Biodiversity

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From cold to warm-stage refugia for boreo-alpine

plants in southern European and Mediterranean
mountains: the last chance to survive or an
opportunity for speciation?
Rodolfo Gentili, Gianluigi Bacchetta, Giuseppe Fenu, Donatella Cogoni,
Thomas Abeli, Graziano Rossi, Maria Cristina Salvatore, Carlo Baroni &
Sandra Citterio
To cite this article: Rodolfo Gentili, Gianluigi Bacchetta, Giuseppe Fenu, Donatella Cogoni,
Thomas Abeli, Graziano Rossi, Maria Cristina Salvatore, Carlo Baroni & Sandra Citterio
(2015): From cold to warm-stage refugia for boreo-alpine plants in southern European and
Mediterranean mountains: the last chance to survive or an opportunity for speciation?,
Biodiversity, DOI: 10.1080/14888386.2015.1116407
To link to this article: http://dx.doi.org/10.1080/14888386.2015.1116407

Published online: 11 Dec 2015.

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BIODIVERSITY, 2015
http://dx.doi.org/10.1080/14888386.2015.1116407

From cold to warm-stage refugia for boreo-alpine plants in southern European and
Mediterranean mountains: the last chance to survive or an opportunity for speciation?
Rodolfo Gentilia*, Gianluigi Bacchettab, Giuseppe Fenuc, Donatella Cogonib, Thomas Abelid, Graziano Rossid,
Maria Cristina Salvatoree, Carlo Baronie and Sandra Citterioa
a

Dipartimento di Scienze dellAmbiente e del Territorio e di Scienze della Terra, Universit degli Studi di Milano-Bicocca, Milano,
Italy; bCentro Conservazione Biodiversit (CCB) Dipartimento di Scienze della Vita e dellAmbiente, Universit degli Studi di
Cagliari, Cagliari, Italy; cDipartimento di Biologia Ambientale, Sapienza Universit di Roma, Roma, Italy; dDipartimento di
Scienze della Terra e dellAmbiente, Universit di Pavia, Pavia, Italy; eDipartimento di Scienze della Terra, Universit di Pisa and
CNR, Istituto di Geoscienze e Georisorse, Pisa, Italy

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

(Received 29 June 2015; nal version received 1 November 2015)

During glacial phases of the Quaternary, Southern European and Mediterranean mountains (SEMms: Pyrenees, Apennines, Balkan Mountains, Maritime Alps, etc.) provided suitable habitats for numerous cold-adapted (boreo-alpine) plant
species migrating from northern regions, which have been described as cold-stage refugia. Speciation events occurred in
these refugia through adaptation and evolution by genetic differentiation; other species still survive as peripheral populations. In the current phase of climate change, SEMms are (macro-)refugia of great interest because they still host important populations of glacial relicts and alpine ora, often in isolated occurrences. Such species can be found in
topographic niches generally linked to peculiar landforms such as fossil glacial cirques, scree slopes and gorges that may
perform as warm-stage (micro-)refugia. We present a review on the boreo-alpine species living across SEMms with the
aim to describe their genetic patterns evolved during Quaternary climatic oscillations as well to highlight the role of
microtopographic/microgeomorphologic niches as microrefugium areas under the current scenario of climate change.
Keywords: interglacial refugia; microrefugia; macrorefugia; genetic refugia; cryptic refugia; species resilience; migration;
evolution; genetic differentiation; climatic change

Introduction
Alpine species occurring across mountains of Europe
have been estimated to be 2025% of European total
plant diversity, but the peak of plant diversity, where
most of the endemic species occurs, is concentrated in
Southern European and Mediterranean mountains
(SEMms hereafter) such as the Pyrenees, Apennines, and
Balkan Mountains (Gaviln et al. 2013; Nagy and Grabherr 2009). It is widely accepted that such biodiversity
originated, in great part, during Quaternary climate oscillations (Mansion et al. 2008). Based on the glacial refugia hypothesis, during the last glacial periods (Riss and
Wrm Auct.) boreo-alpine plants migrated from the
north toward southern areas of Europe. Several refugia
have been identied in the southern sectors of the Alps
(e.g. Maritime Alps) and the Mediterranean Basin with
reference to Iberian, Italian and Balkan Peninsulas
(Hewitt 1999; Taberlet et al. 1998).
Mdail and Diadema (2009), in a comprehensive
review on the Mediterranean Basin, provided for the rst
time a ne scale delimitation of Mediterranean refugia.
These authors identied 52 putative refugia, considering
as a refugium an area whose existence implies the local
*Corresponding author. Email: rodolfo.gentili@unimib.it
2015 Biodiversity Conservancy International

long-term (one or more glacialinterglacial cycles) persistence of a species or of one or more of its component
populations within a well-dened geographical area (e.g.
mountain peak, gorge). Mdail and Diadema (2009) classied the Mediterranean putative refugia in three main
types: (a) moist mid-altitude refugia (about 400800 m),
which would have allowed altitudinal shifts in response
to climate changes or the in situ persistence of species
(type 1); (b) deep gorges or closed valleys with constant
moisture availability owing to the protected microenvironment (type 2); and (c) refugia of mesophilous trees
located in low-altitude areas (type 3). Of the total refugia
identied, 60% (33) are situated in Mediterranean submontane and mountain margins, such as the High and
Middle Atlas, the Rif Mountains in North Morocco, the
Sierras of Andalusia, the Maritime and Apuan Alps, the
Balkan Mountains and the Taurus in Turkey. Mountain
ranges and nunataks have played an important role in
the survival of small and isolated populations of herbs
and shrubs, even mesothermic species, during glacial
periods. For example, the Sierra Nevada mountains
(Spain) that represent the southernmost limit of the
inuence of the Quaternary glaciations in Europe were

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R. GENTILI ET AL.

glaciated only above c. 2500 m (Gmez et al. 2001) and

large areas remained free of permanent ice, favouring the
persistence and diversication of local alpine plant
species (Kropf, Comes, and Kadereit 2006).
After glacial periods, a post-glacial recolonisation
process has been acknowledged with a back-migration of
the same species following two main patterns (Hewitt
1999): (a) toward northern regions; (b) toward higher
elevation in SEMms and in the Alps, in areas that can
be identied as warm-stage refugia.
Rull, Schubert, and Aravena (1988) introduced the
terms microrefugium and macrorefugium, referring with
the former to a small area with local favourable environmental features suitable for populations/species survival,
protected from the unfavourable regional environmental
conditions, and with the last to a large-scale refugium
that may form from a contracting main (continuous)
range (Rull 2009).
Due to the numerous studies dealing with the glacial
refugia hypotheses, the term refugium is usually associated with warm places within a cold context, while the
converse phenomenon of interglacial refugia has been
relatively neglected (Birks and Willis 2008; LpezGarca et al. 2010; Stewart et al. 2010). The microrefugium and macrorefugium concepts can be equally
applied to cold and warm climatic stages (Dobrowski
2011; Gentili et al. 2015a).
In particular, Gentili et al. (2015a) emphasised that
southern and marginal mountain chains across Europe
and the Mediterranean Basin hold macro- and microrefugia for relict alpine plant species; such mountains are the
Apennines, Dinaric Alps, Pyrenees, Central Massif, Jura,
Vosgi, Black Forest Mountains, Corsica and Balkan
Mountains. These mountain chains provide numerous
examples of warm-stage microrefugia that are often
linked to peculiar landforms (scree slopes, nivation
niches, moraine ridges, etc.) for boreo-alpine, EuroSiberian and orophitic plants (Gentili et al. 2015a).
So, the alternation of glacial and interglacial phases
across Europe has been the likely primary impulse to
divergences in plant populations of boreo-alpine species
through isolation (Hewitt 1996; Stevanovi et al. 2009;
Vargas 2003). Particularly, during interglacial periods,
some plant populations of boreo-alpine species have
found in southern refugia the edge of the species range
with isolated populations. In some cases such populations have developed under particular conditions (e.g.
niches or isolation in summit areas). Indeed, several isolated plant populations has challenged allopatric speciation/subspeciation events, resulting in a high number of
endemic taxa in SEMms (Alessandrini et al. 2003; Lobo,
Castro, and Moreno 2001; Lorite, Navarro, and Valle
2007; Stevanovi et al. 2009). For instance, geographical
speciation/subspeciation related to Pleistocene range
shifts and isolation phenomena have been documented

for several genera such as Reseda (Martin-Bravo et al.

2010) and Campanula (Kuss et al. 2011). Patterns of
diversication in boreo-alpine plant species in the
Mediterranean area have been certainly encouraged by
intrinsic factors (i.e. different bio-ecological characteristics) such as: genetic structure of populations, phylogenetic links, breeding system, dispersal ability and
ecological specialisation (Hewitt 2004; Vargas 2003). In
the Mediterranean areas, warm interglacial phases are
likely to have played a role in alpine species range
shifts, contraction of populations, population genetic drift
or bottlenecks. Thompson et al. (2005) pointed out that
isolated rocky habitats on cliffs and gorges with fewer
competitive interactions could have major effects on the
creation of endemic plants and in their persistence. In
addition, the deep variation of geographical distribution
of alpine species together with the geologic complexity
of the European continent, have also provided further
opportunities for speciation and hybridisation after secondary exchange (Comes and Kadereit 1998).
Indeed, the ongoing increasing temperatures due to
climate change are predicted to affect the majority of
alpine plant species as a consequence of a decreased
habitat suitability, which in turn will expose them to a
higher risk of extinction (Arajo et al. 2011; Thuiller
et al. 2005).
We suppose that the range of most of boreo-alpine
plant species is at its minimum during periods of warm
climate (interglacials), like the current period, and that
such species are often conned to mountain tops and
refugium areas in those areas characterised by warm
temperatures (i.e. SEMms). So the aim of this perspective paper is to discuss some views and topics on
warm-stage refugia to stimulate further research on
boreo-alpine plant species living in such areas. By
screening literature data, the specic goals of this work
were: (a) to investigate the patterns of genetic diversity
and evolution of isolated populations of boreo-alpine
species across SEMms and in relation to cold/warmstage refugia and past (cold/warm) climatic oscillations;
(b) to explore the knowledge on boreo-alpine species in
SEMms in relation to climate change studies; (c) to
highlight the role of microtopographic/microgeomorphologic niches as refugium areas (also with reference to
macro- and microrefugia) for boreo-alpine species
within.
Literature screening and denitions
Literature directly or indirectly related to arctic-alpine
species was screened through the following queries used
across the main online search engines (Web of Knowledge, Scopus, Google): boreo-alpine species* across
SEMms in relation to: refugia* (sensu lato), warm-/
cold-stage refugia*, climate changes*, genetic diversity*

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B I O D I V E R S I T Y
peripheral isolated population* and quaternary glacial/interglacial phases*.
Across the work we at rst refer to the classical concept of refugia/refugium as literature data report (Holder,
Montgomerie, and Friesen 1999). In the last two chapters
of the work we then refer to the term macro- and microrefugium according to Rull (2009) and based on the
interpretation made by Gentili et al. (2015a) for warm
stages.
As boreo-alpine plant species we intend, in a classic
sense, those that have their main occurrence above the
treeline and have their core distribution in boreal and
alpine regions, i.e. in the central or northern parts of
Europe and toward higher elevations on the Alps:
circumboreal, eurosibiric, orophitic, boreo-montane and
arctic-alpine elements. As regards more Mediterranean
mountains, some boreo-temperate (cold) species, typically present in the alpine region (above tree line) and in
northern Europe, were also included.
We refer to SEMms as follow: (a) Southern European
mountains: include the southernmost limits of Quaternary
glaciations in Europe that at present host only relict
element of the Mediterranean ora: Maritime Alps,
Apennines (Northern and Central), Apuan Alps,
Carpathians, Balkan Mountains (Dinaric Alps), Pyrenees
and Sierra Nevada, and also the highest peak of Corsica
mountains; (b) Mediterranean mountains: mountains that
host only relict elements of the boreo-alpine and temperate ora, mainly concentrated in refugium areas (sensu
Mdail and Diadema 2009); they comprise Moroccan
(Rif and Atlas), Sardinian (Gennargentu and Supramontes massifs), Sicilian (Etna and Madonie), Calabrian
(Aspromonte), Cretan (Lefka Ori and Psiloritis), Turkish
(Taurus mountains), Cypriot (Troodos mountain) and
Lebanese (Mount Lebanon and Anti-Lebanon)
mountains.
The boreo-alpine ora of SEMms
SEMms complex orogenetic history has produced geological and geomorphological heterogeneity as well as a
diversity of parent materials, for instance limestones, marble, siliceous rocks, ophiolites and so on. In addition,
SEMms often exhibit altitudinal gradients that are over a
few kilometres range from the sea level to more than
2000 m with different climatic regimes (Vogiatzakis
2012). For instance, the Pyrenees extend from the
Mediterranean Sea in the eastern part to the Atlantic
Ocean in the western. All these factors have contributed
to the current species richness of SEMms, which are in
large part included in the Mediterranean biodiversity
hotspot (Cuttelod et al. 2008), as they host numerous
endemic, steno-endemic and disjoint species, some of
which are relicts of earlier biogeographical patterns
(Mdail and Verlaque 1997). From a biogeographic point

of view, SEMms are located at the crossroads of different

bioregions so that their ora during Quaternary climatic
oscillations has enriched different phytogeographic
elements: Euro-Siberian, arctic-alpine, Irano-Turanian
species, often originated from the southward migration of
the alpine ora.
For instance, as regards the alpine ora present on
SEMms, Stevanovi et al. (2009) mapped the distribution
of 77 arctic-alpine species in the Balkans; they found
relationships between oristic richness and distribution
of arctic-alpine ora and altitude, geographical location
and geological substrate, respectively. Lorite, Navarro,
and Valle (2007) studied the orophitic (including alpine
species) and endemic ora of Sierra Nevada.
Alessandrini et al. (2003) in their high-mountain ora of
Northern Apennines (about 500 species) highlighted as
arctic-alpine and boreal elements represent the 35%,
while orophitic centro-european elements, including
some alpine endemics, represent the 28%.
As regards strictly Mediterranean mountains, boreoalpine generally species are represented by relict elements that persist in isolated habitats toward higher elevations. Data for these mountains are scarce or are
represented by grey literature or local oristic studies.
For instance, in the Moroccan High Atlas Mountains
geomorphological heterogeneity and slopes evolution
determine the existence of some alpine plant species,
such as Cerastium cerastioides (L.) Britton, Poa alpina
L. and Luzula spicata (L.) DC. (Alaoui Haroni, Alifriqui,
and Simonneaux 2009). The oristic study of Sicily
islands by Raimondo, Domina, and Spadaro (2010)
showed the occurrence of some relict boreo-alpine species in the Mediterranean mountains, such as Campanula
scheuchzeri Vill., Nardus stricta L., Minuartia verna (L.)
Hiern and so on.
a) The case of the Sardinian mountains
The topic of the SEMms ora is exhaustively covered in
Nagy et al. (2003), so hereafter we will only concisely
focus on the biodiversity of Sardinian mountains.
The Gennargentu, the most important Sardinian massif, represents a typical example of Mediterranean mountains that host only relict elements of the boreo-alpine
and temperate ora, mainly concentrated in small refugium areas (Bacchetta et al. 2013; Caadas et al. 2014).
In fact, the recent oristic study on the Gennargentu
massif highlights that the ora is mostly constituted by
Mediterranean taxa (68.14%) followed by the palaeotemperate chorotype (9.07%); the palaeotemperate elements
outline the temperatesub-Mediterranean bioclimate in
the summit areas of the massif, as well as on its northern
slopes (Bacchetta et al. 2013). The oristic richness of
the Gennargentu massif can be explained by hypothesising that during the Quaternary age, the less drastic

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R. GENTILI ET AL.

climate changes on large Mediterranean islands favoured

the local persistence of high plant richness and the
coexistence of distinct genetic lineages (Mdail and
Diadema 2009), conrming the identication of this area
as one of the Mediterranean putative refugia. For
instance, some more boreal species are present, such as
Gentiana lutea L subsp. lutea and Juniperus communis
L. subsp. alpina Gray (Bacchetta et al. 2013). Also the
Supramontes massif, according to Mdail and Diadema
(2009), holds several areas that can be considered refugia, such as the peak of Mount Corrasi and Monte Novo
San Giovanni, the deep gorge of Gorroppu or the closed
valleys (Codula di Luna, Sisine, Flumineddu and Orbisi)
where the climate stays locally wet during periods of
drought (Fenu et al. 2010).
Cogoni, Alef, and Scrugli (1999) in their oristic
study on the Sardinias bryological ora stressed on the
presence, among mosses, of a consistent group of boreal
species (18.8%) and, although to a lesser extent, the
presence of arctic-alpine species s.l. (4.8%) on the top
areas of Sardinian mountains, principally located on the
islands highest peaks and in particular on the Gennargentu massif. Among these, special mention should be
made of Bryum calophyllum R. Br., Grimmia pilosissima
Herzog, G. elatior Bruch ex Bals.-Criv. & De Not.,
Plagiothecium piliferum (Sw.) Schimp. and Weissia
wimmeriana (Sendtn.) Bruch & Schimp.
Additionally, Gennargentu and Supramontes massifs
should be also considered Southern European refugia
(sensu Tzedakis et al. 2002) for some boreo-temperate
shrub and tree species, for instance Rhamnus alpina L.
subsp. alpina and Taxus baccata L.
b) Peripheral isolated populations of boreo-alpine
species
Several populations of boreo-alpine species in Europe
remained isolated in warm-stage refugia located in
southern mountain chains, after the retrieval of warmer
conditions following the glacial phases (e.g. Escobar
Garca et al. 2012; Gentili et al. 2015a). Examples of
cold adapted species still surviving in southern sites, in
specic cold/fresh niches, are several in all the main
southern mountains. For instance, Saxifraga oppositifolia
L. is a circumboreal species with southern marginal
populations in the Apennines, Pyrenees and Rocky
Mountains (Winkler et al. 2012); Ranunculus glacialis
L. occurs in the High Arctic and in southern mountains
ranges like the Pyrenees and Alps (Ronikier,
Schneeweiss, and Schnswetter 2012) and so on.
Such populations are often at the edge of the species
range, so that southern refugia host the southernmost populations of many cold-adapted species (Jalas and Suominen 19721994; Tomaselli and Agostini 1994). These
geographically and sometimes ecologically peripheral

populations, usually isolated from central populations as a

consequence of range fragmentation, emphasise the role
of southern refugia in range limit formation and plant
adaptation (Jimnez-Mejas et al. 2012). According to the
abundant centre hypothesis (ACH), predictions are for a
lower population performance and decreased genetic variation (Brown, Mehlman, and Stevens 1995) in peripheral
vs. central populations. However, several recent studies
highlighted that geographically peripheral populations
may not be less genetically diverse, or less efcient in
terms of growth and reproductive performance than central populations (Abeli et al. 2014a; Eckert, Samis, and
Lougheed 2008).
An explanation may come from local meteorological
and long-term climatic data showing that southern refugia may be characterised by local climatic conditions
signicantly different from the surrounding regional
climate that may perfectly match the requirement of
northerly distributed species. For instance, Silene
suecica (Lodd.) Greuter & Burdet, a species distributed
in lowland areas of Fennoscandia, Iceland and Greenland other than in North America, occurs in southern
refugia in the Pyrenees, Alps and northern Apennines
with several isolated populations. Interestingly, the
southernmost site of this species located in the Northern
Apennines (Italy) is colder than some sites of occurrence in central Sweden (Abeli et al. 2015). This
suggests that geographically marginal populations of
boreo-alpine species may not necessarily be ecologically
marginal (Soul 1987). In other words, in contrast to
the expectation that marginal populations tend to occur
in less suitable environments than central populations,
ecological conditions of southern refugia may be closer
to the ecological optimum of a given species than sites
in the core area of distribution.
Identifying macro- and microrefugia for boreo-alpine
species in SEMms
To understand the current patterns of genetic diversity of
plant groups in SEMms, the impact of climatic oscillations over the past two million years should be considered (Nieto Feliner 2011). In fact glacialinterglacial
phases during the Pleistocene promoted isolation and
speciation of boreo-alpine plants in SEMms during warm
(interglacial) periods and connections and gene ow during cold (glacial) periods (Vargas 2003). Hybridisation,
genetic drift and gene ow are the major evolutionary
mechanisms that were involved in the shaping of the
present morphologic and genetic (and taxonomic) diversities of numerous SEMms species (Fuertes Aguilar,
Gutirrez Larena, and Nieto Feliner 2011) within refugium areas.
Studies on the phylogeography of orophitic plants
in Mediterranean mountains suggest three main

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B I O D I V E R S I T Y
congurations of spatial segregation and genetic diversity
(see also Jimnez-Mejas et al. 2015):
a) Peripheral isolated populations of widespread
boreo-alpine species include species/populations
that have not yet faced a speciation event because
of the recent isolation or separation and/or the
maintenance of a certain degree of gene ow
between populations [Jimnez-Mejas et al. 2012;
i.e. Carex nigra (L.) Reichard complex]. In particular, the reduced gene ow between marginal/marginal and marginal/central populations and the
directional selection at the range edge is known to
promote the differentiation of marginal populations, and consequently their evolutionary potential (Sexton et al. 2009). Peripheral populations
hold an evolutionarily potential for future speciation events favoured by isolation, genetic drift or
bottlenecks phenomena.
b) Speciation events with high genetic differentiation
through long-term isolation (genetic drift). Populations have been isolated in (macro- and micro-)
refugium areas for long enough during Quaternary
climatic oscillation to result in high genetic differentiation (Garca-Fernndez et al. 2013). This pattern is a consequence of the joint effects of
bottlenecks and genetic drift and/or local adaptation (Gentili et al. 2015b). These processes are further enhanced by the lack of gene ow between
populations (Segarra-Moragues et al. 2005, 2007)
and, in some cases, vegetative reproduction (Amat,
Silvertown, and Vargas 2013). A typical example
is that of Armeria caespitosa (Gmez-Ortega)
Boiss. in DC., which shifted along an altitudinal
gradient in response to Pleistocene climatic oscillations and also adapted to peculiar local environmental conditions (Garca-Fernndez et al. 2013).
Although evidences are scarce, it can be hypothesised that isolation and evolution of some marginal
isolated populations in cold microrefugia (Gentili
et al. 2015a) may be assimilated to the processes
occurred in nunataks during the glacial phases.
Ice-free nunataks hosted small and isolated populations of species for a time long enough to produce
genetic differentiation. Such differentiation is in all
probability at the basis of the current vicariant distribution of several closely related species or subspecies in the Alps and SEMms (Christe et al.
2014; Favarger 1984) like, for example Senecio
incanus L. (western Alps and northern Apennines)
and S. carniolicus Willd. (central and eastern Alps;
Pelser, Gravendeel, and van der Meijden 2003).
c) Speciation event due to extreme reduction of
genetic diversity as a consequence of strong
populations contraction (extinctions, bottlenecks),

and due to founder effect as a result of post-glacial

recolonisation (Garrido et al. 2012; Aquilegia spp.
taxa in Sardinia), leads to a strong loss of genetic
diversity and no clear genetic structure can be
inferred.
So far, although the spatial delimitation of macrorefugium areas across SEMms has been depicted by Mdail
and Diadema (2009), the spatial and genetic characteristics of species that are hosted in microrefugia remains in
great part enigmatic. Literature data suggest that most
boreo-alpine species hosted in SEMms have a distribution independent of each other along mountain ranges
within refugia. So the locations of these refugia can be
ascribed on the one hand by dissimilar histories of
boreo-alpine species during glacial/interglacial phases,
with a succession of range contraction and colonisation
events (Mdail and Diadema 2009; Vargas 2003), and on
the other hand by the local presence of suitable habitat
conditions (Gentili et al. 2015a) and to genetic adaptation. Indeed these (macro- and micro-)refugia have been
hypothesised to have limited extinction rate of species
and performed as a source area of new taxa (Mdail and
Diadema 2009). Such speciation events occurred in a
patchy landscape across a varied topography (Nieto Feliner 2011) and under geomorphological heterogeneity
determining the existence of micro-environmental conditions and ecological niches (Gentili et al. 2015a; Table 1).
Under this view, the review of Gentili et al. (2015a),
based on the denition of macro- and microrefugia of
Rull (2009), claried that during the current interglacial
period, SEMms are functioning as warm-stage
macrorefugia for boreo-alpine species, often linked to
peculiar landforms (scree slopes, nivation niches, moraine ridges, etc.; see Table 1) that can be a reference to
identify microrefugia at the local scale.
Despite the dual role of SEMms mountains as warmand cold-stage (macro-)refugia during interglacial/glacial
phases being at the turning point across the literature,
how the transition from cold to warm (macro and micro)refugia, and vice versa, occurred, has to be still
explained. Help could come from the documentation of
genetic refugia, from phylogeographic studies, investigating the amount of genetic diversity within and across
populations in refugium versus recolonised areas (Hewitt
1996). As a general rule, recolonised areas hold a subset
of the diversity present in the source population within a
certain (micro-)refugia (Petit et al. 2003). Under this
view, it can be hypothesised that the biodiversity spots
resisting within microrefugia could act as reservoirs of
genetic diversity during warm-stage periods when boreoalpine species retracted toward higher elevation and
northern regions. On the other hand, during cold periods,
alpine species could expand toward south and at lower

R. GENTILI ET AL.

Table 1. Species within microrefugia across SEMms: genetic, population, climatic and ecological studies.

Study/species

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Genetic study - population level

Edraianthus serpillyfolius A.DC.

SEMms
Balkan
Peninsula

Habitat
(microrefugia)
Snow beds;
wind exposed
grasslands,
rock crevices
Avalanche
channels and
hayelds
Rocky slopes,
scree slopes

Method:
genetic
marker, trait,
etc.

Main result (genetic, ecological and

conservation features)

Reference

AFLP;
cpDNA

Moderate to high genetic diversity;

geographic structure based on
Pleistocene range shifts.

Surina,
Schnswetter, and
Schneeweiss 2011

AFLP

High genetic diversity withinpopulations; high genetic

differentiation among populations
High genetic diversity withinpopulations; differentiation among
populations
High genetic diversity withinpopulations and high genetic
differentiation among populations;
same genetic variability within
populations of different ploidy level
Low genetic diversity; genetic
differentiation

Gaudeul, Taberlet,
and Till-Bottraud
2000
Kropf, Comes, and
Kadereit 2006

Eryngium alpinum L.

Maritime
Alps

Gentiana alpina Vill., Kernera

saxatilys (L.) Sweet, Papaver
alpinum L., Silene rupestris L.
Ranunculus kuepferi Greut. &
Burd.

Pyrenees,
Sierra
Nevada
Apennines,
Corsica

Rhododendron ferrugineum L.

N-Apennines

Trollius europaeus L.

Pyrenees

Rhamnus persicifolia Moris

Supramontes
and
Gennargentu
massifs
Carpathian

Several
calcareous and
siliceous
habitats
Mountain
peaks, nivation
niches

ISSR

Taurus
mountains

Relict alpine
habitat

cpDNA

Several
habitats

RAPD

Ranunculus glacialis s.l.

Arabis alpina L.

Genetic study: adaptation and speciation

Armeria spp.
Pyrenees

AFLP

Mountain
peaks, snow
beds

AFLP; SSR

Mountain
peaks, nivation
niches
Streams, marsh

AFLP
AFLP

cpDNA

Soldanella spp.

SEMms

Several
habitats

ITS; AFLP

Gentiana spp.

Pyrenees,
Maritime
Alps, Dinaric
Alps
Sardinian
mountains

Several
calcareous vs
siliceous
habitats
Several
siliceous and
calcareous
habitats

Chloroplast
loci; ITS

Supramontes
and
Gennargentu
massifs

Several
calcareous and
siliceous
habitats

Ribes sardoum Martelli; Ribes

multiorum Kit. ex Roem. &
Schult. subsp. sandalioticum
Arrigoni
Sardinian Aquilegia taxa

SSR; ISSR

AFLP

High genetic diversity withinpopulations; high genetic

differentiation among populations
Spatial distribution of genetic diversity
was revealed by a low gene ow, a
fairly high level of genetic
differentiation among populations
The presence of a rare lineage related
to Beringia in the Carpathians
supports the role of these mountains
as a stepping stone between temperate
Europe and the non-European Arctic,
and as an important area of highmountain biodiversity
The highly structured landscape in
combination with the Pleistocene
climate uctuations has created a
network of mountain refugia and the
accumulation of spatially arranged
genotypes
Quaternary glaciation/deglaciation
cycles during favoured downward/
upward migration of mountain
species and speciation/hybridisation
events
Alpine and montane species
of Soldanella experienced different
cycles of range expansion and
contraction during late Quaternary
climatic changes
Likely recent speciation and/or
hybridisation events
Ribes sandalioticum populations
adapted to fresh and humid
microrefugia; the residual single
population of R. sardoum, found
refugia in xerophilous and
calcareous habitats
The intra- and interspecic diversity
of habitats may indicate that habitat
specialisation by divergent selection
may have been a very relevant
force contributing to population
differentiation and species
divergence. In addition, overall
reduced levels of genetic diversity
are also in agreement with this
possibility, since divergent selection
would be eroding genetic variability

Cosendai et al. 2013

Bruni et al. 2012

Despres, Loriot, and
Gaudeul 2002
Bacchetta et al. 2011

Ronikier,
Schneeweiss, and
Schnswetter 2012

Ansell et al. 2011

Fuertes Aguilar,
Gutirrez Larena, and
Nieto Feliner 2011
Zhang, Comes, and
Kadereit 2001

Christe et al. 2014

Gentili et al. 2015b

Garrido et al., 2012

(continued)

B I O D I V E R S I T Y

Table 1. (Continued)

Study/species

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Ecological study
Minuartia recurva (All.) Schinz &
Thell. and other mountain
species
Alopecurus alpinus Vill.

SEMms

Habitat
(microrefugia)

Method:
genetic
marker, trait,
etc.

Pyrenees

Dry
grasslands

Germination

Apennines

Snow beds

Apennines

Snow beds;
mountain
summits;
relict glacial
deposits
Snow beds

Multi-years
observation of
owers and
inorescences
production
Multi-years
observation of
owers and
inorescences
production
Phenology

Carex foetida All.,

Leucanthemopsis alpina (L.)
Heyw., Senecio incanus L.
subsp. incanus, Silene suecica
(Lodd.) Greuter & Burdet
Several snow bed species

Pyrenees

Silene ciliata Pourr.

SEMms

Mountain
summits,
rocky slopes

Minuartia recurva (All.) Schinz &

Thell., Nardus stricta L.
Plantago alpina L.

Sistema
Central

Mountain
summits

Lamyropsis microcephala (Moris)

Dittrich & Greuter

Gennargentu
massif

Mountain
summits

Cerastium cerastioides (L.) Britton,

Deschampsia caespitosa (L.) P.
Beauv., Poa alpina L. subsp.
atlantica (Trabut.), Luzula
spicata (L.) DC., etc.

Atlas
mountains

Mountain
summits

Vegetation
dynamics
through aerial
and satellite
images

Aquilegia barbaricina Arrigoni &

E.Nardi and A. nugorensis
Arrigoni & E.Nardi

Sardinian
mountains

Several
siliceous
and
calcareous
habitats

Phenology and
seed
germination

Sierra
Nevada

Highest
summits;
schistose rocky
slopes
Rocks; scree
slopes

SDM (plus a
study on
genomic
sequences)
SDM

Scree slopes

SDM

Species Distribution Model

Linaria glacialis Boiss.

Primula marginata Curtis

Maritime
Alps,
Apennines

Berardia subacaulis Vill.

Maritime
Alps

Growth and
hydraulic xylem
anatomy along
an elevational
gradient
Multi-years
observation
within
permanent plot
(GLORIA
project). RDA
model
Seed output and
in situ
germination

Main result (genetic, ecological and

conservation features)

Reference

Plants readily germinate without

treatment, reaching an optimum at
relatively high temperatures
Extreme temperatures had a negative
effect on A. alpinus reproductive
performances

Gimnez-Benavides,
Escudero, and
Prez-Garca 2005
Abeli et al. 2012a

Signicant relationships between

species data series and the snow cover
persistence

Abeli et al. 2012b

No substantial differences in species

cycle length under varying snowmelt
regimes but effects on reproductive
performance
The greatest secondary growth and
maximal vessel area are at
intermediate elevations

Lluent et al. 2013

Climatic conditions are the most

important environmental constraints

Gutirrez Girn and

Gaviln 2013

Seeds in the eld germinated in April

June, when diurnal uctuations of
temperatures were almost 10 times
higher than in winter, limiting the
length of the growing season before
the onset of summer drought, and
highlighting an increasing threat from
global warming
These wet pastures are highly
sensitive toclimatic factors. Recent
climatic changes, the anthropic and
pastoral pressures and the global
environmental changes, affect these
zones at the level of their structure
(areas, soil characteristics, etc.)
Phenological patterns and germination
requirements, which differ from those
of typical Mediterranean plants, and
the intraspecic variability detected
among populations, suggest that this
plants are strictly adapted to their
microhabitat

Mattana, Fenu, and

Bacchetta 2012a

Future warming conditions will cause

severe range contractions; genetic
diversity will not diminish at the rate
pace as the distribution range
The species is at its maximum extension,
and any future climate changes might
cause limitations for the survival of the
species
Berardia is predicted to lose more than
80% of its range, becoming endangered
by 2050

Olano et al. 2013

Alaoui Haroni,
Alifriqui, and
Simonneaux 2009

Mattana et al. 2012b

Blanco-Pastor,
FernndezMazuecos, and
Vargas 2013
Casazza et al.
2013
Guerrina et al.
2015

(continued)

R. GENTILI ET AL.

Table 1. (Continued)

Gennargentu
massif

Massif summit

SDM

Increase in the observed distribution

knowledge of Gentiana lutea in Sardinia.
The usefulness of SDM for guiding
discoveries of new localities and
signicantly reduces both the extent of
planned eld surveys and the efforts
related to time and economic resources

Fois et al. 2015

Sierra
Nevada;
Gennargentu
massif
Gennargentu
massif

Mountain
summits

Identication of different spatial levels of

biodiversity hotspots (from nano-to
macro-)

Caadas et al.
2014

Mountain
summits

Floristic
richness
within grid
cells
Floristic
study

Biogeographic sector identication

Bacchetta et al.
2013

Sardinian
mountains

Mountain
summits

Floristic
study

18,8% of boreal and 4.8% of arcticalpine species are present

Cogoni, Alef,
and Scrugli 1999

Central
Apennines

Mountain
summits

Biodiversity
trends

Stanisci, Pelino,
and Blasi 2005

Apuan Alps

Mountains
summits and
refugia

Atlas
mountains

Mountain
summits

Demography
and
conservation
of
endangered
plants
Floristic
study

The 70% of species do not reach the

highest summits and only 11% of the
overall ora is shared by all of the
summits examined
Arctic-alpine elements represent about
12% of high altitude ora. Several of
these species are endangered

The presence of relict boreo-alpine

species is reported

Archibald 1963

Greece
mountains

Mountain
summits

Floristic
study

The presence of relict boreo-alpine

species is reported

Strid, 1995

Sicily
mountains

Mountain
summits

Floristic
study

The presence of relict boreo-alpine

species is reported

Raimondo,
Domina, and
Spadaro 2010

Lebanon
mountains

Mountain
summits

Floristic
study

The presence of relict boreo-alpine

species is reported

Calabrian
mountains
(including
Aspromonte)
Northern
Apennines

Mountain
summits

Floristic
study

The presence of relict boreo-alpine

species is reported

https://en.
wikipedia.org/
wiki/
Flora_of_Lebanon
Bernardo,
Passalacqua, and
Peruzzi 2011

Mountain
summits and
several
microhabitats

IUCN
conservation
status

Due to their evolutionary potential

peripheral isolated populations should be
considered as endemic species

Study/species

SEMms

Gentiana lutea L. subsp. lutea

Conservation/biodiversity study
Flora of Sierra Nevada and
Gennargentu

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Habitat
(microrefugia)

Method:
genetic
marker, trait,
etc.

Rhamnus alpina L., Juniperus

communis L. subsp. alpina
Celack., Potentilla rupestris
subsp. corsica (Soleirol ex
Lehm.) Rouy & E.G.Camus,
Digitalis purpurea L.
Bryum calophyllum R.Br., Grimmia
pilosissima Herzog, G. elatior
Bruch ex Bals.-Criv. & De Not.,
Plagiothecium piliferum (Sw.)
Schimp., etc.
Several high altitude species

Rhododendron ferrugineum L.,

Eriophorum latifolium Hoppe,
Hutchinsia alpina (L.) R.Br,
Homogyne alpina (L.) Cass.,
Empetrum nigrum L., Daphne
alpina L. subsp. alpina, etc.
Arabis alpina L., Calamintha
alpina (L.) Lam. [Acinos
alpinus (L.) Moench.], etc.
Achillea clusiana Tausch, Juncus
tridus L., Ligusticum mutellina
(L.) Crantz., Luzula alpinopilosa (Chaix) Breistr., etc.
Acinos alpinus subsp. meridionalis
(Nyman) P.W.Ball, Adenostyles
alpina subsp. nebrodensis
(Wagenitz & I.Mll.) Greuter,
Minuartia recurva (All.) Schinz
& Thell., Nardus stricta L., etc.
Androsace maxima L., Androsace
villosa L., Lotus corniculatus L.
var. alpinus DC.
Phleum alpinum L., Poa alpina L.,
etc.
Several high altitude peripheral
isolated plant populations

elevation in a macrorefugium context, starting from the

genetic reservoir hosted within microrefugia (Figure 1).
Locating genetic refugia, i.e. quantifying the level
of genetic diversity and gene ow at the landscape level

Main result (genetic, ecological and

conservation features)

Reference

Bedini, Ansaldi,
and Garbari 2007

Abeli et al. 2009

and assessing landscape and geomorphological heterogeneities in the areas where species persist, during
adverse climatic periods could further contribute to
macro- and microrefugia identication and location.

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

B I O D I V E R S I T Y

Figure 1 (a) The main (macro-)refugia areas the SEMms (for details see also Mdail and Diadema 2009). (b) Probable migration
pattern of boreo-alpine species across SEMms within macro- and microrefugia during glacial and interglacial phases.

The boreo-alpine ora of SEMms in a changing

climate: which role for refugia?
The Mediterranean Basin is projected to be a high-sensitive
region, vulnerable to the impacts of climate change due to
the synergistic effects of high temperature and reduced precipitation (Giorgi and Lionello 2008; Abeli et al. 2014b).
According to Nogus-Bravo et al. (2008), during the
twenty-rst century a signicant climate change is
expected for SEMms that will be exposed to a severe modication in terms of structure, functions, services and, of
course, ora and vegetation (Gottfried et al. 2012), even
assuming the most conservative estimates. In addition, the
high anthropisation levels of some mountain ecosystems
prevent or reduce the possibility of mitigation and adaptation actions (Benito, Lorite, and Peas 2011). For this reason, mountain ecosystems across the Mediterranean Basin
have to be considered endangered and prone to extinction
events (Nogus-Bravo et al. 2008; Thuiller et al. 2005).
In this context, numerous studies have dealt with
effects that rising temperatures have on plant species,
considering different major aspects: (a) prediction of
future species/habitat distributions and turnover; (b)
direct observation of upward migration of ora and shift
of vegetation; (c) shift in phenological phases and spe-

cies traits; (d) effect of extreme climatic events on mountain species performances.
a) Predicting species distribution. Models for future
species/habitat distributions both at regional and
local scales have highlighted that biodiversity loss
and species turnover are expected to be high in
SEMms (Sanz-Elorza et al. 2003; Thuiller et al.
2005). Expected habitat loss within the end of
twenty-rst century is greater for high altitude
species and range from 36 to 55% for alpine species and from 31 to 51% for subalpine species
(Engler et al. 2011). Benito, Lorite, and Peas
(2011), in their study of the Mediterraneanalpine ecosystem of Sierra Nevada, emphasised
that an increasing temperature trend may induce a
shift of some thermophilous plant species toward
higher elevations where endemic/unfrequent
mountain species occur that consequently could
disappear within the middle of the century.
b) Shift in ora and vegetation. Recent observations
(20012008) of changes occurring in vascular plant
species richness across Europes major mountains
demonstrated that species have migrated upward,

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

10

R. GENTILI ET AL.
on average. However, the summit ora taxa
richness on boreal-temperate mountains increased
(+3.9 species) while in Mediterranean mountains
decreased (1.4 species) (Pauli et al. 2012).
Gottfried et al. (2012) provided evidence that
across European mountain systems cold-adapted
species decline while warm-adapted species
increase, demonstrating that climate change
progressively transforms mountain ora and
vegetation.
c) Shift in phenological phases and ecological traits.
The assessment of plant traits and phenological
phases at high elevation in SEMms has increased
the knowledge of how individuals and assembled
communities may respond to global and local environmental drivers. For instance, Gonzalo-Turpin
and Hazard (2009) showed how local adaptation
occurs in Festuca eskia Ramond ex DC. along an
altitudinal gradient in the Pyrenees and involves
different adaptive traits (reduced plant stature and
reproductive output), despite the existence of gene
ow. The concomitance of gene ow and phenotypic plasticity along altitudinal gradients may provide opportunities for species to successfully adapt
to climate change. Lluent et al. (2013), in their
study on the phenology of snow-bed plants [e.g.
Cardamine alpina Willd., Salix herbacea L.] in the
Pyrenees, highlighted that the ability of such
species to produce and disperse seeds looks to be a
less conservative feature than cycle length, so the
adaptation to future climate changes may be the
result of modications in their reproductive
potential rather than in the adaptation of their
phenological cycle. Abeli et al. (2012a, 2012b)
analysed multi-year data sets of ower/inorescence production of some alpine plants [Carex
foetida All., Leucanthemopsis alpina (L.)
Heywood, etc.] in the northern Apennines, emphasising that temperature variation (June/July) and the
snow cover persistence negatively affect such traits.
However, in some cases, disjunct southern populations are able to respond differently to environmental stress with respect to core populations (water
availability and drought; see Abeli et al. 2015)
d) Effect of extreme climatic events on mountain
species performances. Extreme climatic events,
such as heat waves, extreme droughts, heavy rains,
storms and their associated effects, are a consequence of climate change (Abeli, Gentili and
Jklniemi 2014). Across SEMms, changes in
reproductive strategies of plants (advanced owering, owers production, sexual and clonal reproduction ratio) have been observed as an effect of
extreme weather events (Abeli et al. 2012b;
Orsenigo et al. 2015).

In mountain areas, climate is a main limiting factor

for plant life, and it is strictly interrelated to topography,
which controls particular micro-environmental conditions
(Gentili et al. 2013). For example, different slopes and
aspects may control the effects of temperature and water
balance for plant species (i.e. topo-climate). Topographic
heterogeneity may increase the survival of alpine species
that are then able to inhabit a variety of habitats, with
different conditions of temperature, soil-moisture content
and wind exposure (Abbott 2008). For these reasons,
across SEMms at higher elevations, some mountain landforms may function as topographic shelters, which persistently keep cold-air pooling and temperature
inversions and can be expected to have a role as warmstage microrefugia (Gentili et al. 2015a). Mosblech,
Bush, and van Woesik (2011) highlighted that local topographic shelter increases the chance of a species surviving in a microrefugium. So, despite recent studies that
have observed an increase of thermophilous species in
the mountain summits of Europe as well a response of
alpine species to climate warming over the last decades
(Gottfried et al. 2012) and have predicted a decline of
cold habitats and ora by the end of the twenty-rst century (Pauli et al. 2012; Thuiller et al. 2005), future
extinction rates could be overestimated if (macro- and
micro-)refugia are not considered in models (Gentili
et al. 2015a).
Perspectives
Under the current trend of climate changes, which
include increases in global temperatures of 24.5 C by
2100 and more intense, frequent and long-lasting heat
waves (IPCC 2014), and its predicted impact on coldadapted plant species, the refugia across the SEMms
may have a key role in the conservation of many boreoalpine plant species (see also Keppel et al. 2012; Taberlet
and Cheddadi 2002). Indeed, a signicant percentage of
species listed in the Bern Convention or in the global
and local IUCN red lists occur in SEMms, in small and
isolated populations and in peculiar micro-habitats and
are often considered under threat due to the increasing
trend of temperatures and altered precipitation patterns
(including snow precipitation). This review has highlighted how in the (warm) Mediterranean mountains
some relict boreo-alpine species persist in microrefugia.
So far, studies on alpine biodiversity across SEMms
have been mainly directed to measure trends and predict
impacts on species, habitats and ecosystems, but relationships and feedbacks between environmental changes,
species trends and refugia have been rarely investigated.
In particular, if the principal areas across SEMms functioning as refugia at the macro-scale (i.e. macrorefugia)
have been in great part identied (see Mdail and
Diadema 2009), studies that predict the duration of

B I O D I V E R S I T Y
effective refugia area at the micro-scale (microrefugia) as
well their ecological characters are lacking. At a ne
scale, a strong biogeographical congruence exists
between microrefugium and micro-nano-hotspot (sensu
Fenu et al. 2010), as in Sardinia and Sierra Nevada
(Caadas et al. 2014).
Thus, (macro- and micro-)refugia need multidisciplinary investigations embracing ecology and palaeoecology, geomorphology and genetics subjects, determining
if boreo-alpine species across SEMms in their own
microrefugium are actually facing extinction, simply
isolation or speciation.
Disclosure statement

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

No potential conict of interest was reported by the authors.

References
Abbott, R. J. 2008. History, Evolution and Future of Arctic
and Alpine Flora: Overview. Plant Ecology and Diversity
1: 129133. doi:10.1080/17550870802460976.
Abeli, T., R. Gentili, G. Rossi, G. Bedini, and B. Foggi. 2009.
Can the IUCN Criteria Be Effectively Applied to Peripheral Isolated Plant Populations? Biodiversity and Conservation 18: 38773890. doi:10.1007/s10531-009-9685-4.
Abeli, T., G. Rossi, R. Gentili, A. Mondoni, and P. Cristofanelli. 2012a. Response of Alpine Plant Flower Production to Temperature and Snow Cover Fluctuation at the
Species Range Boundary. Plant Ecology 213: 113.
doi:10.1007/s11258-011-0001-5.
Abeli, T., G. Rossi, R. Gentili, M. Gandini, A. Mondoni, and P.
Cristofanelli. 2012b. Effect of the Extreme Summer Heat
Waves on Isolated Populations of Two Orophitic Plants in
the North Apennines (Italy). Nordic Journal of Botany 30:
109115. doi:10.1111/j.1756-1051.2011.01303.x.
Abeli, T., R. Gentili, A. Mondoni, S. Orsenigo, and G. Rossi.
2014a. Effects of Marginality: An Overview for Plant
Population Performance. Journal of Biogeography 41:
239249. doi:10.1111/jbi.12215.
Abeli, T., R. Gentili, and A. Jklniemi. 2014b. Living with
Extremes: The Dark Side of Global Climate Change. Plant
Ecology 215: 673675. doi:10.1007/s11258-014-0373-4.
Abeli, T., S. Orsenigo, F. Guzzon, M. Fa, A. Balestrazzi, U.
Carlsson-Granr, J. V. Mller, and A. Mondoni. 2015.
Geographical Pattern in the Response of the Arctic-Alpine
Silene suecica (Cariophyllaceae) to the Interaction between
Water Availability and Photoperiod. Ecological Research
30: 327335. doi:10.1007/s11284-014-1225-3.
Alaoui Haroni, S., M. Alifriqui, and V. Simonneaux. 2009.
Recent Dynamics of the Wet Pastures at Oukaimeden Plateau (High Atlas Mountains, Moroco). Biodiversity and
Conservation 18: 167189. doi:10.1007/s10531-008-9465-6.
Alessandrini, A., B. Foggi, G. Rossi, and M. Tomaselli. 2003.
La Flora di Altitudine dellalto Appennino Tosco-Emiliano.
Bologna: Regione Emilia-Romagna.
Amat, M. E., J. Silvertown, and P. Vargas. 2013. Strong Spatial
Genetic Structure Reduces Reproductive Success in the

11

Critically Endangered Plant Genus Pseudomisopates. Journal of Heredity 104: 692703. doi:10.1093/jhered/est042.
Ansell, S. W., H. K. Stenien, M. Grundmann, S. J. Russell,
A. K. Marcus, H. Schneider, and J. C. Vogel. 2011. The
Importance of Anatolian Mountains as the Cradle of Global
Diversity in Arabis alpina, a Key ArcticAlpine Species.
Annals of Botany 108: 241252. doi:10.1093/aob/mcr134.
Arajo, M. B., D. Alagador, M. Cabeza, D. Nogus-Bravo, and
W. Thuiller. 2011. Climate Change Threatens European
Conservation Areas. Ecology Letters 14: 484492.
doi:10.1111/j.1461-0248.2011.01610.x.
Archibald, J. C. 1963. Notes on Some Plants of the Atlas
Mountains. SRGC Journal 32: 187197.
Bacchetta, G., G. Fenu, E. Mattana, G. Zecca, F. Grassi, G.
Casazza, and L. Minuto. 2011. Genetic Variability of the
Narrow Endemic Rhamnus persicifolia Moris (Rhamnaceae) and Its Implications for Conservation. Biochemical Systematics and Ecology 39: 477484. doi:10.1016/
j.bse.2011.06.018.
Bacchetta, G., G. Fenu, R. Guarino, G. Mandis, E. Mattana, G.
Nieddu, and C. Scudu. 2013. Floristic Traits and Biogeographic Characterization of the Gennargentu Massif (Sardinia).
Candollea 68: 209220. doi:10.15553/c2012v682a4.
Bedini, G., M. Ansaldi, and F. Garbari. 2007. Mapping and
Demography of Endangered Plants in the Apuan Alps, NW
Tuscany, Italy. Bocconea 21: 2744.
Benito, B., J. Lorite, and J. Peas. 2011. Simulating Potential
Effects of Climatic Warming on Altitudinal Patterns of Key
Species in Mediterranean-Alpine Ecosystems. Climatic
Change 108: 471483. doi:10.1007/s10584-010-0015-3.
Bernardo, L., N. G. Passalacqua, and L. Peruzzi. 2011. Flora
Vascolare Della Calabria Prodromo. Informatore Botanico
Italiano 43: 185332.
Birks, H. J. B., and K. J. Willis. 2008. Alpines, Trees, and
Refugia in Europe. Plant Ecology & Diversity 1: 147160.
doi:10.1080/17550870802349146.
Blanco-Pastor, J. L., M. Fernndez-Mazuecos, and P. Vargas. 2013.
Past and Future Demographic Dynamics of Alpine Species:
Limited Genetic Consequences despite Dramatic Range Contraction in a Plant from the Spanish Sierra Nevada. Molecular
Ecology 22: 41774195. doi:10.1111/mec.12383.
Brown, J. H., D. W. Mehlman, and G. C. Stevens. 1995. Spatial Variation in Abundance. Ecology 76: 20282043.
doi:10.2307/1941678.
Bruni, I., F. De Mattia, M. Labra, F. Grassi, S. Fluch, M. Berenyi,
and C. Ferrari. 2012. Genetic Variability of Relict Rhododendron ferrugineum L. Populations in the Northern Apennines
with Some Inferences for a Conservation Strategy. Plant
Biosystems 146: 2432. doi:10.1080/11263504.2011.557093.
Caadas, E. M., G. Fenu, J. Peas, J. Lorite, E. Mattana, and
G. Bacchetta. 2014. Hotspots within Hotspots: Endemic
Plant Richness, Environmental Drivers, and Implications
for Conservation. Biological Conservation 170: 282291.
doi:10.1016/j.biocon.2013.12.007.
Casazza, G., S. Marsili, L. Granato, E. Conti, V. Noblec, A.
Selvaggi, and L. Minuto. 2013. Distribution Range and
Ecological Niche of Primula marginata Curtis (Primulaceae). Plant Biosystems 147: 593600. doi:10.1080/
11263504.2012.760495.

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

12

R. GENTILI ET AL.

Christe, C., S. Caetano, D. Aeschimann, M. Kropf, K.

Diadema, and Y. Naciri. 2014. The Intraspecic Genetic
Variability of Siliceous and Calcareous Gentiana Species is
Shaped by Contrasting Demographic and Re-Colonization
Processes. Molecular Phylogenetics and Evolution 70:
323336. doi:10.1016/j.ympev.2013.09.022.
Cogoni, A., M. Alef, and A. Scrugli. 1999. Sardinias Bryological Flora: The State of Knowledge and Chorological
Considerations. Webbia 53: 381392. doi:10.1080/
00837792.1999.10670666.
Comes, P. H., and J. W. Kadereit. 1998. The Effect of Quaternary Climatic Changes on Plant Distribution and Evolution. Trends in Plant Science 3: 432438. doi:10.1016/
S1360-1385(98)01327-2.
Cosendai, A.-C., J. Wagner, U. Ladinig, C. Rosche, and E.
Hrandl. 2013. Geographical Parthenogenesis and Population Genetic Structure in the Alpine Species Ranunculus
kuepferi (Ranunculaceae). Heredity 110: 560569.
doi:10.1038/hdy.2013.1.
Cuttelod, A., N. Garca, D. Abdul Malak, H. Temple, and V.
Katariya. 2008. The Mediterranean: A Biodiversity Hotspot under Threat. In The 2008 Review of the IUCN Red
List of Threatened Species, edited by J.-C. Vi, C. HiltonTaylor and S. N. Stuart, 113. Gland, Switzerland: IUCN.
Despres, L., S. Loriot, and M. Gaudeul. 2002. Geographic
Pattern of Genetic Variation in the European Globeower
Trollius europaeus L. (Ranunculaceae) Inferred from
Amplied Fragment Length Polymorphism Markers.
Molecular Ecology 11: 23372347. doi:10.1046/j.1365294X.2002.01618.x.
Dobrowski, S. Z. 2011. A Climatic Basis for Microrefugia:
The Inuence of Terrain on Climate. Global Change Biology 17: 10221035. doi:10.1111/j.1365-2486.2010.02263.x.
Eckert, C. G., K. E. Samis, and S. C. Lougheed. 2008.
Genetic Variation across Species Geographical Ranges:
The CentralMarginal Hypothesis and beyond. Molecular
Ecology 17: 11701188. doi:10.1111/j.1365-294X.2007.
03659.x.
Engler, R., C. F. Randin, W. Thuiller, S. Dullinger, N. E. Zimmermann, M. B. Araujo, P. B. Pearman, et al. 2011. 21st
Century Climate Change Threatens Mountain Flora
Unequally across Europe. Global Change Biology 17:
23302341. doi:10.1111/j.1365-2486.2010.02393.x.
Escobar Garca, P., M. Winkler, R. Flatscher, M. Sonnleitner, J.
Krejkov, J. Suda, K. Hlber, G. M. Schneeweiss, and P.
Schnswetter. 2012. Extensive Range Persistence in
Peripheral and Interior Refugia Characterizes Pleistocene
Range Dynamics in a Widespread Alpine Plant Species
(Senecio carniolicus, Asteraceae). Molecular Ecology 21:
12551270. doi:10.1111/j.1365-294X.2012.05456.x.
Favarger, C. 1984. Origine ed Evoluzione della Flora orola
delle Alpi e di altre Montagne DEuropa [The origin and
evolution of the orophilous ora of the Alps and some
other mountain chain of Europe]. Natura & Montagna 3:
529.
Fenu, G., E. Mattana, A. Congiu, and G. Bacchetta. 2010.
The Endemic Vascular Flora of Supramontes: A Priority
Plant Conservation Area in Sardinia. Candollea 65: 347
358. doi:10.15553/c2010v652a10.

Fois, M., G. Fenu, A. Cuena Lombraa, D. Cogoni, and G.

Bacchetta. 2015. A Practical Method to Speed up the Discovery of Unknown Populations Using Distribution Models. Journal for Nature Conservation 24: 4248.
doi:10.1016/j.jnc.2015.02.001.
Fuertes Aguilar, J., B. Gutirrez Larena, and G. Nieto Feliner.
2011. Genetic and Morphological Diversity in Armeria
(Plumbaginaceae) is Shaped by Glacial Cycles in Mediterranean Refugia. Anales Del Jardn Botnico De Madrid
68: 175197. doi:10.3989/ajbm.2260.
Garcia-Fernandez, A., J. M. Iriondo, A. Escudero, F. Fuertes
Aguilar, and G. Nieto Feliner. 2013. Genetic Patterns of
Habitat Fragmentation and past Climate-Change Effects in
the Mediterranean High-Mountain Plant Armeria caespitosa
(Plumbaginaceae). American Journal of Botany 100:
16411650. doi:10.3732/ajb.1200653.
Garrido, J. L., G. Fenu, E. Mattana, and G. Bacchetta. 2012.
Spatial Genetic Structure of Aquilegia Taxa Endemic to
the Island of Sardinia. Annals of Botany 109: 953964.
doi:10.1093/aob/mcs011.
Gaudeul, M., P. Taberlet, and I. Till-Bottraud. 2000. Genetic
Diversity in an Endangered Alpine Plant, Eryngium alpinum L. (Apiaceae), Inferred from Amplied Fragment
Length Polymorphism Markers. Molecular Ecology 9:
16251637. doi:10.1046/j.1365-294x.2000.01063.x.
Gaviln, R. G., B. Jimnez-Alfaro, G. Bacchetta, P. Dimopoulos, and L. Mucina. 2013. Mountain Biodiversity Patterns
in Southern Europe and North Africa. Lazaroa 34: 710.
doi:10.5209/rev_LAZA.2013.v34.n1.43650.
Gentili, R., S. Armiraglio, S. Sgorbati, and C. Baroni. 2013.
Geomorphological Disturbance Affects Ecological Driving
Forces and Plant Turnover along an Altitudinal Stress
Gradient on Alpine Slopes. Plant Ecology 214: 571586.
doi:10.1007/s11258-013-0190-1.
Gentili, R., C. Baroni, M. Caccianiga, S. Armiraglio, A. Ghiani, and S. Citterio. 2015a. Potential Warm-Stage
Microrefugia for Alpine Plants: Feedback between Geomorphological and Biological Processes. Ecological Complexity 21: 8799. doi: 10.1016/j.ecocom.2014.11.006.
Gentili, R., G. Fenu, E. Mattana, S. Citterio, F. De Mattia, and
G. Bacchetta. 2015b. Conservation Genetics of Two Island
Endemic Ribes ssp. (Grossulariaceae) of Sardinia: Survival
or Extinction? Plant Biology 17 (5): 10851094.
doi:10.1111/plb.12330.
Gimnez-Benavides, L., A. Escudero, and F. Prez-Garca.
2005. Seed Germination of High Mountain Mediterranean
Species: Altitudinal, Interpopulation and Interannual Variability. Ecological Research 20: 433444. doi:10.1007/
s11284-005-0059-4.
Giorgi, F., and P. Lionello. 2008. Climate Change Projections
for the Mediterranean Region. Global and Planetary
Change 63: 90104. doi:10.1016/j.gloplacha.2007.09.005.
Gmez, A., A. Palacios, M. Ramos, L. M. Tanarro, L. Schulte,
and F. Salvador. 2001. Location of Permafrost in Marginal
Regions: Corral del Veleta, Sierra Nevada, Spain.
Permafrost and Periglacial Process 12: 93110.
doi:10.1002/ppp.375.
Gonzalo-Turpin, H., and L. Hazard. 2009. Local Adaptation
Occurs along Altitudinal Gradient despite the Existence of

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

B I O D I V E R S I T Y
Gene Flow in the Alpine Plant Species Festuca eskia.
Journal of Ecology 97: 742751. doi:10.1111/j.13652745.2009.01509.x.
Gottfried, M., H. Pauli, A. Futschik, M. Akhalkatsi, P. Barancok,
J. L. Benito Alonso, G. Coldea, et al. 2012. Continent-Wide
Response of Mountain Vegetation to Climate Change. Nature Climate Change 2: 111115. doi:10.1038/nclimate1329.
Guerrina, M., E. Conti, L. Minuto, and G. Casazza. 2015.
Knowing the past to Forecast the Future: A Case Study
on a Relictual, Endemic Species of the SW Alps, Berardia
subacaulis. Regional Environmental Change. doi:10.1007/
s10113-015-0816-z.
Gutirrez Girn, A., and R. G. Gaviln. 2013. Monitoring
Mediterranean High Mountain Vegetation in the Sistema
Central (Spain): GLORIA Project and Collateral Ecological
Studies. Lazaroa 34: 7787. doi: 10.5209/rev_LAZA.2013.v34.n1.43577.
Hewitt, G. M. 1996. Some Genetic Consequences of Ice Ages,
and Their Role in Divergence and Speciation. Biological
Jorunal of the Linnean Society 58: 247276. doi:10.1006/
bijl.1996.0035.
Hewitt, G. M. 1999. Post-Glacial Re-Colonization of European Biota. Biological Jorunal of the Linnean Society 68:
87112. doi:10.1111/j.1095-8312.1999.tb01160.x.
Hewitt, G. M. 2004. Genetic Consequences of Climatic Oscillations in the Quaternary. Proceedings of the Royal Society
of London, Series B: Biological Sciences 359: 183195.
doi:10.1098/rstb.2003.1388.
Holder, K., R. Montgomerie, and V. L. Friesen. 1999. A Test
of the Glacial Refugium Hypothesis Using Patterns of
Mitochondrial and Nuclear Dna Sequence Variation in
Rock Ptarmigan (Lagopus mutus). Evolution 53: 1936
1950. doi:10.2307/2640452.
IPCC. 2014. Summary for Policymakers. Climate Change
2014: Impacts, Adaptation, and Vulnerability. Part a: Global and Sectorial Aspects. Contribution of Working Group
II to the Fifth Assessment Report of the Intergovernmental
Panel on Climate Change, edited by C. B. Field et al, 1
32. Cambridge, UK and New York, NY, USA: Cambridge
University Press.
Jalas, J., and Suominen, J., eds. 19721994. Atlas Flora Europaea, 110. Helsinki: Helsinki University Printing House.
Jimnez-Mejas, P., M. Luceo, K. A. Lye, C. Brochmann, and
G. Gussarova. 2012. Genetically Diverse but with Surprisingly Little Geographical Structure: The Complex History
of the Widespread Herb Carex nigra (Cyperaceae).
Journal of Biogeography 39: 22792291. doi:10.1111/
j.1365-2699.2012.02740.x.
Jimnez-Mejas, P., M. Fernndez-Mazuecos, M. E. Amat, and
P. Vargas. 2015. Narrow Endemics in European Mountains: High Genetic Diversity within the Monospecic
Genus Pseudomisopates (Plantaginaceae) despite Isolation
since the Late Pleistocene. Journal of Biogeography 42:
14551468. doi:10.1111/jbi.12507.
Keppel, G., K. P. Van Niel, G. W. Wardell-Johnson, C. J.
Yates, M. Byrne, L. Mucina, A. Schut, S. D. Hopper, and
S. E. Franklin. 2012. Refugia: Identifying and Understanding Safe Havens for Biodiversity under Climate Change.

13

Global Ecology and Biogeography 21: 393404.

doi:10.1111/j.1466-8238.2011.00686.x.
Kropf, M., H. P. Comes, and J. W. Kadereit. 2006. Long-Distance Dispersal Vs Vicariance: The Origin and Genetic
Diversity of Alpine Plants in the Spanish Sierra Nevada.
New Phytologist 172: 169184. doi:10.1111/j.14698137.2006.01795.x.
Kuss, P., G. F. J. Armbruster, H. H. gisdttira, J. F. Scheepens,
and J. Stcklin. 2011. Spatial Genetic Structure of Campanula thyrsoides across the European Alps: Indications for Glaciation-Driven Allopatric Subspeciation. Perspectives in
Plant Ecology, Evolution and Systematics 13: 101110.
Lluent, A., A. Anadon-Rosell, J. M. Ninot, O. Grau, and E.
Carrillo. 2013. Phenology and Seed Setting Success of
Snowbed Plant Species in Contrasting Snowmelt Regimes
in the Central Pyrenees. Flora 208: 220231. doi:10.1016/
j.ora.2013.03.004.
Lobo, J. M., I. Castro, and J. C. Moreno. 2001. Spatial and
Environmental Determinants of Vascular Plant Species
Richness Distribution in the Iberian Peninsula and Balearic
Islands. Biological Journal of the Linnean Society 73:
233253. doi:10.1006/bijl.2001.0543.
Lpez-Garca, J. M., H.-A. Blain, E. Allu, S. Bauls, A. Bargall, P. Martn, J. I. Morales, et al. 2010. First Fossil Evidence of an Interglacial Refugium in the Pyrenean
Region. Naturwissenschaften 97: 753761. doi:10.1007/
s00114-010-0695-6.
Lorite, J., F. B. Navarro, and F. Valle. 2007. Estimation of
Threatened Orophytic Flora and Priority of Its Conservation
in the Baetic Range (S. Spain). Plant Biosystems 141: 1
14. doi:10.1080/11263500601153560.
Mansion, G., G. Rosenbaum, N. Schnenberger, G. Bacchetta,
J. A. Rossell, and E. Conti. 2008. Phylogenetic Analysis
Informed by Geological History Supports Multiple,
Sequential Invasions of the Mediterranean Basin by the
Angiosperm Family Araceae. Systematic Biology 57: 269
285. doi:10.1080/10635150802044029.
Martin-Bravo, S., V. Valcrcel, P. Vargas, and M. Luceo. 2010.
Geographical Speciation Related to Pleistocene Range
Shifts in the Western Mediterranean Mountains (Reseda
Sect. Glaucoreseda, Resedaceae). Taxon 59: 466482.
Mattana, E., G. Fenu, and G. Bacchetta. 2012a. Seed production and in situ germination of Lamyropsis Microcephala
(Asteraceae), a threatened Mediterranean mountain species. Arctic, Antarctic, and Alpine Research 44: 343349.
doi:10.1657/1938-4246-44.3.343.
Mattana, E., M. I. Daws, G. Fenu, and G. Bacchetta. 2012b.
Adaptation to Habitat in Aquilegia Species Endemic to
Sardinia (Italy): Seed Dispersal, Germination, and Persistence in the Soil. Plant Biosystems 146: 374383.
doi:10.1080/11263504.2011.557097.
Mdail, F., and K. Diadema. 2009. Glacial Refugia Inuence
Plant Diversity Patterns in the Mediterranean Basin. Journal of Biogeography 36: 13331345. doi:10.1111/j.13652699.2008.02051.x.
Mdail, F., and P. Verlaque. 1997. Ecological Characteristics
and Rarity of Endemic Plants from Southeast France and
Corsica: Implications for Biodiversity Conservation.

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

14

R. GENTILI ET AL.

Biological Conservation 80: 269281. doi:10.1016/S00063207(96)00055-9.

Mosblech, N. A. S., M. B. Bush, and R. van Woesik. 2011.
On Metapopulations and Microrefugia: Palaeoecological
Insights. Journal of Biogeography 38: 419429.
doi:10.1111/j.1365-2699.2010.02436.x.
Nagy, L., and G. Grabherr. 2009. The Biology of Alpine Habitats. Oxford: Oxford University Press.
Nagy, L., G. Grabherr, C. Krner, and D. B. A. Thompson,
eds. 2003. Alpine Biodiversity in Europe - A Europe-Wide
Assessment of Biological Richness and Change. Ecological
Studies 167. Berlin: Springer.
Nieto Feliner, G. 2011. Southern European Glacial Refugia: A
Tale of Tales. Taxon 60: 365372.
Nogus-Bravo, D., M. B. Arajo, T. Lasanta, and J. I. Lpez
Moreno. 2008. Climate Change in Mediterranean Mountains during the 21st Century. Ambio 37: 280285.
Olano, J. M., I. Almera, M. Eugenio, and G. von Arx. 2013.
Under Pressure: How a Mediterranean High-Mountain
Forb Coordinates Growth and Hydraulic Xylem Anatomy
in Response to Temperature and Water Constraints. Functional Ecology 27: 12951303. doi:10.1111/13652435.12144.
Orsenigo, S., T. Abeli, G. Rossi, P. Bonasoni, C. Pasquaretta,
M. Gandini, and A. Mondoni. 2015. Effects of Autumn
and Spring Heat Waves on Seed Germination of High
Mountain Plants. PlosOne 10: e0133626. doi:10.1371/
journal.pone.0133626.
Pauli, H., M. Gottfried, S. Dullinger, O. Abdaladze, M. Akhalkatsi, J. L. Benito Alonso, G. Coldea, et al. 2012. Recent
Plant Diversity Changes on Europes Mountain Summits.
Science 336: 353355. doi:10.1126/science.1219033.
Pelser, P., B. Gravendeel, and R. van der Meijden. 2003. Phylogeny Reconstruction in the Gap between Too Little and
Too Much Divergence: The Closest Relatives of Senecio
jacobaea (Asteraceae) according to DNA Sequences and
AFLPs. Molecular Phylogenetics and Evolution 29: 613
628. doi:10.1016/S1055-7903(03)00139-8.
Petit, R., I. Aguinagalde, J. L. de Beaulieu, C. Bittkau, S.
Brewer, R. Cheddadi, R. Ennos, et al. 2003. Glacial Refugia: Hotspots but Not Melting Pots of Genetic Diversity.
Science 300: 15631565. doi:10.1126/science.1083264.
Raimondo, F. M., G. Domina, and V. Spadaro. 2010. Checklist of the Vascular Flora of Sicily. Quaderni di Botanica
Ambientale e Applicata 21: 189252.
Ronikier, M., G. M. Schneeweiss, and P. Schnswetter. 2012.
The Extreme Disjunction between Beringia and Europe in
Ranunculus Glacialis s.l. (Ranunculaceae) Does Not Coincide with the Deepest Genetic Split A Story of the Importance of Temperate Mountain Ranges in Arctic-Alpine
Phylogeography. Molecular Ecology 21: 55615578.
doi:10.1111/mec.12030.
Rull, V. 2009. Microrefugia. Journal of Biogeography 36:
481484. doi:10.1007/s13280-014-0599-3.
Rull, V., C. Schubert, and R. Aravena. 1988. Palynological
Studies in the Venezuelan Guayana Shield: Preliminary
Results. Current Research in the Pleistocene 5: 5456.
Sanz-Elorza, M., E. D. Dana, A. Gonzles, and E. Sobrino.
2003. Changes in the High-Mountain Vegetation of the

Central Iberian Peninsula as a Probable Sign of Global

Warming. Annals of Botany 92: 273280. doi:10.1093/
aob/mcg130.
Segarra-Moragues, J. G., M. Palop-Esteban, F. GonzalezCandelas, and P. Catalan. 2005. On the Verge of Extinction: Genetics of the Critically Endangered Iberian Plant
Species, Borderea chouardii (Dioscoreaceae) and Implications for Conservation Management. Molecular Ecology
14: 969982. doi:10.1111/j.1365-294X.2005.02482.x.
Segarra-Moragues, J. G., M. Palop-Esteban, F. Gonzlez-Candelas, and P. Cataln. 2007. Nunatak Survival Vs. Tabula
Rasa in the Central Pyrenees: A Study on the Endemic
Plant Species Borderea pyrenaica (Dioscoreaceae). Journal of Biogeography 34: 18931906. doi:10.1111/j.13652699.2007.01740.x.
Sexton, J. P., P. J. McIntyre, A. L. Angert, and K. J. Rice.
2009. Evolution and Ecology of Species Range Limits.
Annual Reviews of Ecology, Evolution, and Systematics 40:
415436. doi:10.1146/annurev.ecolsys.110308.120317.
Soul, M. E., ed. 1987. Viable Populations for Conservation.
Cambridge, UK: Cambridge University Press.
Stanisci, A., G. Pelino, and C. Blasi. 2005. Vascular Plant
Diversity and Climate Change in the Alpine Belt of the
Central Apennines (Italy). Biodiversity and Conservation
14: 13011318. doi:10.1007/s10531-004-9674-6.
Stevanovi, V., S. Sneana Vukojii, J. inar-Sekuli, M.
Lazarevi, G. Tomovi, and K. Tan. 2009. Distribution
and Diversity of Arctic-Alpine Species in the Balkans.
Plant Systematics and Evolution 283: 219235.
Stewart, J. R., A. M. Lister, I. Barnes, and L. Dalen. 2010.
Refugia Revisited: Individualistic Responses of Species in
Space and Time. Proceedings of the Royal Society of London, Series B: Biological Sciences 277: 661671.
Strid, A.1995. The Greek Mountain Flora, with Special
Reference to the Central European Element. Bocconea 5:
99112. ISSN: 1120-4060.
Surina, B., P. Schnswetter, and G. M. Schneeweiss. 2011.
Quaternary Range Dynamics of Ecologically Divergent
Species (Edraianthus serpyllifolius and E. tenuifolius, Campanulaceae) within the Balkan Refugium. Journal of Biogeography 38: 13811393. doi:10.1111/j.1365-2699.2011.
02493.x.
Taberlet, P., and R. Cheddadi. 2002. Quaternary Refugia and
Persistence of Biodiversity. Science 297: 20092010.
doi:10.1126/science.297.5589.2009.
Taberlet, P., L. Fumagalli, A. G. Wust-Saucy, and J. F. Cosson.
1998. Comparative Phylogeography and Postglacial
Colonization Routes in Europe. Molecular Ecology 7:
453464.
Thompson, J. D., S. Lavergne, L. Affre, M. Gaudeul, and M.
Debussche. 2005. Ecological Differentiation of Mediterranean Endemic Plants. Taxon 54: 967976.
Thuiller, W., S. Lavorel, M. B. Araujo, M. T. Sykes, and I. C.
Prentice. 2005. Climate Change Threats to Plant Diversity
in Europe. Proceedings of the National Academy of
Sciences of the United States of America 102: 82458250.
Tomaselli, M., and N. Agostini. 1994. A Comparative
Phytogeographic Analysis of the Summit Flora of the

B I O D I V E R S I T Y

Downloaded by [Universit di Pisa] at 09:18 15 December 2015

Tuscan-Emilian Apennines and of the Apuan Alps

(Northern Apennines). Fitosociologia 26: 99109.
Tzedakis, P. C., I. T., Lawson, M. R. Frogley, G. M. Hewitt, and
R. C. Preece. 2002. Buffered Tree Population Changes in a
Quaternary Refugium: Evolutionary Implications. Science
297: 20442047. doi:10.1126/science.1073083.
Vargas, P. 2003. Molecular Evidence for Multiple Diversication Patterns of Alpine Plants in Mediterranean Europe.
Taxon 52: 463476.
Vogiatzakis, I. N., eds. 2012. Biogeography, in Mediterranean
Mountain Environments. Chichester, UK: John Wiley &
Sons, Ltd.

15

Winkler, M., A. Tribsch, G. M. Schneeweiss, S. Brodbeck, F.

Gugerli, R. Holderegger, R. J. Abbott, and P. Schnswetter.
2012. Tales of the Unexpected: Phylogeography of the
Arctic-Alpine Model Plant Saxifraga oppositifolia (Saxifragaceae) Revisited. Molecular Ecology 21: 46184630.
doi:10.1111/j.1365-294X.2012.05705.x.
Zhang, L.-B., H. P. Comes, and J. W. Kadereit. 2001. Phylogeny and Quaternary History of the European Montane/
Alpine Endemic Soldanella (Primulaceae) Based on ITS
and AFLP Variation. American Journal of Botany 88:
23312345.