pearson) of factors strength of correlations; directions represent signs: a. Axis 1
with the three axes. Relations with positive (+), negative (–) vs Axis 2; b. Axis 1 vs Axis 3.
values of the given axis or a weak relationship (±) were
reported for categorical predictors. Note that directions of
Axes 1 and 3 are reversed from those in the NMS ordination
(Table 3). See Table 1 for explanation of SA and factor codes. Discussion
*M n Sp represents lichen species diversity for analyses.
The variability of epiphytic lichen distribution and
F Code Axis1 Axis 2 Axis 3 abundance at plot level is related to variables representing
Total axis r2 0.316 0.113 0.109 both natural environment and human disturbances in this
M n Sp* –0,136 0,452 0,385 heterogeneous Mediterranean region. Parallel applica-
S Tr Sp + ± ± tion of two different ordination methods (NMS and DCA)
Dec Ev ±
M Circ 0,143 0,137 0,1 was carried out to evaluate results, as suggested by sev-
pH - eral authors (Økland 1990; 1996; Økland & Eilertsen
Text - 1993). Congruent configurations were found, which give
Wat Ret -
Exf ± indirect indications that the main gradients of variability
EC Exp ± were detected. The three axes of the ordination showed
Long –0,075 0,292 –0,132 hierarchical relationships of the variables investigated to
Lat 0,306 0,187 –0,266
Elev 0,652 0,208 –0,127 epiphytic lichens in the survey area. The main variables
MA Rain 0,155 0,400 –0,166 involved are similar to those reported for much larger
MA Temp –0,480 –0,128 0,078 temperate areas of Europe, North America and Australia
ED Harv -
Atm Poll - ± (see e.g. Mc Cune et al. 1997; Kantvilas & Minchin
For Fir - - 1989). In several cases, the relative importance and
Agr Pract - covariation between variables was different. Explana-
EH Hab + ±
tions include the Mediterranean location of the project
202 Giordani, P.

and the geomorphological and climatic heterogeneity of montane communities of beechwoods and conifers, char-
the smaller survey area for this project. acterised by several crustose species (e.g. Scoliciosporum
umbrinum, Buellia griseovirens and several species of
Axis 1: Environment-related factors Lecanora); b) communities of mesophilous oakwoods
with a rich contingent of Parmelia-type foliose species
Axis 1 of the NMS and DCA analyses accounted for and crustose Pertusaria species and, lastly, c) warm
most of the explained variation of the dataset, correlated humid coastal communities dominated by sub-oceanic
with a temperature gradient represented by increasing species, such as Parmotrema reticulatum and Hetero-
MA Temp and decreasing Elev and Lat. Although the dermia obscurata.
importance of these factors is well-known for many
kind of organisms, the response of lichens seemed to be Axis 2: Environment-related factors
particularly strong here, related to the occurrence of
sharp geomorphological limits in the survey area (e.g. Axis 2 of both NMS and DCA analyses was associ-
several watersheds running parallel to the coast) ated with a strong gradient of species richness, positively
(Brunialti & Giordani 2003). correlated with increasing rainfall, which appears to be
Some disturbances covaried in relation to effect on the best predictive factor for epiphytic lichen diversity in
epiphytic lichens: Agr Pract, For Fir, Atm Poll and Non- the survey area. These results confirm suggestions by
forest of Harv showed overlapping gradients along Axis 1, Loppi et al. (2002) from data recently collected both on
closely linked to high MA Temp and low Elev. This is a local and national scales that, with the same level of
situation characteristic of many Mediterranean areas, due to disturbances, epiphytic lichens were far more abundant in
the high concentration of human activities along the coasts. humid than in dry areas. A preliminary study in the
It is also consistent with the widespread observation that in province of Genova, central Liguria (Giordani in press),
temperate zones human activity is higher at lower elevations. predicted a considerable increase of lichen abundance for
This probably leads to a synergistic effect on lichen distribu- MA Rain > 1200 mm/year. In the present study, a clear
tion rather than on diversity, deduced from weak associa- distinction between the dry Western Ligurian Riviera
tions of these disturbances with species richness. characterised by low species richness and the humid
A suite of species were preferentially associated with Eastern side with high species richness was definitely
multiple covarying ecological conditions, including distur- confirmed by a significant positive correlation of longi-
bances. In these cases, it was possible to weight the relative tude with Axis 2. Exceptions may occur because of 1) the
importance of covarying factors on distributional patterns effect of disturbances in humid areas and 2) particular
of these taxa, comparing IVA for significative variables: microclimatic conditions (higher humidity) in some parts
e.g. Hyperphyscia adglutinata was preferentially found in of the Western Riviera. Similar patterns of lichen abun-
burnt sites (IVA = 47.9) > low elevations (36.2) > olive dance were reported for other Mediterranean areas with
groves (32.1) > medium air pollution level (28.7). Other high environmental and geomorphologic heterogeneity
species were significantly associated with a single ecologi- (e.g. Sardinia region - Zedda 2002). IVA provided fur-
cal condition, e.g. Lecanora expallens in burnt sites (41.9). ther information in this respect, revealing a high propor-
tion of species indicating humid (both cold and warm)
Axis 1: Substrate-related factors atmospheric conditions, whereas there were no species
that indicated dry conditions. Particularly strong correla-
Significant differences in species distribution seemed tions of climatic variables are related to the unusual
to be linked to substrate-related variables. According to physiology of lichens; they depend closely on atmos-
my results, most variation due to substrate is related to pheric factors for their metabolism (Nash 1996). In par-
Axis 1, which accounted for most of the variation in ticular, saturation of the lichen thalli, directly influenced
distribution of lichen species in the survey area (Fig. 2a, by rainfall and temperature, is essential for such funda-
b). The importance of bark pH, texture and water reten- mental processes as gas exchange, nitrogen fixation and
tion has been reported previously by several authors for photosynthesis (Ahmadjian 1993).
various habitats, bioclimes and levels of geomor-
phological homogeneity (see e.g. Eversman et al. 1987; Axis 2: Anthropogenic disturbances
Kantvilas & Minchin 1989).
In this study, anthropogenic impacts had distinct ef-
Axis 1: Species distribution fects on epiphytic lichens abundance, with particular
reference to harvesting rather than air pollution, the former
Axis 1 exhibited the largest gradient of species, showing strong links with low species richness along
which reflected three main group of communities: a) Axis 2. This result may be explained by the fact that
 - Variables influencing the distribution of epiphytic lichens in heterogeneous areas - 203

anthropogenic pressures have spatial and, above all, tem- to some extent species richness are related to habitat as
poral scales of impact and lichen response which are quite defined by tree species or land use. Certain “natural”
different from the natural rates of growth (Dungan et al. habitats generally showed wide variation in species
2002) and colonization of epiphytic lichens. For instance, richness along Axis 2 related to moisture: broadleaf
substrate-related factors are usually characterized by small forest habitat groups were mostly distinguished from
spatial (from a few centimetre to several metres) and long each other and others primarily along Axis 1 (related to
temporal scales of action, years in some cases (e.g. trunk temperature and elevation), with wide variation in species
circumference ) or even constant (e.g. the tree species on richness (along Axis 2 and related to moisture) within
which lichens grow). This ecological framework is con- oak woods habitat groups. Both montane conifers and
sistent with the characteristics of epiphytic lichens, which beechwoods were strictly related to high elevation on
are long-living organisms with relatively slow growth negative values of Axis 1, but, independently from the
rates (Nimis et al. 2002). On the other hand, most of the harvesting pressure, the former are associated with high
anthropogenic sources of disturbance have different char- species richness, whereas, the latter hosted very species-
acteristics of impact and effect (instantaneous in the case poor lichen communities, probably because of different
of harvesting, usually constant and chronic in the case of substratum conditions for lichen colonization.
air pollution), but, in any case, the time needed to restore Among ‘human-altered’ habitats, non-forested rural
the original condition is significantly long. areas and untreated olive groves, seemed to have suit-
This effect is particularly evident in forest ecosys- able conditions for epiphytic lichens, reflected in high
tems, where harvesting affects lichen communities by species richness at plots (positive values on Axis 2).
means of several disturbance mechanisms, such as me- However, olive groves communities are largely com-
chanical removal of the substratum and fragmentation or posed of a rich contingent of rare species with oceanic to
loss of habitat (Saunders et al. 1991; Spence 2001; Will- suboceanic affinities, whereas non-forested rural areas
Wolf & Scheidegger 2002), which cause an increasing had high species richness but were mainly characterized
distance among suitable sites that may limit dispersal of by widespread species. Urban plots are only partially
vegetative diaspores (Esseen et al. 1996; Sillett & Mc associated with atmospheric pollution (that showed vari-
Cune 1998; Hedenås et al. 2003). Harvesting also alters ation mostly along Axis 1), but showed a prevalent
drastically the microclimatic conditions of the forest, pattern of negative values on Axis 2, corresponding to
increasing light and decreasing relative humidity within very low species richness. This result suggests that the
the site (Palmquist & Sundberg 2000; Mc Cune 2000). lack of proper habitat and substrate continuity may
Considering the large number of species indicating spe- strongly affect lichen diversity partially independently
cific levels of harvesting, monitoring the abundance and from atmospheric pollution impact. This latter hypoth-
distributional variation of these organisms would seem to esis is supported by the similar pattern of low species
be a reliable tool for exploring spatial and temporal richness at heavily harvested plots: another factor with
impact of harvesting in Mediterranean regions as has strong impact on habitat and substrate.
been done for forest continuity elsewhere (Rose 1992; The effects of atmospheric pollution and harvesting
Kuusinen 1996; Esseen et al. 1996). only partially overlap along Axis 2 of the NMS analysis.
This result may be explained by the characteristics of
Axis 1 and Axis 2: Interactions among factors the study area: forests cover more than 60% of the
region and the two disturbances rarely act together, as
It is noteworthy that the gradients found for substrate- harvesting practices are mainly segregated to non-pol-
related factors in this study were closely related to the luted areas. Based on a subset of the present data,
distribution of particular tree species along the strong Giordani (In press) showed that in Liguria major atmos-
temperature gradient correlated with Axis 1: e.g. Fagus pheric pollutants were the predominant influencing fac-
sylvatica, Castanea sativa and Quercus pubescens at tors both in urban and rural non-forested areas, whereas
the same time partitioned a gradient from cool upper harvesting was by far the most important factor in
altitudes to warm lowlands and a gradient from smooth forested areas. Nevertheless, the question as to whether
to very rough bark. On the basis of this plot-level the influence of atmospheric pollution on epiphytic
dataset, it was difficult to discern the relative impor- lichens is more significant than that of harvesting can
tance of these factors, which might be clarified by hardly be generalised. Other authors report different
forthcoming investigations at tree level. Nevertheless, results from other and more geomorphologically homo-
several species were significantly associated with par- geneous regions (e.g. Poland - Kapusta et al. 2004),
ticular categories of substrate-related factors when ana- where one can assume considerable long-distance trans-
lysed with IVA (Table 1). port of pollutants. This is, on the contrary, very limited
Relevant differences both in species distribution and in Liguria.
204 Giordani, P.

Axis 1 and Axis 2: Spatial variability of epiphytic on lichen diversity at plot level. Elevation, mean annual
lichen abundance and distribution temperature and latitude were the main factors influenc-
ing epiphytic lichen distribution in Liguria, together with
This paper confirms that in heterogeneous Mediter- disturbances (such as atmospheric pollution, forest fires
ranean areas relevant differences in epiphytic lichen and agricultural practices) and habitat heterogeneity that
abundance may be also observed on a fine (regional or covary along the strongest gradient (Axis 1 of ordinations)
subregional) scale, since Long, Lat and Elev are closely of lichen community composition. Lichen species rich-
correlated with the main axes of variability (relevant ness was more directly associated with a secondary com-
variation of species richness up to 30% were detected position gradient (Axis 2 of ordinations). This response
for 8 km differences in Lat and Long, within the same variable was positively associated with mean annual rain-
habitat categories, as previously suggested by Ferretti et fall and longitude, negatively associated with harvesting
al. 2004). Furthermore, they are indirect variables for and positively associated, though weakly, with the occur-
macroclimatic factors and they also reflect the rence of past forest fires (these burnt sites were character-
geomorphological heterogeneity and consequently high ized by recolonisation processes).
habitat diversity of the area. IVA analysis allowed selection of subsets of species
as indicators of different ecological situations: many
Axis 3: The effect of fires species were strongly associated with a defined ecologi-
cal condition (e.g. Schismatomma decolorans in olive
Although it only accounts for a minor percentage of groves). For species showing significant indicator val-
variability, Axis 3 may be tentatively linked to a gradient ues for multiple factors (e.g. Hyperphyscia adglutinata),
of species richness, with more species found at recently it was possible to weight the relative importance of the
burnt sites. Fire is a characteristic disturbance of Mediter- covarying factors.
ranean areas; it affects epiphytic lichens directly and The study area has high heterogeneity, and, conse-
instantaneously, both destroying the organism and modi- quently, many factors varying across the study region.
fying the chemical-physical characteristics of the substrate. This study offers a model for understanding lichen
A subset of pioneer species is able to colonize altered response related to the ecosystem as a whole. As a
substrata some years after the fire, and may quickly consequence of the variablility included in this study, it
account for a high diversity. The subset of species most provides a framework generalizable to other Mediterra-
strongly correlated with Axis 3 largely corresponds to nean regions, including those cases where a minor
those indicated for other Mediterranean regions as facili- number of prevailing factors occur (e.g. in very arid
tated by frequent fires (Longán et al. 1999). natural areas or in intensive agricultural sites).
The standard sampling protocol I used minimizes
Weakly correlated variables variability at tree level and facilitates comparison with
other monitoring studies using the same protocol now
Some of the variables investigated seemed to have a and in the future, at the cost of limiting the number of
minor influence on epiphytic lichen in the survey area. suitable trees selected for each plot and therefore statis-
The low correlation of slope Exp with compositional tical robustness of data for within-plot investigations.
gradients may be due to the variability of canopy cover- Several recommendations can be made for future
age in the sampled plots, probably a more important studies:
microclimatic factor. For other variables (e.g. Exf and 1. IVA was found to be a good tool for assessing the
M Circ), the possible effect on lichen species diversity ecological characteristics of lichen species in het-
and composition is more easily investigated at tree-level erogeneous areas and should be preferred to expert-
and it probably depends on more local factors. Giordani assessed indicators (e.g. Nimis 2003), that lack the
et al. (2001) showed that lichen diversity in Ligurian sample-based approach and may overlook local dis-
oliveyards was independent of the circumference of the tributional and ecological variability. The IVA ap-
trunk, although this variable affected the rate of succes- proach, on the other hand, is difficult to generalise
sion of communities. for non-sampled areas.
2. This study confirms the need to develop ad hoc inter-
pretation scales for lichen monitoring of the effect of
Conclusive comments and issues for forthcoming atmospheric pollution (see e.g. Asta et al. 2002) in
studies areas with different amounts of rainfall, as recently
proposed by several authors (Loppi et al. 2002).
This paper provides a hierarchical evaluation of the 3. More detailed investigation including project tree-
effects of substrate- and environmental-related variables level data will clarify the spatial and temporal range
 - Variables influencing the distribution of epiphytic lichens in heterogeneous areas - 205

of response of epiphytic lichens to environment- Degelius, G. 1935. Das ozeanische element der Strauch-und
related variables (including atmospheric humidity), Laubflechtenflora von Skandinavien. Acta Phytogeogr. Suec.
and their relative importance on macro- vs. meso- 7: 1-411.
and microscales in the study area. A more detailed Dufrêne, M. & Legendre, P. 1997. Species assemblages and
indicator species: the need for a flexible asymmetrical
investigation of tree level data at sites with more
approach. Ecol. Monogr. 67: 345-366.
than one tree species might also clarify better the Dungan, J.L., Perry, J.N., Dale, M.R.T., Legendre, P., Citron-
relative importance of substrate- vs. environment- Pousty, S., Fortin, M.-J., Jakomulska, A., Miriti, M. &
related factors, Other factors, e.g. intra- and Rosenberg, M.S. 2002. A balanced view of scale in spatial
interspecific competition and effect of light prob- statistical analysis. Ecography 25: 626-640.
ably also affect epiphytic lichen distribution and Esseen, P.-A., Renhorn, K.-E. & Pettersson, R.B. 1996. Epiphytic
abundance. Much of the unexplained variation in my lichen biomass in managed and old-growth boreal forests:
analyses might depend on these factors, that must be effect of branch quality. Ecol. Appl. 6: 228-238.
investigated at tree level. Eversman, S., Johnson, C. & Gustafson, D. 1987. Vertical
distribution of epiphytic lichens on three tree species in
Yellowstone National Park. Bryologist 90: 212-216.
Ferretti, M., Brambilla, E., Brunialti, G., Fornasier, F., Mazzali,
Acknowledgements. This study was funded by the University C., Giordani, P. & Nimis, P.L. 2004. Reliability of different
of Genoa with the research grant ‘Lichens as biomonitors of sampling densities for estimating and mapping lichen diver-
environmental alteration and naturality: standardization in sity in biomonitoring studies. Environ. Pollut. 127: 249-
Mediterranean areas’. My thanks to Giorgio Brunialti for 256.
stimulating discussions and to Susan Will-Wolf and two anony- Fos, S. 1998. Líquenes epífitos de los Alcornocales Ibéricos.
mous referees for important suggestions. Correlaciones bioclimáticas, anatómicas y densimétricas
con el corcho de reproducción. Guineana 4: 1-507.
Galun, M. (ed.) 1988. CRC Handbook of lichenology. Vol. II.
References CRC Press, Boca Raton, FL, US.
Garty, J. 1992. The postfire recovery of rock-inhabiting algae,
Anon. 1999. Piano di risanamento e tutela della qualità dell’aria. microfungi, and lichens. Can. J. Bot. 70: 301-312.
Technical report. Regione Liguria, Genova. IT. Giordani, P. In press. Is the diversity of epiphytic lichens a
Anon. 2001a. STATISTICA (sistema software di analisi dei reliable indicator of air pollution? A case study from Italy.
dati), versione 6. www.statsoft.it Environ. Pollut.
Anon. 2001b. Carta delle aree percorse dal fuoco – anno 1996/ Giordani, P., Brunialti, G. & Modenesi, P. 2001. Applicability
2001. Technical report. Regione Liguria, Genova, IT. of the Lichen Biodiversity method (LB) in a mediterranean
Anon. 2003a. Piano regionale di previsione, prevenzione e lotta area (Liguria, NW Italy). Cryptog. Mycol. 22: 193-208.
attiva contro gli incendi boschivi. Technical report. Liguria Guisan, A. & Zimmermann, N.E. 2000. Predictive habitat dis-
Regional Council, Erga edizioni, Genova, IT. tribution models in ecology. Ecol. Model. 135: 147-186.
Anon. 2003b. Ecozero. Banca dati ambientale cliamtologica. Hawksworth, D.L. & Rose, L. 1970. Qualitative scale for
(http://ecozero.liguriainrete.it/ecozero). Liguria Regional extimating sulphur dioxide air pollution in England and
Council, Erga edizioni, Genova, IT. Wales using epiphytic lichens. Nature 227: 145-148.
Ahmadjian, V. 1993. The lichen symbiosis. Wiley, New York, Hedenås, H., Bolyukh, V.O. & Jonsson, B.G. 2003. Spatial
NY, US. distribution of epiphytes on Populus tremula in relation to
Aptroot, A. & Berg, M.P. 2004. Collembola help lichens in dispersal mode. J. Veg. Sci. 14: 233-242
competition with algae. Lichenologist 36: 167-169. Hilitzer, A. 1925. Étude sur la végetation épiphyte de la Bohême.
Asta, J., Erhardt, W., Ferretti, M., Fornasier, F., Kirschbaum, Publ. Fac. Sci. Univ. Charles Prague Cislo 41: 1-200.
U., Nimis, P.L., Purvis, O.W., Pirintsos, S., Scheidegger, Hill, M.O. & Gauch, H.G. 1980. Detrended correspondence
C., Van Haluwyn, C. & Wirth, V. 2002. Mapping lichen analysis: an improved ordination technique. Vegetatio 42:
diversity as an indicator of environmental quality. In: Nimis, 47-58.
P.L., Scheidegger, C. & Wolseley P. (eds.) Monitoring with Kantvilas, G. & Minchin, P.R. 1989. An analysis of epiphytic
lichens – Monitoring lichens, pp. 273-279. Kluwer, lichen communities in Tasmanian cool temperate rainfor-
Dordrecht, NL. est. Vegetatio 84: 99-112.
Austin, M.P. 1980. Searching for a model for use in vegetation Kapusta, P., Szarek-Lukaszewska, G. & Kiszka, J. 2004. Spatial
analysis. Vegetatio 42: 11-21. analysis of lichen species richness in a disturbed ecosystem
Austin, M.P. & Smith, T.M. 1989. A new model for the con- (Niepolomice Forest, S Poland). Lichenologist 36: 249-
tinuum concept. Vegetatio 83: 35-47. 260.
Barkman, J.J. 1958. Phytosociology and ecology of crypto- Kershaw, K.A. 1985. Physiological ecology of lichens. Cam-
gamic Epiphytes. Van Gorcum, Assen, NL. bridge University Press, Cambridge, UK.
Brunialti, G. & Giordani, P. 2003. Variability of lichen diversity Kruskal, J.B. 1964. Nonmetric multidimensional scaling: a
in a climatically heterogeneous area (Liguria, NW Italy). numerical method. Psychometrika 29: 115-129.
Lichenologist 35: 55-69. Kuusinen, M. 1996. Cyanobacterial macrolichens on Populus
206 Giordani, P.

tremula as indicators of forest continuity in Finland. Biol. Hawksworth, D.L. & Bailey, R.H. (eds.) Lichenology:
Conserv. 75: 43-49. Progress and problems, pp. 278-307. Academic Press,
Lang, G.E., Reiners, W.A. & Pike, L.H. 1980. Structure and London, UK.
biomass dynamics of epiphytic lichen communities of bal- Rose, F. 1992. Temperate forest management: its effect on
sam fir forests in New Hampshire. Ecology 61: 541-550. bryophyte and lichen floras and habitats. In: Bates, J.W. &
Levins, R. 1966. Strategy of model building in population Farmer, A.M. (eds.) Bryophytes and lichens in a changing
biology. Am. Sci. 54: 421-431. environment, pp. 211-233. University Press, Oxford, UK.
Longán, A., Gaya, E. & Gómez-Bolea, A. 1999. Post-fire Rundel, P.W. 1988. Water relation. In: Galun, M. (ed.) CRC
colonization of a Mediterranean forest stand by epiphytic Handbook of lichenology. Vol. II, pp. 17-36. CRC Press,
lichens. Lichenologist 31: 389-395. Boca Raton, FL, US.
Loppi, S. & De Dominicis, V. 1996. Effects of agriculture on Saipunkaew, W., Wolseley, P.A. & Chimonoides, P.J. 2005.
epiphytic lichen vegetation in central Italy. Isr. J. Plant Sci. Epiphytic lichens as indicators of environmental health in
44: 297-307. the vicinity of Chiang Mai city, Thailand. Lichenologist 37:
Loppi, S., Giordani, P., Brunialti, G., Isocrono, D. & Piervittori, 345-356.
R. 2002. Identifying deviations from naturality of lichen Saunders, D.A., Hobbs, R.J. & Margules, C.R. 1991. Biological
diversity for bioindication purposes. In: Nimis, P.L., consequences of ecosystem fragmentation. A review.
Scheidegger, C. & Wolseley P. (eds.) Monitoring with Conserv. Biol. 5: 18-32.
lichens – Monitoring lichens, pp. 281-284. Kluwer, Seaward, M.R.D. (ed.) 1977. Lichen ecology. Academic Press,
Dordrecht, NL. London, UK.
McCune, B. 2000. Lichen communities as indicators of forest Shepard, R.N. 1962a. The analysis of proximities: Multidimen-
health. Bryologist 103: 353-356. sional scaling with an unknown distance function. I.
McCune, B. & Mefford, M.J. 1999. Multivariate analysis of Psychometrika 27: 125-139.
ecological data. Version 4.25. MjM Software, Gleneden Shepard, R.N. 1962b. The analysis of proximities: Multidimen-
Beach, OR, US. sional scaling with an unknown distance function. II.
McCune, B., Dey, J.D., Peck, J.E., Cassel, D., Heiman, K., Will- Psychometrika 27: 219-246.
Wolf, S. & Neitlich, P. 1997. Repeatability of community Sillett, S.C. & McCune, B. 1998. Survival and growth of
data: species richness versus gradient scores in large-scale cyanolichen transplants in Douglas-fir forest canopies.
lichen studies. Bryologist 100: 40-46. Bryologist 101: 20-31.
McCune, B., Grace, J.B. & Urban, D.L. 2002. Analysis of Spence, J.R. 2001. The new boreal forestry: adjusting timber
ecological communities. MjM Software Gleneden Beach, management to accomodate biodiversity. Trends Ecol. Evol.
OR, US. 16: 591-593.
Nash III, T.H. (ed.) 1996. Lichen biology. Cambridge Univer- van Dobben, H.F., Wolterbeek, H.T., Wamelink, G.W.W. & ter
sity Press, Cambridge, UK. Braak, C.J.F. 2001. Relationship between epiphytic lichens,
Nimis, P.L. 2003. Checklist of the Lichens of Italy 3.0. Univer- trace elements and gaseous atmospheric pollutants. Environ.
sity of Trieste, Dept. of Biology, IN3.0/2 (http:// Pollut. 112: 163-169.
dbiodbs.univ.trieste.it/). van Herk, C.M., Aptroot, A. & van Dobben, H.F. 2002. Long-
Nimis, P.L., Scheidegger, C., Wolseley, P. (eds.) 2002. Moni- term monitoring in the Netherlands suggests that lichens
toring with lichens – Monitoring lichens. Kluwer, Dor- respond to global warming. Lichenologist 34: 141-154.
drecht, UK. Will-Wolf, S. & Scheidegger, C. 2002. Monitoring lichen di-
Økland, R.H. 1990. Vegetation ecology: theory, methods and versity and ecosystem function. An introduction. In: Nimis,
applications with reference to Fennoscandia. Sommerfeltia P.L., Scheidegger, C. & Wolseley P. (eds.) Monitoring with
2: 1-224. lichens – Monitoring lichens, pp. 143-145. Kluwer,
Økland, R.H. 1992. Studies in SE Fennoscandian mires: rel- Dordrecht, NL.
evance to ecological theory. J. Veg. Sci. 3: 279-284. Will-Wolf, S., Scheidegger, C. & McCune, B. 2002. Methods
Økland, R.H. 1996. Are ordination and constrained ordination for monitoring biodiversity and ecosystem function. Moni-
alternative or complementary strategies in general ecologi- toring scenarios, sampling strategies and data quality. In:
cal studies? J. Veg. Sci. 7: 289-292. Nimis, P.L., Scheidegger, C. & Wolseley, P. (eds.) Moni-
Økland, R.H. & Bendiksen, E. 1985. The vegetation of the toring with lichens – Monitoring lichens, pp. 147-162.
forest-alpine transition in the Grunningsdalen area, Telemark, Kluwer, Dordrecht, NL.
SE Norway. Sommerfeltia 2: 1-224. Zedda, L. 2002. The epiphytic lichens on Quercus in Sardinia
Økland, R.H. & Eilertsen, O. 1993. Vegetation-environment (Italy) and their value as ecological indicators. Englera 24:
relationship of boreal coniferous forests in the Solhomfjell 1-457.
area, Gjerstad, S Norway. Sommerfeltia 16: 1-254.
Palmquist, K. & Sundberg, B. 2000. Light use efficiency of dry Received 10 January 2005;
matter gain in five macro-lichens: relative impact of Accepted 4 January 2006.
microclimate conditions and species-specific traits. Plant Co-ordinating Editor: S. Will-Wolf.
Cell Environ. 23: 1-14.
Rose, F. 1976. Lichenological indicators of age and environ- For Apps. 1 - 3, see JVS/AVS Electronic Archives;
mental continuity in woodlands. In: Brown, D.H., www.opuluspress.se/