REVIEW Open Access
Extra-Mediterranean refugia: The rule and not the
exception?
Thomas Schmitt1*
and Zoltán Varga2
Abstract
Some decades ago, biogeographers distinguished three major faunal types of high importance for Europe: (i)
Mediterranean elements with exclusive glacial survival in the Mediterranean refugia, (ii) Siberian elements with glacial
refugia in the eastern Palearctic and only postglacial expansion to Europe and (iii) arctic and/or alpine elements with
large zonal distributions in the periglacial areas and postglacial retreat to the North and/or into the high mountain
systems. Genetic analyses have unravelled numerous additional refugia both of continental and Mediterranean
species, thus strongly modifying the biogeographical view of Europe. This modified notion is particularly true for the
so-called Siberian species, which in many cases have not immigrated into Europe during the postglacial period, but
most likely have survived the last, or even several glacial phases, in extra-Mediterranean refugia in some climatically
favourable but geographically limited areas of southern Central and Eastern Europe. Recently, genetic analyses
revealed that typical Mediterranean species have also survived the Last Glacial Maximum in cryptic northern refugia
(e.g. in the Carpathians or even north of the Alps) in addition to their Mediterranean refuge areas.
Keywords: Phylogeography, Refugia, Faunal types, Last Glacial Maximum (LGM), Postglacial, Range expansions,
Range shifts, Mediterranean, Continental, Siberian
Introduction
The biogeography of the western Palearctic is quite
complex and therefore a fascinating and challenging research
subject [1-8]. Scientists, even about 50 years ago,
distinguished three major faunal components in Europe
(Mediterranean, Siberian, arctic and/or alpine), but the
interpretation of the underlying biogeographical processes
behind these faunal elements has considerably
changed since then, e.g. [8-13]. Furthermore, the understanding
of climatic and other environmental conditions
during glaciations has substantially deepened, e.g. [14-19].
By the time of de Lattin [4], the existence of Mediterranean
faunal elements was largely acknowledged (e.g.
the “holothermic” faunal elements of Rebel [20]). These
elements were thought to have exclusively survived the
ice ages in the Mediterranean region, which was divided
into nine sub-centres [21] composed of several core
areas (German: Arealkerne [2]). Depending on the postglacial
expansion out of these refugia and differentiation
centres, two basic types were distinguished: (i) stationary
elements which did not essentially enlarge their distributions
northwards during the postglacial period and (ii)
expansive elements largely expanding their ranges beyond
their Mediterranean refuge areas, frequently as far
north as southern Scandinavia and often showing peripherally
isolated populations (subspecies) at the northern
boundary of their range e.g. [4] (Figure 1a).
Furthermore, the existence of large ice age distributions
in the zonal periglacial belt was suggested for the
species with arctic, alpine or arctic-alpine distributions
followed by postglacial retreat to high mountain areas in
the South and/or the high latitudes in the North. Retreat
into both directions was interpreted as the reason for
the arctic-alpine disjunctions today [22,23]. However,
local endemics e.g. in the Alps were interpreted (at least
partly) as in situ survival e.g. at nunataks [23] and/or in
some marginal areas of the Alps (“massifs de refuge”,
[24]) and other southern European high mountain systems
[25,26]. Thus, the more widespread species in this
group were interpreted, following the old monoglacial
ideas of Scharff [27], as the only species surviving north* Correspondence: thsh@uni-trier.de
1
Biogeography, Trier University, D – 54 286, Trier, Germany
Full list of author information is available at the end of the article
© 2012 Schmitt and Varga; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the
Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use,
distribution, and reproduction in any medium, provided the original work is properly cited.
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of the mountain chains of the Pyrenees, Alps and Carpathians
(Figure 1b).
The third biogeographical unit, the large group of species
with continental distributions (i.e. missing or rather
fragmented in the Mediterranean parts of Europe and
absent in the vicinity of the Atlantic) was interpreted as
completely missing in Europe during the ice ages, but
surviving in the eastern Palearctic in Siberian and/or
Manchurian refugia [28]. A postglacial and thus very
rapid colonisation of these species throughout Asia to
Europe was postulated (Figure 1c) with a typical “line of
packing” (i.e. the accumulation of distribution borders;
German: Stauungslinie) at the margin of the Mediterranean
area (Figure 2). However, this point of view was
strongly questioned since the 1960-70ies because this
“line of packing” was recognised as an accumulation area
of peripheral subspecies of continental species and was
also re-considered and interpreted as possible survival
areas of such species in some areas of south-central and
south-eastern Europe (Figure 2; [25,29-33]). Since then,
evidence has accumulated for various extra-Mediterranean
refugia in Europe, e.g. [8,9,11-13,34-38].
Over the past two decades genetic analyses of many
animal and plant species, representing different biogeographical
groups, have strongly enhanced our understanding
of the highly complex biogeographical patterns
and processes within the western Palearctic [5-8,10,40-
44]. Therefore, we review the changing view with respect
to extra-Mediterranean refugia with a special focus on
the geographic location of these refugia, their mostly
a) b)
c)
R1 R2 R3R1 R2 R3
RR
RR
Figure 1 The interpretation of glacial refugia (indicated by "R") and postglacial range changes (indicated by arrows) of the three most
important biogeographical elements of Europe (a: Mediterranean, b: arctic/alpine, c: Siberian/Manchurian) as suggested by de Lattin
[4], simplified.
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limited spatial extent and often cryptic natures. As recent
reviews already address these extra-Mediterranean
refugia in artic/alpine species [10,45-48], we focus in this
article on continental and Mediterranean species.
Continental species: less mobile but much more
complex and diverse
The species with typical continental distribution patterns
(i.e. not reaching the areas with typical Atlantic and
Mediterranean climates, but being widely distributed
from continental Europe throughout temperate Asia)
were formerly thought to have immigrated to Europe
from eastern Asiatic Würm glacial refuge areas (i.e. from
the Siberian and the Manchurian core areas) during the
postglacial period (Figure 1c) [28]. However, this idea
was questioned afterwards on the basis of chorological
(i.e. the classical interpretation of distribution patterns)
and intraspecific taxonomical analyses (cf. Figure 2).
Consequently, survival of such continental species was
postulated in Europe outside the classical Mediterranean
refuge areas [25,29-33].
One of the best studied examples of these continental
species is the woodland ringlet Erebia medusa [49-53].
Allozyme analyses over major parts of the species’ European
distribution range showed strong differentiation
into a variety of different genetic lineages: three in
Central and East Europe, one in the southern Alps, four
or more in and around the Carpathian Basin and one
with remarkable sub-structures in Bulgaria [50,51]. Analyses
of the mtDNA locus COI of the samples from
Central and East Europe, the southern Alps and the
western Carpathian Basin strongly supported the genetic
lineages detected with allozyme electrophoreses [53].
These results confirm the idea of a larger number of
extra-Mediterranean Würm ice age refuge areas in
Europe and not postglacial immigration to Europe out
of Asiatic core areas. These data strongly support such
refugia having been localised (i) west of the Alps, (ii)
south of the Alps, (iii) east/south-east of the Alps, (iv)
south of the northern Carpathians, (v) in the eastern
Carpathian Basin between the Apuseni Mts. and the
eastern Carpathians, (vi) on the southern slopes of the
50%
40%
50%
40%
Figure 2 European accumulation zones of marginal subspecies of species showing the continental distribution type (shaded areas).
Most of these areas were later discovered as being important as extra-Mediterranean centres of glacial survival of thermophilic species. The
southern limits of some of these zones coincide with the line of packing of the "Siberian" faunal type in Europe (sensu de Lattin [4]; dotted line).
The representation of "Siberian" species in the local faunal lists is given as broken lines with indication of their respective percentages. Redrawn
after de Lattin [4] and Varga [39].
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southern Carpathians and (vii) in the vicinity of the
Bulgarian mountain systems, the latter most probably in
a structured distribution possibly with temporal disjunctions
during some periods of the last ice age (Figure 3).
Most of these refugia are assumed to be geographically
small and situated in climatically buffered pockets in the
landscape cf. [9]. Although numerous morphological
subspecies of E. medusa have been described, in some
cases even supporting these genetic patterns, the refugia
postulated on allozyme patterns are even more numerous
and are geographically more informative and concise
than the known phenotypically differentiated groups.
Also, they cannot be deduced from the actual, more or
less continuous, distribution pattern of E. medusa. Therefore,
the only adequate possibility to comprehensively
asses the complex biogeography and refugial structure of
this species is through an analysis of its genetic patterns.
A similar situation was observed in the eastern phylogenetic
clade of the clouded apollo Parnassius mnemosyne
by an analysis of mtDNA sequences of the COI
locus over large parts of eastern and south-eastern Europe
[54]. This analysis also supported a larger number of
extra-Mediterranean Würm ice age refugia from the
lower parts of the northern Carpathians and the eastern
Alps forelands throughout the Carpathian Basin to the
extra-Mediterranean regions of the Balkan Peninsula
(Figure 4). The Carpathian Basin shows the overlap of
three main haplotype groups of the eastern lineage of
this polytypic species. At least one of them has expanded
northwards from the Carpathian region reaching southern
Finland.
A complex hierarchical pattern was also observed in
the adder Vipera berus, a snake distributed from western
Europe throughout Asia as far east as the island of Sakhalin.
Ursenbacher et al. [55] showed a strong differentiation
into three major genetic lineages of most probably
pre-Pleistocene origin with two of these being geographically
restricted (northern Italian Alps; western Balkan
mountains) and one being fairly widespread from France
and the UK to the Pacific. The widespread lineage is further
divided into several sub-clades of which all apart
from one are confined to some part of Europe. These
data suggest that two relict lineages most probably survived
long periods of time (maybe even the whole Pleistocene)
in extra-Mediterranean regions at the southern
Alps margin and in the mountainous regions of the
western Balkan Peninsula.
The sub-clades in the widespread lineage persisted
during at least the last ice age (and maybe even evolved)
in other extra-Mediterranean refugia in France, north of
the Alps and in the Carpathian Basin. Northern Europe
and Asia were postglacially colonised from the northern
and north-eastern most lineages, respectively. The refugial
populations in France contracted from their ice age
distribution to the northern parts of the country and to
the British Isles, as well as to the higher elevations (e.g.
Massif Central) in southern France (Figure 5).
The sibling Vipera seoanei, restricted to the mountain
ranges of northern Iberia, is even more strongly differentiated
from V. berus than the lineages within this latter
species [55]. The split between these two species probably
occurred before the beginning of the glacial-interglacial
R
RR
R R
R
R
R
R
R
R
R
R
R
RR
R R
R
R
R
R
R
R
R
R
Figure 3 Possible Würm glacial distribution patterns (indicated by "R") of the butterfly Erebia medusa and assumed postglacial range
changes (arrows). Overlapping refuge symbols or lines between them indicate possible gene flow between them during the last ice age or even a
larger structured refuge area (especially in the case of Bulgaria). Redrawn after Schmitt & Seitz [51], Schmitt et al. [50] and Hammouti et al. [53].
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cycles, with V. seoanei most likely having continuously
existed over time in the extra-Mediterranean regions of
Iberia. It is in this area that the species has two morphologically
differentiated subspecies [56], thus indicating
two centres of glacial survival.
Furthermore, mtDNA analyses of the snail Arion fuscus
support an extra-Mediterranean survival of this species
especially in the eastern regions of the Alps, but
maybe also in other extra-Mediterranean retreats such
as in the area of the Tatras [57]. A strongly differentiated
lineage of this species is restricted to the Balkan Peninsula.
Whether the respective refugia have to be considered
Ponto-Mediterranean or Balkan extra-Mediterranean
is in need of further genetic analyses.
The particular importance of a Carpathian refugium as
extra-Mediterranean retreat has repeatedly been suggested
in several groups of vertebrates, e.g. in the moor
frog (Rana arvalis), the agile lizard (Lacerta agilis), the
bank vole (Clethrionomys glareolus), the common and
the field vole (Microtus arvalis, M. agrestis), the wild
boar (Sus scrofa), the roe deer (Capreolus capreolus) and
the red deer (Cervus elaphus), and even in the brown
bear (Ursus arctos), e.g. [34,35,58-64] (Figure 6). In the
lizard Zootoca vivipara, a special mtDNA haplotype
restricted to northern Hungary and Austria was found.
This ovo-viviparous form shows peculiar karyotypic
characters and demonstrates that the ovo-vivipary has
independently evolved in the western European and
Pannonian (Zootoca vivipara pannonica) populations
[65,66].
Surveys of the bank vole (Clethrionomys glareolus)
have not only shown the significance of “northern” refugia
in the Carpathians, but also in some other areas, e.g.,
the vicinity of the Alps, southern France, and southern
parts of the Ural Mountains (Figure 6b). New fossil and
genetic records support the refugial character of the
southern Urals in eastern Europe. Recently, a morphometric
analysis of bank vole molars has unravelled the
existence of a “Ural” morphotype of this species [75].
Although the transitional forest steppic character of
the LGM vegetation of the Russian plain already was
demonstrated in several palaeo-ecological publications e.
g. [76,77], the importance of the refugia in the Urals
(Figure 6), also in Kazakhstan and south-western Siberia
was only recently shown [67,78,79], and Danukalova et al.
[78] pointed out that “the changes of the palaeoenvironment
were not so sharp as in the adjacent northwestern
territories. Biota of the region has been formed under the
influence of the European and Asiatic elements”.
For common shrews (Sorex araneus), two major continental
refugia have been discovered, one in the southern
Urals, from which the re-population of northern
Europe started, and a southern Siberian core area which
shows a geographic co-incidence with some nemoral
species ([67]; further details e.g. in Walter and Straka
[80]; Walter and Breckle [81]). These results have been
repeatedly confirmed by the karyological and molecular
analyses of Wóycik et al. [82], and also perfectly harmonise
with the suggested history of postglacial expansion
of C. glareolus from a southern continental core
area (Urals) to northern Russia [75]. Additionally, in forest
bird species, the Caucasus appears to be an area of
genetic divergence. Endemic (or nearly so) clusters of
haplotypes in the Caucasus have been documented for
several species (Carpodacus erythrinus, Motacilla alba,
Sitta europaea, Troglodytes troglodytes; reviewed by Zink
et al. [83]).
All these examples clearly show that the continental
species have had much more refugia and thus, performed
much smaller range shifts and expansions than
previously thought. Expansion from Siberian core areas
into Europe have only been demonstrated in mobile species
of boreo-temperate forests such as the great spotted
R
R
R
R
R
R
R
R
R
RR
RR
RR
RR
RR
RR
RR
RR
RR
Figure 4 Possible Würm glacial distribution patterns of the
butterfly Parnassius mnemosyne, eastern lineage (refuge areas
with closely related haplotypes are grouped and in the same
colour) and assumed postglacial range changes (arrows) in
eastern and south-eastern Europe. Redrawn after Gratton et al. [54].
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woodpecker (Dendrocopus maior), the boreal warbler
(Phylloscopus borealis), the Siberian flying squirrel (Pteromys
volans), or the wood lemming (Myopus schisticolor)
[84-87]. These species exhibit a higher level of genetic
differentiation only at the eastern-southeastern parts of
their distributions. Additionally, the dwarf damselfly
Nehalennia speciosa, a specialist species of oligotrophic
peat bogs, shows a very shallow differentiation all over
the Palearctic and most probably expanded from an
eastern Asiatic ice age refuge at the beginning of the
postglacial period [88]. Some species of boreal forests
have had at least two subsequent waves of expansion
from the eastern Palaearctic to Europe, from which the
representatives of the earlier ones have been preserved
in some southern European high mountains as the Pyrenees,
the Cantabrian mountains and/or in the Balkans,
as e.g. the capercaille [89,90].
For Holarctic boreal forest species, a deeper split has
only been shown between the Nearctic and the
Palearctic populations (e.g. the birds Picoides tridactylus,
Pinicola enucleator, Troglodytes troglodytes), mostly connected
with stronger genetic differentiation in the Nearctic
[84,91,92]. Therefore, a direct Siberian invasion to
Europe is rare and can only be supported for some boreal
forest species by shallow phylogeographic structures.
This pattern might be the strict exception in temperate
non-forest species and not one of the paradigms as postulated
by de Lattin [28].
In general, these extra-Mediterranean refugia were apparently
often located in the vicinity of water donating
mountains systems as the glaciated Alps, Carpathians or
Balkan mountain systems cf. [51], which may have
received more precipitation during the kryoxerotic LGM
than the adjacent lowland loess steppe areas. The same
idea implicitly appears in some recent papers of Bhagwat
and Willis [36], Varga [13] and Stewart et al. [12] supported
by habitat preference data of numerous, mostly
woody plant and vertebrate species. Furthermore, many
of these refugia must have been small and sporadic in
their geographic extent [93,94] so that they have been
overlooked in the past reconstruction of the glacial faunas
mostly based on fossil records. This might explain
their cryptic character, which is in clear contrast to their
great importance for the re-colonisation of major parts
of Europe, a fact that could only be demonstrated by the
recent genetic analyses.
R R
R
Siberia
R
R
R
R R
R
Siberia
R
R
R
Figure 5 Possible Würm glacial distribution patterns (indicated by "R") of the adder Vipera berus and assumed postglacial range
changes (arrows). The three major genetic lineages are indicated by different signatures of the refugia – dotted line, blue: western Balkan lineage;
broken line, red: south-eastern Alps line; solid line, black: widespread lineage with different sub-lineages. Redrawn after Ursenbacher et al. [55].
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Simultaneous ice age survival in Mediterranean
and extra-Mediterranean refugia of temperate
species
De Lattin’s paradigm [21] of survival of thermophilic
animal and plant species exclusively in Mediterranean
Würm refugia remained untouched until quite recently.
However, evidence has accumulated that glacial distribution
patterns were considerably more intricate than
previously thought [8,38], and even additional extraMediterranean
ice age refugia are looking more and more
likely for some of these Mediterranean taxa [11,12].
The combination of southern and continental refugia
became especially evident in the often cited case of the
“paradigmatic” brown bear, e.g. [42,62,74,95]. The successful
extraction and sequencing of mtDNA from fossil
bones has shown the highly complex phylogeographic
pattern of this species [68,69,71-73]. Thus, the predictions
of the “expansion-contraction” (E/C) model were not
supported, and consequently the classic glacial refugium
model is insufficient to explain the genetic history of
European brown bears.
The Pleistocene glacial refugia of the European
Bombina toads were located both in the “classical” refugial
areas of the Apennines and the Balkans (core areas
of B. pachypus and subspecies of B. variegata; [96,97]) as
well as more to the North, in the Carpathians and the
adjoining lowlands [98,99]. Also, strong genetic evidence
shows that B. variegata survived the LGM in climatically
favourable regions in the southern Carpathians. The
mtDNA and allozyme data suggest two separate refugia.
One clade probably had its refugium in the south-eastern
edge of the Carpathians, while the most likely refugium
of the other clade was in the area of the southern Carpathians
where the highest haplotype diversity was
a) b)
c)
CC
CC
CCCC
CCCC
CG
CG
CG
CGCG
CGCG
CGCG
SA
SA
UA
SASA
SASA
UAUA
Figure 6 Extra-Mediterranean refugia in eastern Europe and their postglacial expansions of (a) Sorex araneus (SA, black), Ursus arctos
(UA, brown), (b) Clethrionomys glareolus (CG) and (c) Cricetus cricetus (CC). Redrawn after Polyakov et al. [67], Hofreiter et al. [68], Hedrick &
Waits [69], Neumann et al. [70], Saarma et al. [62], Valdiosera et al. [71], Ho et al. [72], Krause et al. [73], Korsten et al. [74] and Ledevin et al. [75].
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detected (Figure 7). However, the deep genetic overall divergence
among European Bombina lineages suggests
their pre-Pleistocene origin. A similar south–north duplicity
was found in the common hamster (Cricetus cricetus)
in which a Pannonian and a northern clade have
been distinguished [70] with tracks of expansion (i)
crossing the “Porta Hungarica” into southern Czech Republic
(Moravia), and (ii) north of the Carpathian arc
into northern Central Europe (Figure 6c).
Furthermore, Fink et al. [100] found a genetic lineage
in the rodent Microtus arvalis, endemic to the region of
the Black Forest (south-western Germany). Tougard
et al. [63] described two more lineages of this species,
which most likely have evolved in extra-Mediterranean
refugia of Central and East Europe, including the Carpathian
Basin. Consequently, M. arvalis survived at least the
last ice age in a complex system of extra-Mediterranean
and classical Mediterranean core areas. However, we
have to assume that the more northern part of the glacial
distribution of this vole was, at least transitionally,
restricted to geographically small regions with a more
buffered climate, thus only some extra-zonal areas in the
periglacial tundra and steppe region, although M. arvalis
in general was a common component of fossil remains
of last glacial faunas [101].
The highly important recent work on the phylogeography
of the beech, Fagus sylvatica, [102,103] strongly suggest
a larger number of additional but geographically
restricted extra-Mediterranean Würm glacial refugia for
this species, which beforehand had always been considered
to be of pure Mediterranean origin cf. [6]. Thus,
retreats were demonstrated in Mediterranean southern
Italy and in a number of geographically restricted areas
in the Balkan Peninsula, of which some even should have
been located in the continental extra-Mediterranean part
of this peninsula. A similar pattern is true for Iberia
where the retreats were most probably located along the
northern mountain chains of the Cordillera Cantabrica
and thus in the extra-Mediterranean area of this region.
Further extra-Mediterranean refugia of the beech are
likely in two areas of southern France (with one in the
vicinity of the Massif Central), the eastern Alps and,
maybe, the Carpathian Basin (Apuseni Mts.) and the
northern Carpathians (Figure 8). Furthermore, refugia
for some other but more cold-tolerant tree species were
frequently proved for the Carpathian region and the Carpathian
Basin by classical pollen analyses and macrofossil
surveys, e.g. [37,38,104-112].
General discussion and conclusions
A large number of recent publications have shown the
great importance of extra-Mediterranean refugia for temperate
species and not only for alpine and arctic taxa.
While the latter two groups may have frequently had
wide ranges over this cold-continental zonobiome [10],
the glacial range contractions of thermophilic temperate
species, in most cases, must have led to small (and very
small) meso- or microclimatically favourable extra- or
intrazonal areas within the extended periglacial belt.
Many species with typical continental distributions
might have had glacial distribution patterns with multiple
extra-Mediterranean refugia, and were mostly not
V V
V
B
B
P
P
P
VV VV
VV
BB
BB
PP
PP
PP
Figure 7 Possible Würm glacial distribution patterns of fire-bellied toads (indicated by "B" (in red) for Bombina bombina, "V" (in black)
for B. variegata and "P" (in brown) for B. pachypus) and assumed postglacial range changes (arrows) in Europe. Areas of sympatry of
both species are indicated by hatched areas. Redrawn after Szymura et al. [96], Canestrelli et al. [97], Vörös et al. [98] and Hofman et al. [99].
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restricted to refuge areas in the eastern Palearctic, as
often previously thought. However, this is not to say that
they were absent from the eastern Palearctic, but these
contractions were not the exclusive ones for these
species.
Instead, recent research showed that even thermophilic
species, which were formerly thought of having
been completely restricted to Mediterranean core areas,
could in some cases survive in extra-Mediterranean refugia
in addition to the typical Mediterranean areas.
Such populations in many cases have an even higher
genetic diversity and expansive power than populations
restricted to the more southern “classical” refugia.
These observations can be explained by two different
factors, which might have acted in combination. The
southern refugia of temperate species were often surrounded
by extended cold-arid steppe areas, e.g. in the
central part of the Balkan Peninsula and also in the Carpathian
Basin [113]. Furthermore, the populations of the
scattered extra-Mediterranean refugial pockets could expand
and hybridise among each other during the milder
interstadial phases of the Würm and also between the
LGM and the younger Dryas period [12]. It means that
these extra-Mediterranean refuge populations have survived
at the rear edge of the range during the ice ages,
with all evolutionary consequences of this situation
[114]. These ice age rear edges became the leading edges
of the postglacial northwards range expansions, thus
strongly impacting the genetic constitution of Central
and North Europe in many plant and animal species. In
many cases, such populations have been characterised as
localised subspecies of extended polytypic continental
species, and they are considered as evolutionarily significant
units (ESUs) of high conservation priority [95].
For all these reasons, the extra-Mediterranean refugia
apparently represent an important biogeographical component
of the western Palaearctic, maybe nearly equivalent
to the Mediterranean refugia further south.
Through these new findings, we can also answer the
question of the article’s title: whether extra-Mediterranean
refugia are the rule or the exception. In fact, they are a
bit of both. Extra-Mediterranean refugia have been a
common feature during, at least, the last ice age and
thus are paradigmatic. However, they are also represented
by many individual patterns of particular biogeographical
features so that each case shows at least some
uniqueness. The principle of individual responses of the
species to climatic oscillations between glacial and interglacial
conditions was repeatedly postulated in this context
(cf. Stewart et al., [12], but also see Bhagwat &
Willis [36]). During glaciations, ecosystems that exist
today had been largely disintegrated and were represented
by de novo ecosystems without close connection
with the succeeding ones (e.g. the mammoth steppe with
tundra, cold steppic and alpine elements). These ecosystems
were locally intermingled with small forest refugia
(i.e. the pockets of forests of Bhagwat & Willis, [36])
and also showed non-analogous mammal assemblages
[13,35,77,115].
Therefore, no regular North–South shifts took place
between glacial and interglacial conditions and vice versa
(as implicitly assumed in the biogeographical range paradigms,
cf. [5,6]). Instead, a new sequence of ecosystems
always had to be established, influenced by a combination
of precipitation and temperature. The newly
evolved macro-biome of a continental cold steppe (that
no longer exists) must have had characteristic macroecotones
against the (glacially reduced) boreal forests
R
?
R
R
R
R
R
R
?
?
R
R
R
R
?
R
R
R
R
R
R
?
?
R
R
R
Figure 8 Possible Würm glacial distribution patterns (indicated by "R"; "?" is used in cases of still doubtful refuge areas) of the beech,
Fagus sylvatica, and assumed postglacial range changes (arrows). Redrawn after Magri et al. [102] and Magri [103].
Schmitt and Varga Frontiers in Zoology 2012, 9:22 Page 9 of 12
http://www.frontiersinzoology.com/content/9/1/22
and against the continental meadow steppes of temperate
latitudes.
Although not existing under the recent climatic conditions,
these macro-ecotones can be modelled based on
the zonality of the cold-continental conditions of southern
Siberia, northern Mongolia or even Yakutia. Here,
many floral and faunal elements can be observed together
on species-rich meadow steppes of these regions,
species assemblages, which are partitioned to different
habitats in eastern Europe like dry steppic grasslands,
meadow steppes, damp meadows or even salt meadows.
The large number of macro-ecotones with their specific
species assemblages is the background for the phenomenon
of the evolution of so many species specific biogeographies,
but hereby also for the paradigmatic patterns, i.
e. the regular existence of micro-refugia. However, this is
only a special case of the law of uniformity because even
today such micro-refugia with peculiar mixtures of faunal
and floral elements exist under analogous climatic
conditions.
Competing interests
The authors declare that they have no competing interests.
Author’s contributions
Both authors wrote this article in equal parts. Both authors read and
approved the final manuscript.
Author’s information
Thomas Schmitt is Professor of Molecular Biogeography at Trier University.
His main scientific interests are biogeography (classical and molecular),
ecology (classical and molecular), evolutionary biology, conservation biology
as well as the taxonomy of butterflies. He also has a special interest in the
high mountain systems of the western Palearctic.
Zoltán Varga is Professor emeritus of Zoology at the University of Debrecen.
His scientific focus is on biogeography, evolutionary biology, conservation
biology and ecology as well as the taxonomy of butterflies and noctuid
moths. He is one of the leading experts for the Carpathian Basin, the Balkan
Peninsula and the arid zones of Central Asia.
Author details
1
Biogeography, Trier University, D – 54 286, Trier, Germany. 2
Dept.
Evolutionary Zoology, Faculty of Science and Technology, University of
Debrecen, Egyetem-tér 1, Debrecen H-4010, Hungary.
Received: 29 June 2012 Accepted: 28 August 2012
Published: 6 September 2012
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doi:10.1186/1742-9994-9-22
Cite this article as: Schmitt and Varga: Extra-Mediterranean refugia: The
rule and not the exception?. Frontiers in Zoology 2012 9:22.
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