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Forests 2021, 12, 27. https://doi.org/10.3390/f12010027 www.mdpi.com/journal/forests
Article
The Reproductive Strategy as an Important Trait for the
Distribution of Lower-Trunk Epiphytic Lichens in Old-Growth
vs. Non-Old Growth Forests
Giorgio Brunialti
1,
*, Paolo Giordani
2
, Sonia Ravera
3
and Luisa Frati
1
1
TerraData Environmetrics, Spin-Off Company of the University of Siena,
58025 Monterotondo Marittimo, Italy; frati@terradata.it
2
DIFAR, University of Genova, 16148 Genova, Italy; giordani@difar.unige.it
3
STEBICEF, University of Palermo, 90128 Palermo, Italy; sonia.ravera@unipa.it
* Correspondence: brunialti@terradata.it
Abstract: (1) Research Highlights: The work studied the beta diversity patterns of epiphytic lichens
as a function of their reproductive strategies in old-growth and non-old growth forests from the
Mediterranean area. (2) Background and Objectives: The reproductive strategies of lichens can drive
the dispersal and distribution of species assemblages in forest ecosystems. To further investigate
this issue, we analyzed data on epiphytic lichen diversity collected from old-growth and non-old
growth forest sites (36 plots) located in Cilento National Park (South Italy). Our working hypothesis
was that the dispersal abilities due to the different reproductive strategies drove species beta diver-
sity depending on forest age and continuity. We expected a high turnover for sexually reproducing
species and high nestedness for vegetative ones. We also considered the relationship between forest
continuity and beta diversity in terms of species rarity. (3) Materials and Methods: we used the
Bray–Curtis index of dissimilarity to partition lichen diversity into two components of beta diversity
for different subsets (type of forest, reproductive strategy, and species rarity). (4) Results: The two
forest types shared most of the common species and did not show significant differences in alpha
and gamma diversity. The turnover of specific abundance was the main component of beta diver-
sity, and was significantly greater for sexually reproducing species as compared to vegetative ones.
These latter species had also the least turnover and greater nestedness in old-growth forests. Rare
species showed higher turnover than common ones. (5) Conclusions: Our results suggest that sex-
ually reproducing lichen species always have high turnover, while vegetative species tend to form
nested assemblages, especially in old-growth forests. The rarity level contributes to the species turn-
over in lichen communities. Contrary to what one might expect, the differences between old-growth
and non-old growth forests are not strong.
Keywords: sexual reproduction; vegetative propagules; forest management; functional traits; beta
diversity
1. Introduction
Reproductive strategies widely affect the species distribution of vascular plants, bry-
ophytes, and lichens. A tradeoff between dispersion and establishment abilities is the key
to the success of most of the species of plants. Relying on different dispersal vectors such
as wind, water, or animals, vascular plants have evolved a broad range of dispersal modes
or strategies [1,2], using generative (such as spores, seeds, or fruits) and vegetative (such
as fragments of stems, stolons, rhizomes, or bulbils) diaspores [3].
Lichens are symbiotic organisms in which fungi and algae and/or cyanobacteria form
an intimate biological union [4] and both partners must be present for their successful
reproduction and dispersal [5]. Lichen propagules (diaspores) contain cells from both
Citation: Brunialti, G.; Giordani, P.;
Ravera, S.; Frati, L. The
Reproductive Strategy as an
Important Trait for the Distribution
of Lower-Trunk Epiphytic Lichens
in Old-Growth vs. Non-Old Growth
Forests. Forests 2021, 12, 27.
https://doi.org/10.3390/f12010027
Received: 11 November 2020
Accepted: 24 December 2020
Published: 28 December 2020
Publisher’s Note: MDPI stays neu-
tral with regard to jurisdictional
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Copyright: © 2020 by the authors.
Licensee MDPI, Basel, Switzerland.
This article is an open access article
distributed under the terms and con-
ditions of the Creative Commons At-
tribution (CC BY) license (http://cre-
ativecommons.org/licenses/by/4.0/).
Forests 2021, 12, 27 2 of 13
partners and represent an essential evolutive solution to this problem [6]. This vegetative
reproduction grants a reasonable survival rate and success for the establishment of new
lichen thalli [7]. Still, it is characterized by a low dispersal ability [8]. Some authors have
shown that diaspores usually have a dispersal range of about 10–100 m for Lobaria pulmo-
naria [9–12], and up to 30 m for Evernia prunastri, Ramalina farinacea [13], and Hypogymnia
physodes [14].
Sexual reproduction in lichens only involves the mycobiont partner, through spore
production and propagation. To germinate and give rise to a new individual, the spore
must find a compatible photosynthetic partner on a suitable substrate to colonize [4]. Sex-
ual spores are generally smaller than vegetative structures and they are also actively dis-
charged (except those of Caliciales), so they are likely to be dispersed over longer distances
[6]. Further, this propagation form allows the genetic turnover of the populations, which
is extremely important for adaptation to environmental changes [15]. For example, even
in the hostile environments of Antarctica, Seymour et al. [6] reported that many lichens
produced sexual structures, often in abundance.
In forest ecosystems, the distribution of lichen species is driven both by landscape
and stand-level factors [16–19]. In this paper we focus on these latter aspects. In particular,
the structural characteristics of the stand (e.g., basal area, tree height) and the availability
of tree substrates suitable for lichen colonization (e.g., old trees) and of micro-habitats can
be the main limiting factors conditioning the most appropriate reproductive strategies to
obtain better species dispersal abilities [16–19].
So far, most studies have focused on the effect of reproductive strategies on the dis-
persal ability and distribution of species assemblages (see e.g., [18]) or on single forest-
dwelling species (see e.g., the studies on the umbrella and flagship species Lobaria pulmo-
naria; [11,12,19]). Only a few papers have explored this issue in terms of beta diversity and
species turnover [20]. Furthermore, no previous study, to our knowledge, has addressed
the topic comparing what happens to lichen communities in old-growth (hereafter OG)
and non-old growth (NOG) forests, especially in Mediterranean oak and beech forests.
In the present study, we assess the hypothesis that the dispersal abilities for to the
different reproductive strategies drive the species turnover and nestedness (beta diver-
sity) depending on forest age and continuity. To address this question, we used the data
from a study on epiphytic lichen diversity carried out in OG and NOG forest stands in a
national park in Southern Italy [21,22].
The details of the study hypothesis are illustrated in Figure 1, where possible patterns
of species dispersion with different reproductive strategies in OG and NOG forests are
reported. We expect sexually reproducing species to be characterized by a high turnover
regardless of forest type (Figure 1b,d). This hypothesis is based on the observation that
spores have a potentially very high spatial range of dispersion, but, at the same time, they
may encounter more difficulties than vegetative species in the formation and establish-
ment of new thalli. These biological characteristics would lead to strong discontinuities
(turnover) in the floristic compositions of the various sites. On the other hand, we hypoth-
esize that the beta diversity of vegetative species is mainly determined by a high nested-
ness between sites of the same forest types and that this pattern is more evident in OG
forests than in NOG ones (Figure 1a,c). This assumption is based on the fact that vegeta-
tive species are particularly favored in the colonization of contiguous sites which would
tend to host a similar set of species, especially in conditions of ecological continuity such
as those found in OG forests.
Additionally, we also considered the relationship between forest continuity and li-
chen beta diversity in terms of species rarity. Since diversity may be influenced by disper-
sal ability, we expect that rare species spread more easily in OG forests.
Forests 2021, 12, 27 3 of 13
Figure 1. Schematic representation of the hypotheses tested in the study on the beta diversity pat-
terns of lichen species with contrasting reproductive strategies in old-growth (OG) and non-old
growth (NOG) forests. The squares represent the areas with different types of forest. We report the
possible dispersion flows (arrows) of the different species (colors) between sites (circles) that de-
termine the colonization and are the basis of the potential compositional differences: (a) vegetative
species in OG forests; (b) sexual species in OG forests; (c) vegetative species in NOG forests; (d)
sexual species in NOG forests.
Old-growth forests
Vegetative species
High nestedness throughout the area
Sexual species
High turnover throughout the area
Non-Old-growth forests
Vegetative species
High nestedness within clusters
Sexual species
High turnover throughout the area
Site colonized by species «red», «green», «blue» and «yellow»
Unsuitable site with no lichens
Dispersion of species «red»
a) b)
c) d)
Forests 2021, 12, 27 4 of 13
2. Materials and Methods
We analyzed lichen diversity data collected within a long-term monitoring project fo-
cused on old-growth forests of The Cilento, Vallo di Diano e Alburni National Park, in
Southern Italy (see the results here: [21–26])
2.1. Study Area
The Cilento, Vallo di Diano e Alburni National Park extends over 181,000 ha, stretch-
ing between the Tyrrhenian coast and the margin of the Lucania mountains, in the Cam-
pania Region (southern Italy). This study was carried out in the interior forest habitats,
from 300 to 1696 m, in a survey area of 30 × 42 km (Figure 2). The hilly substrates mainly
develop on flysch formations; the inner mountains are carbonate massifs predominantly
constituted by carbonate and dolostone [27]. Native forests are mostly represented by tur-
key oak (Quercus cerris L.) woodlands of the hilly and sub-montane belts (from 450 to 850
m in altitude), mesophilous mixed forests dominated by turkey oak mostly on the north-
facing slopes (between 800 and 1000 m in altitude), and beech (Fagus sylvatica L.) wood-
lands (thermophilous and microthermal coenoses) in upland areas. Chestnut (Castanea sa-
tiva Mill.) coppices and holm oak (Quercus ilex L.) woods are less common. In this area,
bioclimatic characteristics range from Mediterranean to temperate with a cooler and more
humid climate, and inland areas are usually subject to a temperature lower than 10 °C for
three months per year. Rainfall increases along with altitude from 730 to 1700 mm year
−1
.
2.2. Sampling Design
Thirty-six plots (50 × 50 m) were randomly selected, taking into account structural
attributes, “old-growths”, and forest types, in proportion to their area within the park
(Figure 2). They represented a sub-sample of the 132 sites investigated during a prelimi-
nary extensive survey on forest structural attributes (systematic survey, grid dimension
500 m; see [28]). The selected plots were classified as old-growth (OG) or non-old growth
(NOG) forests according to their structural attributes. In particular, OG stands were con-
sidered to be structurally more heterogeneous than younger ones in relation to the follow-
ing criteria: (1) the presence of OG individual trees (individuals with DBH >50 cm); (2)
weak or no human disturbance; (3) multi-layered canopy; (4) large volumes of standing
and fallen deadwood; and (5) decaying ancient and veteran trees (standing dead trees).
OG forest sites significantly differed (Wilcoxon test, p < 0.05) from NOG forests with re-
gard to higher tree circumference (median: 113 vs. 72 cm), number of diameter classes
(median: 11 vs. 9), and volume of fallen deadwood (median: 1.394 vs. 0.0 vol ha
−1
). The
other structural variables were similar between the two forest types (Table 1).
The sampling plots represented overall five forest types as follows: (1) beech wood-
lands (10 NOG, 7 OG plots); (2) turkey oak woodlands (7 NOG, 4 OG plots); (3) mixed
broadleaf forests (2 NOG, 2 OG plots); (4) chestnuts woods (2 NOG plots); and (5) holm
oak woods (2 OG plots). The dominant tree species of each forest type were considered as
tree substrate for lichen sampling. In each plot, three sampling trees were considered
within one randomly selected circular sub-plot (7-m radius). In mixed broadleaf forests
we sampled different tree species (Alnus cordata (Loisel.) Desf., Quercus pubescens Willd.,
Q. cerris, and C. sativa). OG and NOG stands showed moderate differences in the propor-
tion of the sampled tree species composition, with a predominance of beech and turkey
oak, as well as seven less frequent tree species (see Table S1).
Forests 2021, 12, 27 5 of 13
Figure 2. Study area: Cilento National Park (South Italy), with 36 sampling plots.
Table 1. Descriptive statistics of the structural variables included in the models. Results of the
Wilcoxon test performed for the two forest types are also reported. n.s.: not significant (p > 0.05).
Structural Variables Abbr.
OG (
n
:15)
NOG (
n
:21)
Wilcoxon Test
(df:1; n:36)
Median
Min–Max
Median
Min–Max
Tree circumference (cm)
TC
113
38–226
72
45–182
W = 219.5, p < 0.05
Diameter classes number (n)
DCN
11
3–15
9
4–15
W = 221.5, p < 0.05
Number of old trees (n)
OT
7
0–28
1
0–20
W = 213, n.s.
Basal area (m
2
ha
−1
)
BA
28.0
7.5–48.9
23.4
3.5–44.4
W = 208, n.s.
Standing deadwood (vol ha
−1
)
SDW
0.271
0–1.179
0.0
0.0–10.242
W = 162, n.s.
Fallen deadwood (vol ha
−1
)
FDW
1.394
0–4.823
0.0
0.0–3.723
W = 256, p < 0.001
Tree Species Richness (n) TSRich
3 1–7 3 1–6 W = 176.5, n.s.
Number of trees (n)
NT
132
56–365
125
50–271
W = 163, n.s.
2.3. Lichen Sampling
To assess epiphytic lichen diversity, on the three trees with a DBH >16 cm and bole
inclination <30° closest to the center of each plot, the abundance of each lichen species was
recorded on the bole, from 0 to 2 m. According to Tallent-Halsell [29], an abundance score
Forests 2021, 12, 27 6 of 13
was assigned to each species in relation to its frequency on the recording area: (1) rare =
1–3 thalli in the area; (2) uncommon = 4–10 thalli in the area; (3) common = >10 thalli in
area but less than 50% of the considered substrate; and (4) abundant = more than 50% of
the considered substrate. In total, 106 trees were sampled.
Nomenclature and author’s abbreviations follow Species Fungorum (www.spe-
ciesfungorum.org). Dominant reproductive strategy (sexual vs. vegetative) and status fol-
low Nimis [30]. In particular, (1) the rarity of each taxon was obtained using commonness-
rarity values calculated for two phytoclimatic units: montane and humid sub-Mediterra-
nean Italy, and (2) threat assessment was performed according to Nascimbene et al. [31].
2.4. Reproductive Strategies in Lichens
Lichens are able to reproduce both sexually and asexually. Sexual reproduction is
carried out through sexual spores of the mycobiont reproducing the fungus alone. Vege-
tative reproduction is carried out through various types of propagules (e.g., conidia, thal-
lus fragments, schizidia, lobules, isidia, soredia). Among them, (1) soredia are more or less
granular aggregations of hyphal and algal cells ranging from 20 to 100 µm in diameter or
more, and (2) isidia are small thallus outgrowths with varied morphology (e.g., cylindri-
cal, clavate, coralloid) containing both symbionts [6,7]. In this work, we define “sexual
species” as those species that reproduce mainly sexually through ascospores and “vege-
tative species” as those that reproduce mainly through vegetative diaspores. Among these
latter, we only considered the most representative ones, namely soredia and isidia, while
we did not take into account other less frequent types of propagules, such as conidia, thal-
lus fragments, schizidia, and lobules.
2.5. Data Analysis
The Wilcoxon signed-rank non-parametric test has been used for pairwise compari-
sons among the two types of forest management, OG and NOG.
The beta diversity between site pairs was calculated based on the abundance matrices
of the lichen species in the sites following the framework proposed by Baselga [32]. This
approach is based on the use of Bray–Curtis dissimilarity and breaks down beta diversity
into two components: (1) balanced variation in abundance, accounting for the individuals
of some species in one site that are substituted by the same number of individuals of dif-
ferent species in another site (hereafter “turnover”); and (2) abundance gradients,
whereby some individuals are lost from one site to the other (hereafter “nestedness”).
To compare the diversity components observed in the different conditions investi-
gated, the beta diversity was calculated for different subsets concerning the type of forest
management of the sites (OG vs. NOG), the reproductive strategy (sexual vs. vegetative),
and the status of national rarity (common vs. rare) of the species.
Calculations of beta diversity were performed using the vegan [33], ecodist [34] and
betapart [35] packages in R environment [36].
3. Results
3.1. The Lichen Biota in the Study Area
In total, 148 lichen species were found in the 106 sampled trees (see Table S2): 89
species with sexual reproduction (60%) and 59 with vegetative reproduction (40%). Of the
latter, 43 were sorediate and 16 were isidiate species. Most of the species (106 out of 148)
were present in under 20% of the plots, with 34 species (23%) distributed in only one plot,
while 16 lichens were present in more than 50% of the plots. Most of the lichens were
nationally rare (92 species, 62%; 47 rare and 45 very rare), while common lichens repre-
sented 38% of the species pool (56 species; 42 common and 14 very common). Fifteen per-
cent (22 species) of the floristic list was represented by lichens included in the Italian Red
List: one Endangered species (Alyxoria ochrocheila), 4 Vulnerable species (Agonimia allobata,
Solitaria chrysophthalma, Sticta limbata, Vahliella saubinetii), 11 Near-Threatened species
Forests 2021, 12, 27 7 of 13
(Arthopyrenia salicis, Buellia disciformis, Caloplaca herbidella, Diarthonis spadicea, Lobarina scro-
biculata, Nephroma resupinatum, Pachyphiale carneola, Pectenia plumbea, Ricasolia amplis-
sima—chloromorph, Ricasolia amplissima—cyanomorph, Schismatomma ricasolii), 4 Least
Concern species (Gyalecta liguriensis, Lobaria pulmonaria, Parmeliella testacea, Ramalina sub-
geniculata), and two Data-Deficient species (Lepra slesvicensis, Ochrolechia dalmatica)
3.2. Comparison between OG and NOG Forest Stands
With the exception of the species occurring in only one plot, OG and NOG stands
shared most of the common species detected in the study area (83% of the vegetative spe-
cies and 83% of the sexual ones) and also a significant part of the rare species (58% and
71%, respectively). Further, rare species (both vegetative and sexual) were more exclusive
than common ones, above all in NOG stands where they represented more than 20% of
the species (Figure 3).
Figure 3. Schematic representation of shared and exclusive species in the OG and NOG forests of the study area (dataset
without the species occurring only in a single plot, 34 species). The definition of “common” or “rare” species follows their
commonness–rarity values in montane and humid sub-Mediterranean Italy (Nimis 2016).
Forests 2021, 12, 27 8 of 13
In terms of both alpha and gamma diversity, OG and NOG forest sites did not show
statistically significant differences for any combination of groups of species considered
(rare vs. common, vegetative vs. sexual) (Table 2, Wilcoxon test, p > 0.05).
Table 2. Descriptive statistics of lichen species richness: alpha diversity (average number of species on each tree within a
plot) and gamma diversity (average overall number of species within a plot). Results of the Wilcoxon test performed for
the two groups of plots are also reported. n.s.: not significant (p > 0.05).
Alpha Diversity OG (n:15) NOG (n:21) Wilcoxon Test
(df:1; n:36)
Median
Min–Max
Median
Min–Max
Common species
Sexual species 5 1–11.7 6.3 3.3–9.3 W = 116, n.s.
Vegetative species 6 0–9.7 5.7 3–10.3 W = 129, n.s.
Rare species
Sexual species 5 2.7–8.7 4 1–7 W = 215.5, n.s.
Vegetative species
2
0–6
2
0–6.7
W = 150, n.s.
Gamma Diversity
Common species
Sexual species 7 0–14 9 3–15 W = 126, n.s.
Vegetative species 8 2–18 10 4–15 W = 120, n.s.
Rare species
Sexual species 3 0–10 3 0–14 W = 155.5, n.s.
Vegetative species
8
3–14
7
1–11
W = 199, n.s.
3.3. Beta Diversity within OG and NOG Forest Stands
In all cases considered the turnover of specific abundance was the main component
of beta diversity (Table 3). On the other hand, the values of nestedness of specific abun-
dance between two sites always had lower values. In particular, the turnover values were
greater for rare species (from 0.805 to 0.879) than for common ones (from 0.594 to 0.842).
In general terms, the turnover in sexually reproducing species was always greater than
that in vegetatively propagating species. In addition, turnover was greater in NOG than
in OG forests. However, considering rare species, regardless of the type of forest stands
(OG and NOG), the differences in beta diversity between sexually reproducing vs. vege-
tative species were smaller than those observed for common species. On the contrary, as
far as common species are concerned, the differences in turnover were extremely relevant,
both between species with different reproductive strategies and between different types
of forest. In particular, the vegetative species had the least turnover (0.594) and greater
nestedness (0.232) in OG forests than all other possible combinations of factors.
Table 3. Components of beta diversity in OG and NOG forests of the study area. The results are presented and are dis-
aggregated according to the reproductive strategy and the level of national rarity of the species.
Beta Diversity OG (n:15) NOG (n:21)
Total Turnover Nestedness Total Turnover Nestedness
Common species
Sexual species 0.877 0.783 0.093 0.886 0.842 0.045
Vegetative species
0.826
0.594
0.232
0.866
0.769
0.098
Rare species
Sexual species 0.902 0.879 0.023 0.918 0.872 0.045
Vegetative species 0.920 0.805 0.115 0.933 0.846 0.087
Forests 2021, 12, 27 9 of 13
4. Discussion
In this work, we investigated the relationship between the reproductive strategy of
epiphytic lichen species and their beta-diversity patterns found in OG vs. NOG forests.
The acquired results only partially support the hypotheses formulated in the study but
provide new insights into the interpretation of the ecology of lichen species in Mediterra-
nean forest ecosystems.
4.1. Sexually Reproducing Lichen Species Had Always High Turnover
The beta diversity analysis confirms the assumption that sexually reproducing spe-
cies had a high turnover in the forests of the study area, regardless of the type of forest
structure, both between old-growth and between non-old growth forests (hypotheses
schematized in Figure 1b,d). Our outcomes are consistent with those found by various
authors (see [37] for a review), and we can trace back the reasons behind this scenario to
several factors:
(1) The spores are lighter than vegetative diaspores and are potentially able to travel
longer distances, reaching more remote sites [38,39].
(2) Sexually reproducing species could have more problems in the early stages of devel-
opment and establishment of new thalli because they have to find a photobiont part-
ner [37,40,41].
(3) Consequently, these species would have less of a tendency to form clusters with ho-
mogeneous communities than vegetative species.
4.2. Vegetative Species Tend to Form Nested Communities Especially in OG Forests
Our hypothesis that the vegetative species were distributed in the two types of forest
stands (OG and NOG) mainly according to nestedness patterns between sites was only
partially supported by the results obtained. Indeed, turnover was always mostly the main
component of beta diversity for this group of species. However, in partial support of the
hypothesis depicted in Figure 1a,c, higher nestedness values were recorded for vegetative
species than for sexual ones, with particular regard to those found among OG forest sites.
The spatial continuity of suitable habitats is undoubtedly the factor that determines these
results (Figure 1a), and justifies the (admittedly small) differences with the observed situ-
ation between NOG sites (Figure 1c). In addition, our old-growth forest sites are charac-
terized by a high number of old and uneven trees (Table 1) that may represent suitable
intermediate substrates (micro-refugia) for the low-range dispersal diaspores [42]. This
structural complexity may contribute to this trend of vegetative species. However, the
prevalence of turnover between sites suggests that, even in ideal habitat conditions and
substrate availability, a limited distance of dispersion strongly conditioned the coloniza-
tion capacity of vegetative species, as suggested by many authors (see e.g., [19,40,43]). This
driver leads to the formation of gaps in the distribution of species within the forest habitat
and, consequently, to a high compositional turnover. Although we can imagine consider-
able differences in the dynamics, range, and success of the establishment depending on
the level of rarity, apparently these propagation characteristics limit the distribution not
only of rare taxa but also of even highly competitive common species.
4.3. The Rarity Level Determines the Species Turnover in Lichen Communities
We found support for explaining the differences in beta diversity observed as a func-
tion of the rarity level of the species. Although the overall beta diversity values were com-
parable to those observed for common species, the contribution of turnover for rare spe-
cies in our study area was considerably higher than that observed for common species.
The turnover was independent of the forest stand (OG and NOG) and the reproductive
strategy of the species. This could be partly affected by the characteristic structure of the
species community datasets, where, in the face of a set of highly represented species, there
Forests 2021, 12, 27 10 of 13
are numerous species with few occurrences, potentially improving turnover values. Nev-
ertheless, we can find possible explanations both in the environmental drivers that shape
the distribution of the species and in the autoecological characteristics of the species them-
selves. With regard to the first aspect, numerous examples in the literature show how the
ecological niche of rare species, defined by the interaction of environmental factors, is
much more restricted than that of common species [44–47]. The drivers involved in defin-
ing the niche of rare species could differ from those decisive for common species. For ex-
ample, by analyzing the beta diversity patterns of the Lobarion communities, Nascimbene
et al. [31] noted that the forest structure variables that influence the distribution of species
of conservation interest do not entirely coincide with those that explained communities of
common species. For example, the average distance between trees and the age of the
stands affected the turnover of rare species much more than that of common ones.
On the other hand, the inadequate dispersal capacity and the low establishment suc-
cess determined the reduced spatial distribution of rare lichen species (both vegetative
and sexual). For example, the effective dispersal range of the large vegetative propagules
of Lobaria pulmonaria was typically 10 m and rarely reached further than 100 m ([41] and
various others). Similarly, Giordani et al. [48] found that sexual reproducing Seirophora
villosa occupied only a small portion of its colonizable niche because of the minimal prop-
agation ability of its spores.
4.4. The Differences between OG and NOG Are Less Evident than One Might Think
Another aspect that emerges from our results and is worth considering is that con-
cerning the actual differences found between OG and NOG in terms of diversity and com-
position.
In the case of our study area, OG and NOG shared a high number of species and had
no significant differences in terms of both alpha and gamma diversity. Furthermore, con-
trary to what one might expect, NOG forests were home to the largest number of exclusive
species, particularly with regard to rare species. Net of other differences that still exist, it
is evident that from a conservation perspective, NOGs play a significant role which cannot
be underestimated. This situation may be for at least two reasons. Firstly, Castanea sativa
trees represent a substrate that in our dataset is exclusive for NOG stands (chestnut woods
and also some individuals in mixed stands). It is well-known that chestnut woods are
suitable habitats for mature lichen communities in the Mediterranean area [24,25]. Sec-
ondly, sustainable management of NOG forests in the study area may have been sub-
jected, in a more or less conscious way, to management techniques compatible with the
maintenance of structured lichen communities [31]. Among others, these techniques in-
clude the integration of old trees in commercial stands [49,50], the reduction of the dis-
tance between regeneration units and sources of propagules [51], or the prolongation of
the rotation cycle [52].
Although there is much evidence showing that epiphytic communities in OG forests
are different from those in NOG forests [24], our results highlight some common aspects
between the two types of forests. These features should be taken into consideration with
greater attention both from a scientific interpretation point of view and from an applica-
tive perspective [31]. This vision is in agreement with [53] who focused on the need to use
multiple community-based approaches to interpret the effects of forest management and
on the opportunity of an integrated investigation of the dynamics of colonization that per-
sist along gradients of forest use. For example, Brunialti et al. [54] pointed out that many
of the methods developed in the past (e.g., [55]) were mainly designed for high forests
rather than coppice forests, even though today this management system covers more than
10% of the total European forests.
Forests 2021, 12, 27 11 of 13
5. Conclusions
The main highlights of our study can be summarized as follows:
Sexually reproducing lichen species always had high turnover. This confirms our
starting hypothesis based on the long-range dispersal ability of this strategy.
Vegetative species tend to form nested communities, especially in OG forests. Spatial
continuity and structural complexity of our old-growth stands could be the main
driver for this result.
The rarity level determines the species turnover in lichen communities.
The differences between OG and NOG are less evident than one might think. It is
evident that non-old growth stands, when managed with a sustainable approach, can
play a significant role in the conservation of well-structured lichen assemblages.
Although our findings only partially support the hypotheses formulated in the study,
we believe that they may provide new insights into the interpretation of the ecology of
lichen species in Mediterranean forest ecosystems.
Supplementary Materials: The following are available online at www.mdpi.com/1999-
4907/12/1/27/s1, Table S1: Distribution of the sampled tree species in old-growth (OG) and Non old-
growth (NO) stands. Table S2: List of the 148 lichen species found on the 106 sampled trees, with
their occurrence (number and percentage of plots).
Author Contributions: Conceptualization, G.B., L.F. and P.G.; methodology, L.F., P.G.; formal
analysis, L.F. and P.G.; investigation, G.B., S.R.; resources, G.B., S.R.; data curation, L.F. and G.B.;
writing—original draft preparation, G.B., L.F., S.R. and P.G.; writing—review and editing, G.B.,
L.F., S.R. and P.G. All authors have read and agreed to the published version of the manuscript.
Funding: Funding for field sampling was provided by the Cilento and Vallo di Diano National
Park and is part of the project “Monitoraggio alla rete dei boschi vetusti del Parco nazionale del
Cilento e Vallo di Diano” with the coordination of the Department of Plant Biology of “La Sapi-
enza” University, Rome.
Institutional Review Board Statement: Not applicable.
Informed Consent Statement: Not applicable.
Data Availability Statement: The data presented in this study are available on request from the
corresponding author.
Acknowledgments: We thank the three reviewers for useful suggestions that helped to improve
this paper.
Conflicts of Interest: The authors declare no conflict of interest.
References
1. Eriksson, O.; Kiviniemi, K. Evolution of plant dispersal. In Life History Evolution in Plants; Vuorisalo, T.O., Mutikainen, P.K.,
Eds.; Kluwer: Dordrecht, The Netherlands, 2001; pp. 215–237.
2. Sádlo, J.; Chytrý, M.; Pergl, J.; Pyšek, P. Plant dispersal strategies: A new classification based on multiple dispersal modes of
individual species. Preslia 2018, 90, 1–22, doi:10.23855/preslia.2018.001.
3. Van der Pijl, L. Principles of Dispersal in Higher Plants; Springer: New York, NY, USA, 1982.
4. Nash, T.H., III. Lichen Biology, 2nd ed.; Cambridge University Press: Cambridge, UK, 2008.
5. Dobson, F. Getting a liking for lichens. Biologist 2003, 50, 263–267.
6. Seymour, F.A.; Crittenden, P.D.; Dyer, P.S. Sex in the extremes: Lichen-forming fungi. Mycologist 2005, 19, 51–58,
doi:10.1017/S0269-915X(05)00201-6.
7. Bowler, P.A.; Rundel, P.W. Reproductive strategies in lichens. Bot. J. Linn. Soc. 1975, 70, 325–340, doi:10.1111/j.1095-
8339.1975.tb01653.x.
8. Stofer, S.; Bergamini, A.; Aragón, G.; Carvalho, P.; Coppins, B.J.; Davey, S.; Dietrich, M.; Farkas, E.; Kärkkäinen, K.; Keller, C.;
et al. Species richness of lichen funtional groups in relation to land use intensity. Lichenologist 2006, 38, 331–353,
doi:10.1017/S0024282906006207.
Forests 2021, 12, 27 12 of 13
9. Walser, J.C. Molecular evidence for the limited dispersal of vegetative propagules in the epiphytic lichen Lobaria pulmonaria.
Am. J. Bot. 2004, 91, 1273–1276, doi:10.3732/ajb.91.8.1273.
10. Öckinger, E.; Niklasson, M.; Nilsson, S.G. Is local distribution of the epiphytic lichen Lobaria pulmonaria limited by dispersal
capacity or habitat quality? Biodivers. Conserv. 2005, 14, 759–773, doi:10.1007/s10531-004-4535-x.
11. Jüriado, I.; Liira, J.; Csencsics, D.; Widmer, I.; Adolf, C.; Kohv, K.; Scheidegger, C. Dispersal ecology of the endangered wood-
land lichen Lobaria pulmonaria in managed hemiboreal forest landscape. Biodivers. Conserv. 2011, 20, 1803–1819,
doi:10.1007/s10531-011-0062-8.
12. Ronnås, C.; Werth, S.; Ovaskainen, O.; Várkonyi, G.; Scheidegger, C.; Snäll, T. Discovery of long-distance gamete dispersal in a
lichen-forming ascomycete. New Phytol. 2017, 216, 216–226, doi:10.1111/nph.14714.
13. Tapper, R. Dispersal and changes in the local distributions of Evernia prunastri and Ramalina farinacea. New Phytol. 1976, 77, 725–
734, doi:10.1111/j.1469-8137.1976.tb04667.x.
14. Armstrong, R.A. Dispersal in a population of the lichen Hypogymnia physodes. Environ. Exp. Bot. 1987, 27, 357–363,
doi:10.1016/0098-8472(87)90046-3.
15. Scheidegger, C.; Werth, S. Conservation strategies for lichens: Insights from population biology. Fungal Biol. Rev. 2009, 23, 55–
66, doi:10.1016/j.fbr.2009.10.003.
16. Moning, C.; Werth, S.; Dziock, F.; Bässler, C.; Bradtka, J.; Hothorn, T.; Müller, J. Lichen diversity in temperate montane forests
is influenced by forest structure more than climate. For. Ecol. Manag. 2009, 258, 745–751, doi:10.1016/j.foreco.2009.05.015.
17. Ellis, C.J.; Coppins, B.J. Integrating multiple landscape-scale drivers in the lichen epiphyte response: Climatic setting, pollution
regime and woodland spatial-temporal structure. Divers. Distrib. 2010, 16, 43–52, doi:10.1111/j.1472-4642.2009.00624.x.
18. Giordani, P.; Brunialti, G.; Bacaro, G.; Nascimbene, J. Functional traits of epiphytic lichens as potential indicators of environ-
mental conditions in forest ecosystems. Ecol. Indic. 2012, 18, 413–420, doi:10.1016/j.ecolind.2011.12.006.
19. Martínez, I.; Flores, T.; Otálora, M.A.G.; Belinchón, R.; Prieto, M.; Aragón, G.; Escudero, A. Multiple-scale environmental mod-
ulation of lichen reproduction. Fungal Biol. 2012, 116, 1192–1201, doi:10.1016/j.funbio.2012.09.005.
20. Hurtado, P.; Prieto, M.; Aragón, G.; De Bello, F.; Martínez, I. Intraspecific variability drives functional changes in lichen epi-
phytic communities across Europe. Ecology 2020, e03017, doi:10.1002/ecy.3017.
21. Brunialti, G.; Frati, L.; Aleffi, M.; Marignani, M.; Rosati, L.; Burrascano, S.; Ravera, S. Lichens and bryophytes as indicators of
old-growth features in Mediterranean forests. Plant Biosyst. 2010, 144, 221–233, doi:10.1080/11263500903560959.
22. Brunialti, G.; Ravera, S.; Frati, L. Mediterranean old-growth forests: The role of forest type in the conservation of epiphytic
lichens. Nova Hedwig. 2013, 96, 367–381, doi:10.1127/0029-5035/2012/0069.
23. Blasi, C.; Marchetti, M.; Chiavetta, U.; Aleffi, M.; Audisio, P.; Azzella, M.M.; Brunialti, G.; Capotorti, G.; Del Vico, E.; Lattanzi,
E.; et al. Multi-taxon and forest structure sampling for identification of indicators and monitoring of old-growth forest. Plant
Biosyst. 2010, 144, 160–170, doi:10.1080/11263500903560538.
24. Nascimbene, J.; Brunialti, G.; Ravera, S.; Frati, L.; Caniglia, G. Testing Lobaria pulmonaria (L.) Hoffm as an indicator of lichen
conservation importance of Italian forests. Ecol. Indic. 2010, 10, 353–360, doi:10.1016/j.ecolind.2009.06.013.
25. Ravera, S.; Brunialti, G. Epiphytic lichens of a poorly explored National Park: Is the probabilistic sampling effective to assess
the occurrence of species of conservation concern? Plant Biosyst. 2013, 147, 115–124, doi:10.1080/11263504.2012.736425.
26. Brunialti, G.; Frati, L.; Ravera, S. Ecology and conservation of the sensitive lichen Lobaria pulmonaria in Mediterranean old-
growth forests. In Old-Growth Forests and Coniferous Forests. Ecology, Habitat and Conservation; Weber, P.R., Ed.; Nova Science
Publisher: New York, NY, USA, 2015; pp. 1–20.
27. Magliulo, P.; Terribile, F.; Colombo, C.; Russo, F. A pedostratigraphic marker in the geomorphological evolution of the Cam-
panian Apennines (southern Italy): The Paleosol of Eboli. Quat. Int. 2006, 156, 97–117, doi:10.1016/j.quaint.2006.05.006.
28. Marchetti, M.; Tognetti, R.; Lombardi, F.; Chiavetta, U.; Palumbo, G.; Sellitto, M.; Colombo, C.; Iovieno, P.; Alfani, A.;
Baldantoni, D.; et al. Ecological portrayal of old-growth forests and persistent woodlands in the Cilento and Vallo di Diano
National Park (southern Italy). Plant Biosyst. 2010, 144, 130–147, doi:10.1080/11263500903560470.
29. Tallent-Hansel, N.G. Forest Health Monitoring. Field Methods Guide, EPA/620/R-94/027; US Environmental Protection Agency:
Washington, DC, USA, 1994.
30. Nimis, P.L. The Lichens of Italy. A Second Annotated Catalogue; EUT: Trieste, Italy, 2016.
31. Nascimbene, J.; Nimis, P.L.; Ravera, S. Evaluating the conservation status of epiphytic lichens of Italy: A red list. Plant Biosyst.
2013, 147, 898–904, doi:10.1080/11263504.2012.748101.
32. Baselga, A. Separating the two components of abundance-based dissimilarity: Balanced changes in abundance vs. abundance
gradients. Methods Ecol. Evol. 2013, 4, 552–557, doi:10.1111/2041-210X.12029.
Forests 2021, 12, 27 13 of 13
33. Oksanen, J.; Blanchet, F.G.; Kindt, R.; Legendre, P.; O’Hara, R.G.; Simpson, G.L.; Solymos, P.; Henry, M.; Stevens, H.; Wagner,
H. Vegan: Community Ecology Package; R Package Version 1.17-0; 2010. Available online: http://CRAN.R-project.org/ (accessed
on 29 October 2020).
34. Goslee, S.C.; Urban, D.L. The ecodist package for dissimilarity-based analysis of ecological data. J. Stat. Softw. 2007, 22, 1–19,
doi:10.18637/jss.v022.i07.
35. Baselga, A.; Orme, C.D.L. Betapart: An R package for the study of beta diversity. Methods Ecol. Evol. 2012, 3, 808–812,
doi:10.1111/j.2041-210X.2012.00224.x.
36. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria,
2020. Available online: https://www.R-project.org/ (accessed on 2 November 2020).
37. Ellis, C.J. Lichen epiphyte diversity: A species, community and trait-based review. Perspect. Plant Ecol. Evol. Syst. 2012, 14, 131–
152, doi:10.1016/j.ppees. 2011.10.001.
38. Maynard Smith, J. The Evolution of Sex; Cambridge University Press: Cambridge, UK, 1978.
39. Walser, J.C.; Gugerli, F.; Holderegger, R.; Kuonen, D.; Scheidegger, C. Recombination and clonal propagation in different pop-
ulations of the lichen Lobaria pulmonaria. Heredity 2004, 93, 322–329, doi:10.1038/sj.hdy.6800505.
40. Hedenås, H.; Bolyukh, V.O.; Jonsson, B.G. Spatial distribution of epiphytes on Populus tremula in relation to dispersal mode. J.
Veg. Sci. 2003, 14, 233–242, doi:10.1111/j.1654-1103.2003.tb02148.x.
41. Werth, S.; Wagner, H.; Gugerli, H.; Holderegger, R.; Csencsics, D.; Kalwij, J.; Scheidegger, C. Quantifying dispersal and estab-
lishment limitation in a population of an epiphytic lichen. Ecology 2006, 87, 2037–2046.
42. Zemanová, L.; Trotsiuk, V.; Morrissey, R.C.; Bače, R.; Mikoláš, M.; Svoboda, M. Old trees as a key source of epiphytic lichen
persistence and spatial distribution in mountain Norway spruce forests. Biodivers. Conserv. 2017, 26, 1943–1958,
doi:10.1007/s10531-017-1338-4.
43. Löbel, S.; Snäll, T.; Rydin, H. Metapopulation processes in epiphytes inferred from patterns of regional distribution and local
abundance in fragmented forest landscapes. J. Ecol. 2006, 94, 856–868, doi:10.1111/j.1365-2745.2006.01114.x.
44. Nilsson, S.G.; Arup, U.; Baranowski, R.; Ekman, S. Tree-dependent lichens and beetles as indicators in conservation forests.
Conserv. Biol. 1995, 9, 1208–1215, doi:10.1046/j.1523-1739.1995.9051199.x-i1.
45. Spitale, D. A comparative study of common and rare species in spring habitats. Ecoscience 2012, 19, 80–88, doi:10.2980/19-1-3435.
46. Markham, J. Rare species occupy uncommon niches. Sci. Rep. 2014, 4, 6012, doi:10.1038/srep06012.
47. Williams, L.; Ellis, C.J. Ecological constraints to ‘old-growth’ lichen indicators: Niche specialism or dispersal limitation? Fungal
Ecol. 2018, 34, 20–27, doi:10.1016/j.funeco.2018.03.007.
48. Giordani, P.; Benesperi, R.; Mariotti, M.G. Local dispersal dynamics determine the occupied niche of the red-listed lichen Sei-
rophora villosa (Ach.) Frödén in a Mediterranean Juniperus shrubland. Fungal Ecol. 2015, 13, 77–82, doi:10.1016/j.fu-
neco.2014.08.008.
49. Moning, C.; Muller, J. Critical forest age thresholds for the diversity of lichens, molluscs and birds in beech (Fagus sylvatica L.)
dominated forests. Ecol. Indic. 2009, 9, 922–932, doi:10.1016/j.ecolind.2008.11.002.
50. Király, I.; Nascimbene, J.; Tinya, F.; Ódor, P. Factors influencing epiphytic bryophyte and lichen species richness at different
spatial scales in managed temperate forests. Biodiv. Conserv. 2013, 22, 209–223, doi:10.1007/s10531-012-0415-y.
51. Nascimbene, J.; Marini, L.; Nimis, P.L. Influence of forest management on epiphytic lichens in a temperate beech forest of north-
ern Italy. For. Ecol. Manag. 2007, 73, 43–47, doi:10.1016/j.foreco.2007.04.011.
52. Humphrey, J.W.; Davey, S.; Peace, A.J.; Ferris, R.; Harding, K. Lichens and bryophyte communities of planted and semi-natural
forests in Britain: The influence of site type, stand structure and deadwood. Biol. Conserv. 2002, 107, 165–180, doi:10.1016/S0006-
3207(02)00057-5.
53. Giordani, P. Assessing the effects of forest management on epiphytic lichens in coppiced forests using different indicators. Plant
Biosyst. 2012, 146, 628–637, doi:10.1080/11263504.2011.654136.
54. Brunialti, G.; Frati, L.; Calderisi, M.; Giorgolo, F.; Bagella, S.; Bertini, G.; Chianucci, F.; Fratini, R.; Gottardini, E.; Cutini, A.
Epiphytic lichen diversity and sustainable forest management criteria and indicators: A multivariate and modelling approach
in coppice forests of Italy. Ecol. Indic. 2020, 115, 106358, doi:10.1016/j.ecolind.2020.106358.
55. Rose, F. Temperate forest management: Its effects on bryophyte oras and habitats. In Bryophytes and Lichens in a Changing Envi-
ronment; Bates, J.W., Farmer, A.M., Eds.; Clarendon Press: Oxford, UK, 1992; pp. 211–233.