.sciencedirect.com

f u n g a l e c o l o g y 1 3 ( 2 0 1 5 ) 7 7e8 2

available at www

ScienceDirect

journal homepage: www.elsevier .com/locate/ funeco

Local dispersal dynamics determine the occupiedniche of the red-listed lichen Seirophora villosa(Ach.) Fr€od�en in a Mediterranean Juniperusshrubland

Paolo GIORDANIa,b,*, Renato BENESPERIc, Mauro Giorgio MARIOTTIa

aBotanic Centre Hanbury, DISTAV, Universit�a di Genova, ItalybDIFAR, Universit�a di Genova, ItalycDepartment of Biology, Universit�a di Firenze, Via La Pira, 4, I50121 Firenze, Italy

a r t i c l e i n f o

Article history:

Received 12 February 2014

Revision received 12 June 2014

Accepted 28 July 2014

Available online

Corresponding editor: Darwyn Coxson

Keywords:

Coast

Connectivity

Lichens

Mediterranean

Threatened species

* Corresponding author. Botanic Centre HanE-mail address: giordani@dipteris.unige.i

http://dx.doi.org/10.1016/j.funeco.2014.08.0081754-5048/ª 2014 Elsevier Ltd and The Britis

a b s t r a c t

The red-listed lichen Seirophora villosa is associated with undisturbed coastal dune systems

dominated by Juniperus spp. The clustered distribution of this species suggests that prop-

agative traits may be responsible for its conservation status. We tested whether the local

distribution of an S. villosa population under undisturbed conditions is limited by habitat

filtering or by low dispersal fitness. Using Strip Adaptive Cluster Sampling, we estimated

the size of one of the largest undisturbed Italian populations of S. villosa. We considered the

abundance of both mature and juvenile thalli in relation to geographical and environ-

mental spaces. Multiple regression on distance matrices models were in accordance with

the hypothesis that S. villosa is occupying only a small portion of its colonizable niche

because of a very limited propagation ability. Apart from the co-occurrence of mature

thalli, the presence of juvenile thalli was independent of pure spatial and environmental

factors.

ª 2014 Elsevier Ltd and The British Mycological Society. All rights reserved.

Introduction These habitats are presently threatened worldwide owing

Epiphytic lichens are an ecologically important component

of coastal Juniperus habitats, which are characterized by

assemblages of predominantly Mediterranean-distributed

species restricted to coastal ranges (Nimis and Schiavon,

1986). One such epiphytic lichen, Seirophora villosa, is a red-

listed macrolichen (Nascimbene et al., 2013) strictly asso-

ciated with dune environments such as coastal Juniperus

shrublands (Natura 2000 priority habitat code 2250*).

bury, DISTAV, Universit�at (P. Giordani).

h Mycological Society. Al

to various anthropogenic pressures, such as urban coastal

development, tourism, habitat fragmentation, alien species

introduction and coastal erosion (Mclachlan and Brown, 2006;

Picchi, 2008; Prisco et al., 2012; Bertacchi and Lombardi, 2014).

The distribution of S. villosa is spatially clustered on both

large and local scales (Fr€od�en and Lassen, 2004). The large-

scale clustering is mainly due to the effect of habitat frag-

mentation caused by anthropogenic and natural disturbances

such as tourism pressure or dune erosion (Benesperi et al.,

di Genova, Corso Dogali, 1M, I-16136 Genova, Italy.

l rights reserved.

78 P. Giordani et al.

2013). On a local scale, the clustered distribution of S. villosa is

purportedly driven by both environmental filtering and the

species’ dispersal capability as previously reported for other

epiphyte species (€Ockinger et al., 2005; Schei et al., 2012).

However, the importance of different predictors seems to vary

with spatial scale (McGill, 2010).

Dispersal is a process fundamental for the persistence and

dynamics of a population (Levin et al., 2003). Its relevance in

shaping population distribution is particularly important in

organisms whose habitats exhibit spatiotemporal dynamics

and in patch-tracking organisms, such as several epiphytic

lichens (Sn€all et al., 2005; Werth et al., 2006).

The recruitment of new individuals in lichen populations

depends on two non-mutually exclusive processes (Werth

et al., 2006): dispersal limitation, i.e., a limited availability of

propagules in a given habitat (€Ockinger et al., 2005; Belinch�on

et al., 2009), and establishment limitation, i.e., the inability of

young individuals to become established in a given habitat

due to interactions with biotic and/or abiotic factors. This

issue recurs in epiphytic communities independently by the

colonized habitat. For example, Schei et al. (2012) showed that

both local dispersal and environmental conditions influence

the spatial distribution and abundance of epiphytic lichen

species of the Lobarion community at fine spatial scales, in

contrast with the assumption of McGill (2010) who suggests

that microclimate and dispersal are more important than

habitat-related factors at scales < 102 m.

According to metapopulation theory, both local habitat

availability and habitat isolation are important in determin-

ing a species’ distribution (Hanski, 1999), so that sometimes

species may not be able to colonize all suitable habitat

because they cannot disperse to isolated habitat fragments

(Johansson and Ehrl�en, 2003). The abiotic niche of a species,

defined using only scenopoetic variables, contributes to shape

its colonizable niche. Reductions of the abiotic niche, due to

competition and dispersal restrictions, lead to the occupied

niche (Sober�on, 2007).

In this work, we explored the colonizable versus the

occupied niche of S. villosa in one of its larger, undisturbed

populations situated at the Feniglia dune system (Tuscany,

Italy). Basing on a Strip Adaptive Cluster Sampling procedure

and by applying unbiased HorwitzeThompson estimators to

the sampled data, we calculated the total abundances of

both mature and juvenile thalli in the entire dune system.

Then, we used the detailed plot-level dataset for testing two

alternative hypotheses for the propagation of S. villosa.

According to the first hypothesis, S. villosa is presently

occupying most of its potential niche because many parts of

the Juniperus shrubland are not a suitable habitat for this

species. In this case, the environmental predictors would

play a decisive role in shaping the abundance of both mature

and juvenile thalli within the population. The second

hypothesis predicts that the occupied niche of S. villosa is

considerably smaller than its colonizable area because of the

poor dispersal performance of the species. If the second

hypothesis is correct, the effects of pure space and/or the

abundance of mature thalli on the occurrence of juvenile

thalli should overcome those of environmental factors, the

juvenile thalli being in strict relation with the occurrence of

mature thalli at the same site.

Methods

Seirophora villosa is a fruticose lichen with compressed-

canaliculate laciniae, a hispid villose cinereous upper side,

and a whitish, naked lower side. Apothecia are usually pres-

ent, and are sub-apical, concave, and with red disks. In the

Mediterranean basin this lichen is widespread, but not com-

mon, along the coasts of Spain, Portugal, Italy, the Greek

islands, Israel and North Africa (Fr€od�en and Lassen, 2004). In

Italy, S. villosa has a western distribution along the peninsula

(Nimis and Martellos, 2008), occurring in Tuscany, Latium,

Campania, Sardinia and Sicily, where it grows on twigs of

shrubs and trees (mainly Juniperus spp.) exposed to frequent

humid maritime winds on sand dunes (Benesperi and Ravera,

2011).

The Duna Feniglia State Nature Reserve is a protected area

encompassing Special Protection Area IT51A0028 (92/43 CEE

Directive) in the coastal region of Southern Tuscany (Italy).

Occupying an area of 474 ha, the reserve includes three main

vegetational zones: a band overlooking the sea, consisting of

typical coastal dune with psammophilous plants and a pri-

ority habitat with Juniperus spp. (Natura 2000 code 2250*), a

central belt covered by Italian stone pine forest, and a nar-

rower band with mixed pine-broadleaved species.

Preliminary observations of the survey area revealed a

clustered distribution of the S. villosa population. We, there-

fore, applied strip adaptive cluster sampling (SACS), which in

the case of non-homogeneous distribution of a target pop-

ulation gives better performance than the usual non-adaptive

strategies (Pontius, 1997). SACS is based on two-level sam-

pling, with a biased selection of sampling units. We randomly

selected 15 primary units (strips) all along the dune system

(Fig 1). Each strip was divided into secondary units, which

were represented by 5 � 5 m square plots extending from the

sea front to the back edge of the Juniperus shrubland across the

dune. If S. villosa occurred in a secondary unit selected by the

initial sample, we inspected every secondary unit in its

neighborhood (Fig 2). Similarly, if S. villosa was found in a

neighboring secondary unit, then every unit in that unit’s

neighborhood was inspected. This process continued until no

additional secondary units hosting thalli were identified. The

set of all such units in which S. villosa occurred was defined as

the network associated with the initial sample. In this man-

ner, we investigated a total of 92 secondary sampling units.

We visually counted both juvenile and mature thalli on

each shrub and summed themper plot. Thalli thatwere<3 cm

in diameter and lacking apothecia were considered to be

‘juvenile’. To control for the effect of thallus detectability, we

carried out quality assurance procedures on a subset of plots,

fixing the accuracy threshold at 80 %with respect to the count

obtained by a control team.

For each plot, a set of environmental predictors potentially

related to the establishment success of juvenile thalli was

recorded in the field or obtained from cartographic data,

including number of shrub species within the plot, average

trunk circumference, total number of shrubs, distance of the

plot from the sea, and the angle between the shrubland front

and the main wind direction. We calculated pairwise dis-

similarity matrices for geographic distance between plots

Fig 1 e Location of the primary sampling units (strips) in the Feniglia dune system.

Niche of the lichen Seirophora villosa 79

(Euclidean distance), the environmental predictors and the

abundance of both juvenile and mature thalli (BrayeCurtis

distance).

We used HorvitzeThompson unbiased estimators to esti-

mate the number of sub-populations and the total number of

mature and juvenile thalli in the survey area. Based on the

HorvitzeThompson estimator of the parametric total

(Thompson, 1990), an unbiased estimator of s is defined as

bs ¼Xk

k¼1

ykIkak

:

where yk is the number of thalli sampled in plot k, Ik ¼ 1 if

network k is intersected by at least one primary unit in the

initial sample, and 0 otherwise, and ak is the probability that

network k is intersected by at least one primary unit in the

initial sample.

Fig 2 e Magnification of the area enclosed in the frame of Fig 1.

indicating the strip randomly selected as primary sampling unit

the network (i.e. those sampling units where S. villosa occurred

occur. The gray scale of the shading is proportional to the abund

the abundances of mature thalli.

We performed a multiple regression on distance matrices

(MRM) analysis (Legendre et al., 1994) to detect the relevance of

space and environment in shaping the abundance of both

juvenile and mature thalli producing sexual spores. MRM

involves a multiple regression of a response matrix on any

number of explanatory matrices (Lichstein, 2007). In our case,

the abundances ofmature or of juvenile thalli were used in two

separate analyses as response matrices, whereas spatial and

environmental for both response matrices and distance of

abundance of mature thalli when the abundance of juveniles

was used as a response matrix. Each matrix contained dis-

tances between all pair-wise combinations of sample units.

Testsof statistical significancewereperformedbypermutation.

We applied a Mantel test (Legendre and Legendre, 1998)

to test the relationship between dissimilarity matrices for

mature thalli abundance and geographic distance. The shape

The layout of network 3 (see Table 1) is reported, the arrow

. Shaded squares represent the secondary units enclosed in

) and the surrounding edge units where the species did not

ance of juvenile thalli, whereas numbers in the squares are

Table 1e Sampled networks andHorvitzeThompson unbiased estimators of total numbers of juvenile andmature thalli inthe survey area

Network No. secondarysampling units

Total no.of thalli

Total no.juvenilethalli

Total no.maturethalli

Total no.colonizedshrubs

Shrubs colonizedby juvenile thalli

Shrubs colonizedby mature thalli

1 6 293 259 34 11 10 6

2 14 222 168 54 21 16 14

3 23 3 428 3 114 314 125 110 51

4 1 1 1 0 1 1 0

HT estimates

(total � st. dev.)

47 403 � 10 317 41 845 � 12 204 5 558 � 969 2058 � 503 1854 � 505 1 051 � 277

80 P. Giordani et al.

of the relationship was then evaluated calculating a Mantel

correlogram. A Mantel coefficient obtained in this fashion can

be interpreted as a parametric Pearson correlation among

similarity indices. Statistical significance ofMantel test results

was assessed using a randomization approach with 999 per-

mutations. A progressive Bonferroni correction was used to

account for multiple testing (Legendre and Legendre, 1998).

Distance matrix construction, Mantel testing and MRM

analysis were performed in the R statistical environment

(R Development Core Team, 2013) using the ecodist package

(Goslee and Urban, 2012).

Results

By means of SACS, we detected four networks of sampling

units occupied by S. villosa. Network extension and abundance

were quite uneven, the latter ranging from only one sampled

thallus tomore than 3 000 (Table 1). Using HorvitzeThompson

estimators, we calculated that the overall population of S.

villosa at the Feniglia dune system comprised more than

47 000 thalli. Nearly 90 % of individuals were juvenile, with

only about 6 000 mature apothecia-producing thalli recorded.

The entire population colonized only about 2 000 shrubs

(mostly J. phoenicea), half of which hosted mature thalli. Hor-

vitzeThompson estimators produced 67 clustered sub-

populations (density ¼ 0.28 ha�1), with a median extension

area of 25 m2.

MRM showed that spatial distance matrix had a significant

effect on the abundance of mature thalli, whereas the effects

of environmental distance matrix was negligible and non-

significant (Table 2). The Mantel correlogram revealed a clear

trend of dissimilarity of mature thalli in relation to geographic

distance,withpositivesignificantautocorrelations(rM¼�0.147;

p < 0.05) at distances <199 m and negative autocorrelations

Table 2 e Multiple regression on distance matrices (MRM) spacjuvenile thalli of Seirophora villosa at Feniglia

Response dissimilarity matrix F

Space

Abundance of mature thalli 49.7* �5.068 10�5*

Abundance of juvenile thalli 466.8** �1.605 10�5

*p < 0.05; **p < 0.05.

(0.05< rM< 0.10) at various lagdistances>1 300m.According to

the MRM analysis only mature thalli dissimilarity showed a

significant effect (Table 2). The effects of both spatial and envi-

ronmental distances were negligible and non-significant.

Discussion

The S. villosa population was abundant at Feniglia, and

included a considerable number of juvenile thalli, suggesting

high spore production and good population fitness. On the

other hand, mature thalli producing sexual spores were rela-

tively rare, and were scattered throughout the Juniperus

shrubland and clustered into very small sub-populations.

The small, non-significant effect of environmental dis-

tance on S. villosa abundance leads us to reject our first

hypothesis that the species is presently occupying most of its

potential niche. Potentially, the entire Juniperus shrubland is a

suitable habitat, thus representing the colonizable niche for

the lichen. This conclusion is also supported by the high

positive spatial autocorrelation of mature thallus abundance,

which was only observed at smaller lag distances (<200 m).

In accordance with our second hypothesis, we demon-

strated that S. villosa is only occupying a small part of its col-

onizable niche at Feniglia. Despite its relatively high

reproductive rate (ca. 7.5 juvenile thalli/mature thallus), the

species possesses a very low dispersal ability within the dune

system, as evidenced by the fine-scale independence of

juvenile thallus occurrence from pure spatial and environ-

mental factors, apart from the co-occurrence of mature thalli.

Generally, the supply of propagules in lichens is expected to

exponentially decrease with increasing distance from the

source (Sillett et al., 2000). Accordingly, it was demonstrated

that trees colonized by the rare epiphytic lichen Lobaria pul-

monaria are clustered around important propagule sources

e/environment models for abundances of mature and

Predictor dissimilarity matrices

Environment Abundance of mature thalli

* 8.838 10�3 ns N/Ans 0.128ns 0.468**

Niche of the lichen Seirophora villosa 81

(Werth et al., 2006). This is possibly related to the fact that the

probability of successful establishment generally increases

with the number of deposited propagules (see Gravel et al.,

2008). In this regard, it was shown that the abundance of

epiphytic lichen individuals is best explained by the sum of

individuals in the immediate neighborhood (Schei et al., 2012).

That being said, differences in colonization capacity in lichen

species can be explained by differences in reproductive

strategy (Gjerde et al., 2012), with species producing sexual

spores being more adapted to long-range dispersal than those

propagating by vegetative propagules (Heden�as and Ericson,

2000). However, the importance of local dispersal vs. envi-

ronmental filtering for species dispersing with sexual versus

asexual propagules seems to be unimportant at fine spatial

scale (Schei et al., 2012). Our data on the pattern of abundance

of the sexual reproducing S. villosa seem to support the fact

that spores do not always ensure an effective dispersal at

small or medium scale. Possibly, the spores, micro-

morphology and the mechanisms of dispersion might be

fundamentally responsible for this. The small, light spores of

S. villosa (10e15 � 5e7 mm) are hosted in 8-spored asci and are

dispersed by sea winds. The high humidity and high salt

concentration under these conditions might aggregate the

spores, reducing their dispersal distance.

Benesperi et al. (2013) have demonstrated the dependence

of S. villosa on undisturbed Juniperus stands showing a sig-

nificant effect of disturbance on the presence and abundance

of this lichen species. Although Juniperus shrublands are pri-

ority habitats, human activities in littoral areas are still

widespread and common. The low propagation ability of S.

villosa and its clumped distribution, as highlighted in our

study, suggests that sporadic habitat disturbance events

causing vegetation loss, e.g. due to localmaintenancework for

tourist facilities or opening in the shrubland for excessive

trampling, can also trigger the decline in communities of this

red-listed species, even in well-preserved habitats set aside

for its conservation.

Acknowledgment

This research was carried out under the project COREM

(Cooperazione delle Reti Ecologiche nel Mediterraneo) of the

Operational Programme Italy e Maritime France 2007e2013,

financed by European Regional Development Fund (ERDF).

r e f e r e n c e s

Belinch�on, R., Mart�ınez, I., Ot�alora, M.A.G., Arag�on, G., Dimas, J.,Escudero, A., 2009. Fragment quality and matrix affectepiphytic performance in a Mediterranean forest landscape.American Journal of Botany 96, 1974e1982.

Benesperi, R., Ravera, S., 2011. Seirophora villosa (Ach.) Fr€od�en.Informatore Botanico Italiano 43, 69e72.

Benesperi, R., Lastrucci, L., Nascimbene, J., 2013. Humandisturbance threats the red-listedmacrolichen Seirophora villosa(Ach.) Fr€od�en in coastal Juniperus habitats: evidence fromwesternpeninsular Italy.EnvironmentalManagement52, 939e945.

Bertacchi, A., Lombardi, T., 2014. Diachronic analysis (1954e2010)of transformations of the dune habitat in a stretch of theNorthern Tyrrhenian Coast (Italy). Plant Biosystems 148,227e236.

Fr€od�en, P., Lassen, P., 2004. Typification and emendation ofSeirophora Poelt to include species segregated fromTeloschistes Norman. Lichenologist 36, 289e298.

Gjerde, I., Blom, H., Lindblom, L., Sætersdal, M., Schei, F.H., 2012.Community assembly in epiphytic lichens in early stages ofcolonization. Ecology 93, 749e759.

Goslee, S., Urban, D., 2012. Ecodist: Dissimilarity-based Functionsfor Ecological Analysis (R-package) http://cran.r-project.org/web/packages/ecodist.

Gravel, D., Beaudet, M., Messier, C., 2008. Partitioning the factorsof spatial variation in regeneration density of shade toleranttree species. Ecology 89, 2879e2888.

Hanski, I., 1999. Habitat connectivity, habitat continuity, andmetapopulations in dynamic landscapes. Oikos 87, 209e219.

Heden�as, H., Ericson, L., 2000. Epiphytic macrolichens asconservation indicators: successional sequence in Populustremula stands. Biological Conservation 93, 43e53.

Johansson, P., Ehrl�en, J., 2003. Influence of habitat quantity,quality and isolation on the distribution and abundance of twoepiphytic lichens. Journal of Ecology 91, 213e221.

Legendre, P., Lapointe, F.J., Casgrain, P., 1994. Modeling brainevolution from behavior: a permutational regressionapproach. Evolution 48, 1487e1499.

Legendre, P., Legendre, L., 1998. Numerical Ecology, second edn.Elsevier, Amsterdam.

Levin, S.A., M€uller-Landau, H.C., Nathan, R., Chave, J., 2003. Theecology and evolution of seed dispersal: a theoreticalperspective. Annual Review of Ecology and Systematics 34,575e604.

Lichstein, 2007. Multiple regression on distance matrices: amultivariate spatial analysis tool. Plant Ecology 188, 117e131.

McGill, B.J., 2010. Matters of scale. Science 328, 575e576.Mclachlan, A., Brown, A.C., 2006. The Ecology of Sandy Shores.

Academic Press, Burlington, MA, USA.Nascimbene, J., Nimis, P.L., Ravera, S., 2013. Evaluating the

conservation status of epiphytic lichens of Italy: a red list.Plant Biosystems 147, 898e904.

Nimis, P.L., Martellos, S., 2008. ITALIC, The Information Systemon Italian Lichens. Version 4.0. University of Trieste, Dept. ofBiology. IN4.0/1 http://dbiodbs.univ.trieste.it.

Nimis, P.L., Schiavon, L., 1986. The epiphytic lichen vegetation ofthe Tyrrhenian coast in central Italy. Annali di Botanica 44,39e67.

€Ockinger, E., Niklasson, M., Nilsson, S.G., 2005. Is localdistribution of the epiphytic lichen Lobaria pulmonaria limitedby dispersal capacity or habitat quality? Biodiversity andConservation 14, 759e773.

Picchi, S., 2008. Management of Natura 2000 habitats. 2250*Coastal dunes with Juniperus spp. European Commission.

Pontius, J.S., 1997. Strip adaptive cluster sampling: probabilityproportional to size selection of primary units. Biometrics 53,1092e1096.

Prisco, I., Acosta, A.T.R., Ercole, S., 2012. An overview of the Italiancoastal dune EU habitats. Annals of Botany 2, 39e48.

R Development Core Team, 2013. R: A Language and Environmentfor Statistical Computing. R Foundation for statisticalcomputing, Vienna, Austria, ISBN 3-900051-07-0. URL http://www.R-project.org.

Schei, F.H., Blom, H.H., Gjerde, I., Grytnes, J.-A., Heegaard, E.,Sætersdal, M., 2012. Fine-scale distribution and abundance ofepiphytic lichens: environmental filtering or local dispersaldynamics? Journal of Vegetation Science 23, 459e470.

Sillett, S.C., McCune, B., Peck, J.E., Rambo, T.R., Ruchty, A., 2000.Dispersal limitations of epiphytic lichens result in species

82 P. Giordani et al.

dependent on old-growth forests. Ecological Applications 10,789e799.

Sn€all, T., Pennanen, J., Kivist€o, L., Hanski, I., 2005. Modellingepiphyte metapopulation dynamics in a dynamic forestlandscape. Oikos 109, 209e222.

Sober�on, J., 2007. Grinnellian and Eltonian niches and geographicdistributions of species. Ecology Letters 10, 1115e1123.

Thompson, S.K., 1990. Adaptive cluster sampling. Journal of theAmerican Statistical Association 85, 1050.

Werth, S., Wagner, H.H., Gugerli, F., Holderegger, R.,Csenscsics, D., Kalwij, J.M., Scheidegger, C., 2006. Quantifyingdispersal and establishment limitation in a population of anepiphytic lichen. Ecology 87, 2037e2046.