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Cladonia subturgida (Cladoniaceae, Lecanoromycetes),
an overlooked, but common species in the Mediterranean region
Raquel Pino-Bodas
1
&Elena Araujo
2
&Blanca Gutiérrez-Larruga
2
&Ana Rosa Burgaz
2
Received: 13 April 2020 /Accepted: 25 May 2020
#The Author(s) 2020
Abstract
Cladonia subturgida is a Mediterranean species that has been overlooked. Apparently it was restricted to the Iberian Peninsula
and Canary Islands. However, during the study of the genus Cladonia in the Mediterranean region, new populations from 44
localitieswere found in: south France, Sardinia, south Italian peninsula, Crete and continental Greece. Distribution models based
on MaxEnt, GLM, GAM and MARS algorithms were used to estimate the potential distribution of C. subturgida. Sicily, Corsica
and the north of Africa were regions with suitable climatic conditions for C. subturgida where it has not been reported yet. The
climatic variables with greatest relative influence in the C. subturgida distribution were the Precipitation of Warmest Quarter and
the Annual Precipitation. Additionally, the ITS rDNA region was used to study the genetic variation of this species across its
distribution area. Eleven haplotypes were found, one of them widely distributed through its geographical range. AMOVA
analyses indicated lack of geographical structure.
Keywords Cladoniaceae .Distribution modelling .Genetic diversity .Lichen forming fungi
1 Introduction
The Mediterranean basin is one of the world’sbiodiversity
hotspots (Médail and Quézel 1999; Myers et al. 2000), concen-
trating 10% of all the known vascular plants, of which 80% are
endemic (Fady-Welterlen 2005). Three factors are crucial to
explain the high biodiversity of the Mediterranean basin: the
complicated geology of the area, the climate, characterized by
hot and dry summers, and the high impact of human activities,
that have substantially altered the landscape (Thompson 2005).
There exist lichen catalogues for several Mediterranean
countries (e.g. Litterski and Mayrhofer 1998; Llimona and
Hladún 2001; Abbott 2009; Mayrhofer et al. 2013;Roux
2012;Nimis2016). According to these inventories, more than
2500 lichen species grow in this region, though its diversity is
not absolutely well-known, since many areas are still poorly
explored, especially in North Africa. For reasons of similarity
to the Mediterranean biogeographical pattern of vascular
plants (Thompson 2005), several authors have adopted this
same pattern in lichens (Nimis and Poelt 1987; Nimis and
Tretiach 1995;Galloway2008). Yet the validity of this as-
sumption has been questioned because very few endemic li-
chen species exist in the Mediterranean region (Barreno 1991;
Nimis 1996; Nimis 2016), unlike what happens with plants.
The lichens of the genus Cladonia are characterized by a
dimorphic thallus composed by a crustose or foliose primary
thallus and a fruticose secondary thallus. In the Mediterranean
region, the species of this genus mainly grow on roadside
slopes, shrublands (as heaths), and pine groves (Burgaz and
Ahti 2009), since most of the species are heliophilous. Though
the genus Cladonia has been well studied in some countries of
the Mediterranean basin, such as Spain, Croatia, Italy, France,
Georgia (Burgaz and Ahti 2009; Nimis 2016; Burgaz and
Pino-Bodas 2012;Burgazetal.2017; Roux 2017), the current
knowledge for the whole region is still scarce, and the proof is
that new records are regularly reported (Burgaz et al. 2017,
2019a,2019b; Monia et al. 2018; Gheza et al. 2018; Kocakaya
et al. 2018). To date, 90 species of this genus have been re-
ported for the Mediterranean basin (Burgaz et al. 2020). The
species of Cladonia present in the region show different dis-
tribution patterns; many of them have wide distributions that
Electronic supplementary material The online version of this article
(https://doi.org/10.1007/s13199-020-00688-7) contains supplementary
material, which is available to authorized users.
*Raquel Pino-Bodas
r.pino@kew.org
1
Royal Botanic Gardens, Kew, Richmond, Surrey TW9 3DS, UK
2
Department of Biodiversity, Ecology and Evolution, Complutense
University, E-28040 Madrid, Spain
https://doi.org/10.1007/s13199-020-00688-7
/ Published online: 8 June 2020
Symbiosis (2020) 82:9–18
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embrace several continents (e.g., C. furcata,C. humilis,
C. pyxidata, etc.), while others are restricted to Europe and
Macaronesia (for instance C. subcervicornis,
C. cyathomorpha). Some species of Cladonia characteristic
of the Mediterranean region are, for example,
C. mediterranea, C. cervicornis, C. subturgida, C. foliacea,
C. rangiformis and C. firma (Litterski and Ahti 2004;Burgaz
and Ahti 2009;AhtiandStenroos2013). Though these spe-
cies do not restrict themselves to the Mediterranean region, it
is there where they are most abundant (Litterski and Ahti
2004; Burgaz and Ahti 2009;AhtiandStenroos2013).
Cladonia subturgida is a species with a persistent and dom-
inant primary thallus, often lacking a secondary thallus
(Fig. 1a, b). It is distributed in the western area of the Iberian
Peninsula and in the Canary Islands (Pino-Bodas et al. 2012).
During our field work in different countries of the
Mediterranean region (France, Italy, Greece) we found numer-
ous specimens of C. subturgida. We hypothesize that
C. subturgida is a common species in the Mediterranean region,
but poorly sampled, or mistaken for other species of Cladonia
with dominant primary thallus, such as C. cervicornis and
C. firma. In order to test this hypothesis, species distribution
models have been used, based on all the known records.
Species distribution models are helpful when it comes to under-
standing the environmental factors that determine the occurrence
of species. These methods have been succesfully used to predict
the potential distribution of several epiphytic lichen species
(Glavich et al. 2005;Bolligeretal.2007; Pearson et al. 2018;
Guttová et al. 2019), and likewise to assess the impact of the
climatic change on the lichen distribution, to propose conserva-
tion plans (Allen and Lendemer 2016; Ellis et al. 2007;Wiersma
and Skinner 2011; Pearson et al. 2018; Ellis 2019),andtode-
termine zones that played the role of glacial shelters for certain
species (Kukwa and Kolanowska 2016).
In this study we report new findings of Cladonia
subturgida in several countries of the Mediterranean basin,
Fig. 1 aPrimary thallus of Cladonia subturgida bPodetia of C. subturgida cDistribution of C. subturgida based on specimens studied and literature
references
10 Pino-Bodas R. et al.
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the chemical variation of this species and its genetic diversity
based on ITS rDNA region. Additionally, we model its poten-
tial distribution in order to identify the key environmental
variable that shapes the ecological niche of C. subturgida.
2 Material and methods
2.1 Specimens studied
Specimens were collected from France, Italy, Sardinia, Greece
and Crete between 2015 and 2018 (Supplementary material).
The surveys were conducted on ca. 260 localities. All the new
collections were deposited at MACB herbarium in Madrid
and some duplicates were sent to Helsinki (H) and Trieste
(TSB) herbaria. The secondary metabolites of each specimen
were analysedby thin layer chromatography (TLC) according
to standardized procedures (White and James 1985;Orange
et al. 2001), using the solvents A, B and C.
Thirty eight newly collected specimens, in addition to the
sequences from Pino-Bodas et al. (2012), were used to esti-
mate the genetic diversity of C. subturgida. The specimens
selected covered the whole distribution area (Fig. 1c). In total
we included 18 specimens from Greece, three from Southern
Italy, seven from Sardinia, nine from Spain, ten from France,
one from Portugal and one from Canary Islands. The ITS
rDNA region, the barcoding of fungi (Schoch et al. 2012),
was selected to study the genetic diversity of Cladonia
subturgida.
2.2 DNA extraction and amplification
The E.Z.N.A. Forensic DNA Isolation Kit (Omega Bio-Tek)
was used to extract the genomic DNA, following the manu-
facturer’s instructions. PCRs were carried out with Biotaq
polymerase (Bioline). The volume of reaction was 25 μl,
0.3 μLofTaq polymerase, 2.5 μL of 10× PCR buffer,
1.4 μL of MgCl 2 50 μm/μL, 1.6 μL of dNTPs (2.5 μm/
μL), 1 μLofBSA(1μm/μL), 1 μLofeachprimer(10μm/
μL), and 1 μL of extracted DNA.The primers used to amplify
ITS rDNA region were ITS1F and ITS4 (White et al. 1990;
Gardes and Bruns 1993) and PCR program was initial dena-
turation at 95 °C for 2 min; five cycles of 95 °C for 30 s, 58 °C
for 30 s and 72 °C for 1 min and 34 cycles of 95 °C for 30 s,
56 °C for 30 s and 72 °C for 1 min; with a final extension at
72 °C for 10 min. PCR products were cleaned with
ExoProStar TM 1-step (GE Healthcare). The sequencing re-
actions were done at Macrogen Spain service (www.
macrogen.com), with the same primers used for the PCR.
Sequencher 4.1.4 program (Gene Codes Corporation, Inc.,
Ann Arbor, Michigan, USA) was used to assemble the se-
quences. The alignment was made in MAFFT (Katoh and
Standley 2013), then it was checked and improved manually in
BIOEDIT 7.0 (Hall 1999). A phylogenetic analysis based on ITS
rDNA was carried out to test the monophyly of Cladonia
subturgida. One hundred and sixty one species of Cladonia were
included in this analysis based on the phylogenetic study of
Stenroos et al. (2019). Cladonia wainioi was selected as
outgroup. The ambiguous regions were removed using Gblock
(Talavera and Castresana 2007) with the less stringent options.
The alignment contained 211 sequences and 524 positions.
Maximun likelihood analysis was implemented in RAxML
7.0.3 (Stamatakis et al. 2005) assuming the GTRGAMMA mod-
el. The bootstrap searches were conducted with 1000
pseudoreplicates using the rapid bootstrap algorithm.
2.3 Genetic diversity and haplotype analyses
The program DnaSP (Librado and Rozas 2009) was used to
calculate the haplotype diversity, segregate sites and nucleo-
tide diversity. Haplotype network under statistical parsimony
were constructed in TCS 1.21 (Clement et al. 2000), consid-
ering the gaps as missing data. Mantel test was carried out to
study the correlation between the ITS rDNA genetic distances
and the geographical distances (using Euclidean distance)
with 2000 random permutations to test the significance in
VEGAN package (Oksanen et al. 2007)forR.
Analysis of molecular variance (AMOVA) was performed
in Arlequin v 3.5 (Excoffier and Lischer 2000) in order to
assess the proportion of the genetic variation attributed to
different geographical regions (Iberian Peninsula, France,
Italy and Greece). The single specimen from Canary Islands
was excluded from these analyses.
2.4 Species distribution modeling
Species distribution modeling was used to estimate the poten-
tial distribution of C. subturgida under the current climatic
conditions. The distribution modeling was based on 158 oc-
currence records whose identification has been verified by
morphological studies according to Pino-Bodas et al. (2012)
under dissecting microscope. The 19 bioclimatic variables at
2.5 min of spatial resolution were downloaded from the
WorldClim website (https://www.worldclim.org;Hijmans
et al. 2005). A pseudo-absences set was generated avoiding
the overlap with the presences. Firstly the models were gen-
erated using all bioclimatic variables. Then, the models were
estimated using only uncorrelated variables, according
Kendall rank correlation coefficient, and selecting those vari-
ables which contributed more significantly in the first models.
The variables selected were: Annual Mean Temperature
(BIO1), Temperature Seasonality (BIO4), Mean
Temperature of Driest Quarter (BIO9), Mean Temperature
of Coldest Quarter (BIO11), Annual Precipitation (BIO12)
and Precipitation of Warmest Quarter (BIO18).
11 (Cladoniaceae, Lecanoromycetes), an overlooked, but common species in the Mediterranean...
Cladonia subturgida
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Four modeling methods were used: Generalized additive
models (GAM), generalized linear models (GLMs),
Multivariate adaptive regression splines (MARS) and maxi-
mum entropy (Maxent). The models GAM, GLMs and
MARS were implemented in R using the libraries GAM,
DISMO and EARTH (Wood 2012; Milborrow et al. 2014;
Hijmans et al. 2017).The method selected to assess the model
fitting was the area under the receiver operating characteristic
curve (AUC) (Fielding and Bell 1997). This value gives a
measure of model discrimination accuracy, values close to 1
indicate a good discrimination. Jackknife test was run in
Maxent, using 25 random points and 5 replicates to estimate
the contribution of each variable to the model. This test com-
pares the fitting of the models with and without a variable in
order to assess the contribution of this variable to the
distributionl prediction (Phillips et al. 2006).
Then a consensus ensemble prediction from all individual
models with selected variables was built.
3 Results
In this study 44 new records of Cladonia subturgida for three
countries are presented. The specimens were collected in
south France, Sardinia, south continental Italy, Crete and con-
tinental areas of Greece, representing the first records for all
the countries. The complete distribution of C. subturgida is
presented in Fig. 1c, based on the new data, our previous
studies (Burgaz and Ahti 2009; Pino-Bodas et al. 2012)and
a few literature reports (Kocakaya et al. 2018). It grows on
bare soils or earth banks, preferably acidic or
subneutrophilous soils of xerothermic evergreen vegetation
dominated by Cistus shrubs, heathlands, Pinus or Quercus
woodlands, in an altitude range from 25 to 1760 m.
Twelve populations were found in France at the Provence-
Alpes-Côte d’Azur Region. Eleven from the Department of
Var (Le Cannet des Maures, Massif des Maures and Massif de
l’Esterel) and one from Alpes-Maritimes (Contes). The spe-
cies was found on acidic substrate of Quercus suber,Pinus
pinea and P. pinaster forests, 33–476 m altitude. In Italy 17
populations were found, 15 of them from Sardinia, growing
on maquis shrubland with Quercus suber or deciduous
Quercus and acidic substrate. Additionally, two populations
were found in Calabria, on Cistus monspeliensis shrubs and
deciduous Quercus, growing between 459 and 607 m altitude.
Fifteen populations were found in Greece. Eight of them in
Macedonia and Thrace, one in Thessaly, three in the
Peloponnese, and one in West-Greece counties, growing on
Quercus coccifera and Pistacia lentiscus formations, on acidic
soils. In Crete island two populations were found, one of them
in Heraklion and the another one in Chania, growing on
Arbutus unedo and Erica manipuliflora shrubs.
The accompanying species were Cladonia cervicornis,
C. corsicana,C. firma,C. foliacea,C. humilis,C. pyxidata
or C. ramulosa.
Table 1shows the chemical variation found in the new
collections of C. subturgida. Eight different chemotypes
were detected, the most common contains atranorin and
protolichesterinic acid and the second one contains addi-
tionally zeorin. Greek populations were the most variable
chemically, with seven different chemotypes. Five of them
were present in Crete (Table 1). Intra-population chemical
variation was detected on tree localities, all of them from
Greece. In one locality in the Peloponnese the chemotypes I
and III were detected, in one locality in Macedonia-Thrace
the chemotypes I and IV were detected and in Chania, Crete
Island, the chemopytes I, III and VII were found.
The new DNA sequences generated have been deposited
in GenBank (MT510881-MT510918). The phylogenetic
analysis shows that C. subturgida is monophyletic (Fig.
1S). A single haplotype network containing 11 haplotype
without missing haplotypes was generated by TCS. One
haplotype was widespread in the Mediterranean basin
(Fig. 2), three haplotypes were unique to Greece, one was
exclusive to south Italy, one was exclusive to France, one
was restricted to Sardinia and two were exclusive to Iberian
Peninsula. Three haplotypes were shared: one was shared
between populations from Spain and France, other haplo-
type was shared between populations from Spain and
Portugal and a third haplotype was shared between popula-
tions from Spain and Greece.
The genetic diversity of Cladonia subturgida is presented
in Table 2. The populations from the Iberian Peninsula were
the most diverse, following those from Greece. The AMOVA
test did not show differentiation among the populations of
different regions (Table 3). The Mantel test did not find any
correlation between the genetic distance of C. subturgida and
the geographical distance (r = 0.04239, Pvalue = 0.24338).
Table 1 Chemical variation of C. subturgida found in the specimen
newly collected
Chemotypes France Greece (Crete) Italy Total
ATR, PLIC 3 9 (1) 16 28
ATR, PLIC, ZEO 6 2 8
ATR, PLIC, FUM 4 (1) 4
ATR, PLIC, FUM, ZEO 2 1 3
ATR, FUM 1 1
ATR 1 (1) 1
FUM 1 (1) 1
FUM, PLIC 1 (1) 1
ATR Atranorin, PLIC Protolichesterinic acid, FUM Fumarprotocetraric
acid complex, ZEO Zeorin
12 Pino-Bodas R. et al.
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3.1 Species distribution modelling
In total, 9 models were generated, 2 for each of the methods
used, plus the consensus model of all models with selected
variables. The AUC values obtained for each model with se-
lected variables are shown in Table 4. All the models showed
high AUC values (> 0.90), meaning a fine fitting. The overall
agreement among models built using different methods was
high (see suplementary material). Table 5shows the relative
contribution of every climatic variable. Annual Precipitation
(37.3%) and Precipitation of Warmest Quarter (25.6%) were
the variables with highest contribution to the models.
Figure 3shows the consensus model, showing the areas
with the highest suitability for C. subturgida. The predicted
suitable areas for C. subturgida were the Iberian Peninsula,
southern France, Corsica, Sardinia, Sicily, Italian
Mediterranean area, Greece, western Turkey, north of Africa
and a few spots on the southernmost parts of England.
4 Discussion
4.1 New records and distribution of Cladonia
subturgida
This species was described for Portugal (Sampaio 1918)
and for a long time known only from the type locality
(Burgaz and Ahti 1998,2009). Morphological similarities
with C. iberica were noted (Burgaz and Ahti 1998,2009)
and the phylogenetic studies confirmed that both taxa,
C. iberica and C. subturgida, represented a single species
phenotypically very variable, distributed in the Iberian
Peninsula and Canary Island (Burgaz and Ahti 2009;
Pino-Bodas et al. 2012). Recently, it has been reported for
Turkey (Kocakaya et al. 2018) and the authors consider that
this species should be common in the Mediterranean re-
gion, though reported only as scattered. Our results confirm
that C. subturgida is widely distributed in the
Mediterranean basin. The reasons why this species has been
scarcely cited could be the following: 1) In general, only the
primary thallus is developed; 2) It has been mistaken for
other species; 3) Insufficient sampling in the territory. With
the exception of some few species, the identifications of
Cladonia based on the characters associated with the pri-
mary thallus are difficult (Ahti 2000). Although the colour
and the morphology of the squamules of C. subturgida are
very characteristic, the species can be difficult to identify
for the non-specialists in the genus since it is morphologi-
cally very variable (Pino-Bodas et al. 2012). It is character-
ized by a dominant primary thallus with large and fragile,
(6–25 mm long × 1.5–4 mm wide) undivided and laciniate
or deeply lobate (Fig. 1). The upper surface is green glau-
cous to green olivaceous; lower surface white, purplish to-
ward the margin. Podetia are rare, branched near the tips
with open axils and corticate (Pino-Bodas et al. 2012;
Burgaz et al. 2020).
In addition, C. subturgida is also chemically very variable.
Pino-Bodas et al. (2012) reported six different chemotypes,
five of which are also present in the newly collected material.
In accordance with previous studies the commonest
chemotype is the one containing atranorin and
protolichesterinic acid. The latter substance is absent from
most of the species morphologically closely related. But it is
an aliphatic acid that can only be detected by TLC or HPLC
methods and in many cases these techniques are not routinely
used to identify Cladonia specimens (Haughland et al. 2018).
The species morphologically close for which C. subturgida
could have been mistaken are C. firma and C. cervicornis,
both common in the Mediterranean region and with a domi-
nant primary thallus (Burgaz and Ahti 2009; Pino-Bodas et al.
2012). Although both species have podetia with scyphi and
Fig. 2 aGeographical
distribution of the haplotypes of
Cladonia subturgida bHaplotype
network inferred by TCS based
on ITS rDNA region. Each circle
represents a haplotype, the circle
size is proportional to haplotype
frequency
Table 2 Genetic diversity of Cladonia subturgida across its distribution
range
Nh H πS
Iberian populations 12 5 0.66667 0.00143 4
French populations 9 3 0.55556 0.00109 2
Italian populations 10 3 0.37778 0.00071 2
Greek populations 17 5 0.42647 0.00137 4
Total 49 11 0.54965 0.00146 10
Nnumber of specimens, hnumber of haplotypes, Hhaplotype diversity, S
number of polymorphic sites
13 (Cladoniaceae, Lecanoromycetes), an overlooked, but common species in the Mediterranean...
Cladonia subturgida
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C. subturgida never has scyphi, thalli without podetia are
highly frequent (Burgaz and Ahti 2009).
Our result indicates that more lichen sampling in the
Mediterranean region is needed, even in the countries
where the lichens have been best studied, like Italy and
France. Though terricolous lichens in the Mediterranean
region have been studied (for instance Klement 1969;
Alonso and Egea 1994,1995;Martínezetal.2006; Gheza
et al. 2016; Cogoni et al. 2011), in general they are less well
known than epiphytic ones (Nimis and Martellos 2004;
Nimis 2016).
According to the potential distribution models, the re-
gions with climatic conditions suitable for the growth of
C. subturgida, but in which it has not yet been reported,
are Sicily, Corsica, north of Africa (including the northern
regions of Morocco, Algeria and Tunisia), certain enclaves
in Cyprus, the south of England, the east of Ireland, the
north of Scotland. Numerous localities were sampled in
Sicily and Cyprus during the study of the family
Cladoniaceae in the Mediterranean region (Burgaz et al.
2020), but C. subturgida was not found. Nevertheless we
consider it plausible that some populations of C. subturgida
exist in the northeast of Sicily (Monti Peloritani, Messina
province) where the potential vegetation corresponds to
oakwoods of Quercus suber.InCyprusitisalsolikelyfor
the species to be present in some spots of acid substrate.
Corsica presents a large extensión of acid substrates (Reille
et al. 1997) and is another region where the species proba-
bly grows and should be looked for. In Italy C. subturgida
has only been found in Calabria region to date, but the
models point out for this country a wider distribution,
broadly coincident with the humid, submediterranean,
Tyrrhenian zone (Incerti and Nimis 2006). In Calabria,
C. subturgida probably restricts itself to a narrow coastal
strip, the true location of the Mediterranean vegetation
(Nimis 2016). But more populations of this species are to
be expected in the Tuscany and in parts of the Puglia that
share the same vegetation type. We are informed of a pop-
ulation of C. subturgida extant in the northwest of Algeria
(Boudial et al. unpublished). There probably are still more
populations in Algeria and Tunisia, very scarcely sampled
regions whose lichen flora is poorly known (Seaward 1996;
Amrani et al. 2018;Moniaetal.2018). Even in the south of
England some populations of C. subturgida can be expect-
ed in habitats where C. firma and C. cervicornis have been
reported.
It is helpful to keep in mind that the distribution
models generated here only included climatic variables,
but the soil conditions, key in the distribution of this spe-
cies, were not included. Cladonia subturgida is restricted
to acid pH substrates (Burgaz and Ahti 2009), and many
of the areas potentially suitable for the species from a
climatic standpoint present a basic pH (gypsisols or
calcisols), therefore it is probable that this model over-
predicts C. subturgida distribution. For example, a large
part of the north of Morocco, a great part of Sicily, some
of the selected areas of Cyprus, and some locations of
southern England present calcareous substrates (Jones
et al. 2010,2013;Cohenetal.2012;Soilscape,https://
www.landis.org.uk/soilscapes).
According to our results, the distribution of C. subturgida
would be similar to that of C. firma, that grows in the south-
west of Europe, the north of Africa, the Macaronesia, the west
of Asia, occasionally the English Channel islands and south-
ern Britain (Burgaz and Ahti 2009;James2009;Nimis2016).
In general, both species live together in bare soils, roadside
slopes and shrubland clearings in the Iberian Peninsula
(Burgaz and Ahti 2009).
Table 3 Analyses of molecular
variance (AMOVA) among pop-
ulations from different geograph-
ical areas (Iberian Peninsula,
France, Italy and Greece)
d.f. S.S Variance % variation Fst Pvalue
Among populations 3 1.043 0.00611 2.17915 0.02179 0.13196
Within populations 45 12.345 0.27433 97.82085
Total 13.388 0.28044
Table 5 Relative contribution of each bioclimatic variable to the
Maxent model, calculated with jackknife test
Bioclimatic variables Relative importance (%)
Precipitation of Warmest Quarter 25.6
Annual Precipitation 37.3
Temperature Seasonality 19.3
Mean Temperature of Driest Quarter 1.8
Annual Mean Temperature 9.9
Mean Temperature of Coldest Quarter 6
Table 4 AUC values for
the distribution models
with selection of
variables estimated
Method AUC value
MAXENT 0.989
GAM 0.970
GLMs 0.948
MARS 0.960
14 Pino-Bodas R. et al.
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The most relevant climatic variables in the distribution
model for C. subturgida are those related to precipitation.
Litterski and Ahti (2004) had already pointed out that humid-
ity is the most important limitant climatic factor in the distri-
bution of Cladonia species, in fact more than temperature.
Species distribution models have proved that the variables
related to precipitation are the key ones to predict the distri-
bution of other Mediterranean species such as Solenospora
candidans,S. grisea and S. olivacea subsp. olbiensis
(Guttová et al. 2019).
4.2 Chemical and genetic variation of Cladonia
subturgida across its distribution
As previous studies have proved (Burgaz and Ahti 2009;
Pino-Bodas et al. 2012), Cladonia subturgida is a chemically
highly variable species. The study of the new specimens
gathers together all the six chemotypes found by Pino-Bodas
et al. (2012). In accordance with previous findings, the
commonest chemotype is the one that contains atranorin and
protolichesterinic acid, occasionally accompanied by zeorin.
The chemical variation is not homogeneous across the geo-
graphical distribution of the species, the Greek populations
being the most variable. Specifically five chemotypes have
been found in Crete (Table 1).
Genetically C. subturgida is not a very variable species and
has a weak geographical structure; there is gene flow among
the different regions of the Mediterranean basin. This species
reproduces both sexually and asexually but, due to the low
frequence of apothecia, it is assumed that asexual reproduc-
tion, by means of the dispersion of thallus fragments, is dom-
inant. Therefore, the low genetic variation found was
expected, since selection usually affects more directly the ge-
netic variation in asexual species, making most of the loci to
be effectively linked (Domaschke et al. 2012). However, a
pronounced population structure would be expected due to a
lower dispersal capacity of vegetative propagules against
spores (Werth 2010; Seymour et al. 2005). But similar results
were found in other lichens with dominant asexual
reproducction (Werth and Sork 2008), which means that
long-distance dispersal of the vegetative propagules is effec-
tive. In addition to wind (Muñoz et al. 2004), dispersion
through seas (Bailey 1968; Jahns et al. 1976;Søchtingand
Castello 2012) and birds (Bailey and James 1979;Armstrong
1987;Wedin1995) have been proposed as dispersal mecha-
nisms in lichens.
Though it is not easy to establish comparisons with other
studies (based on different markers and different geographical
scales) it is necessary to note that the lack of a geographical
structure is a recurent pattern found in several species of the
genus Cladonia (Myllys et al. 2003;Yahretal.2006;Parketal.
2012; Pino-Bodas et al. 2017). Which means that, in general,
Cladonia species have a great dispersal ability and the success
of the settlements will be determined by ecological factors.
In some studies about population genetics in the
Mediterranean region, some patterns similar to those of
Cladonia subturgida have been found, i.e. with scarce genetic
variation and populations geographically little structured, for
example in Buellia zoharyi (Chiva et al. 2019)andParmelina
carporhizans (Alors et al. 2017). The lack of geographical
structure has been attributed to the high dispersal capacity of
the species, to the absence of geographical barriers (Alors
et al. 2017) and to the fact that the habitats were not affected
by glaciations.
Fig. 3 Consensus distribution
model for Cladonia subturgida in
Europe based on Maxent, GAM,
GLM and MARS methods with
selection of variables
15 (Cladoniaceae, Lecanoromycetes), an overlooked, but common species in the Mediterranean...
Cladonia subturgida
Content courtesy of Springer Nature, terms of use apply. Rights reserved.
5 Conclusions
A knowledge of the species distribution as well as the genetic
variation pattern needs to be substantial in order to predict the
impact that anthropic disturbances and climatic change will
have on them and consequently take appropriate measure for
conservation purposes. In many cases, however, this implies a
challenge difficult to confront, especially for those species
difficult to identify (Allen and McMullin 2019). Therefore,
species distribution models can be of great help to identify
suitable areas for the species and to efficiently plan the sam-
plings (Hao et al. 2020). Our data, along with the potential
distribution models generated in this study, indicate that
C. subturgida is a species widely distributed in the
Mediterranean region in the Thermomediterranean,
Mesomediterranean and Supramediterranean belts.
Acknowledgments This study was funded by the project CGL2013-
41839-P, Ministry of Economy and Competitiveness (MINECO),
Spain. R. P-B was supported by Juan de la Cierva-incorporación 2015-
23526, MINECO and a pilot project from Kew foundation.
Open Access This article is licensed under a Creative Commons
Attribution 4.0 International License, which permits use, sharing,
adaptation, distribution and reproduction in any medium or format, as
long as you give appropriate credit to the original author(s) and the
source, provide a link to the Creative Commons licence, and indicate if
changes were made. The images or other third party material in this article
are included in the article's Creative Commons licence, unless indicated
otherwise in a credit line to the material. If material is not included in the
article's Creative Commons licence and your intended use is not
permitted by statutory regulation or exceeds the permitted use, you will
need to obtain permission directly from the copyright holder. To view a
copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
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