Species persistence in northerly glacial refugia of Europe: a matter of chance or biogeographical traits?

Authors

  • Shonil A. Bhagwat,

    Corresponding author
    1. Oxford Long-Term Ecology Laboratory, Biodiversity Research Group, Oxford University Centre for the Environment, Oxford, UK
      *Shonil Bhagwat, Oxford University Centre for the Environment, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK.
      E-mail: shonil.bhagwat@ouce.ox.ac.uk
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  • Katherine J. Willis

    1. Oxford Long-Term Ecology Laboratory, Biodiversity Research Group, Oxford University Centre for the Environment, Oxford, UK
    2. Department of Biology, University of Bergen, Bergen, Norway
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*Shonil Bhagwat, Oxford University Centre for the Environment, Dyson Perrins Building, South Parks Road, Oxford OX1 3QY, UK.
E-mail: shonil.bhagwat@ouce.ox.ac.uk

Abstract

Aim  The southern European peninsulas (Iberian, Italian and Balkan) are considered to have been refugia for many European species of plants and animals during the climatic extremes of the Pleistocene ice ages. A number of recent studies (fossil and genetic), however, have provided evidence for full-glacial survival of some species beyond these peninsulas. Here we explore the biogeographical traits of these species, and ask whether they possessed certain characteristics that enabled them to persist in more northerly refugia.

Location  Europe.

Methods  Fossil and genetic evidence for refugial localities of species that survived in Europe during the last full-glacial was obtained from the literature (totalling 90 species: 34 woody plants and 56 vertebrates). Forty-seven of these species (23 woody plants and 24 vertebrates) had fossil evidence, whereas the remaining 43 species (11 woody plants and 32 vertebrates) had only genetic evidence. All species were scored according to their present geographical distribution, habitat preference and life-history traits. The species were classified on the basis of these traits using hierarchical cluster analysis. Analysis of similarities was used to examine differences in vertebrate and woody plant species groups that survived only in southerly refugia and those that also persisted in more northerly locations. Non-metric multi-dimensional scaling was used to examine patterns observed between and within groups.

Results  Results from our analysis of species with fossil and genetic evidence for survival in refugia reveal that species that survived only in southerly refugia were large-seeded trees or thermophilous vertebrates. In contrast, species that had a full-glacial distribution, including more northerly locations, were wind-dispersed, habitat-generalist trees with the ability to reproduce vegetatively, and habitat-generalist mammals with present-day northerly distributions.

Main conclusions  Analysis of the geographical distribution, habitat preference and life-history traits of the species studied suggests that underlying biogeographical traits may have determined their response to Pleistocene glaciation. The traits most commonly found in present populations with a northerly distribution in Europe enabled the same species to exist much farther north than the southern European peninsulas during the full-glacial. It is possible that many of these species are now in restricted populations, within the ‘warm-stage’ refugia of the current interglacial. The northerly full-glacial survival of a number of woody plants and vertebrate species has significant implications for understanding migration rates of these species in response to climate change. It also has important implications for understanding current patterns of genetic diversity of European species. We suggest that both fossil and genetic evidence should be used to identify and prioritize for conservation of refugial localities in southern and northern Europe.

Introduction

During the Pleistocene ice ages, large areas of northern Europe were covered by ice sheets, while glaciers and ice fields developed in many mountain regions of central and southern Eurasia, including the Pyrenees, the Alps, the Carpathians and the Caucasus (Ehlers & Gibbard, 2003) (Fig. 1). Beyond the ice sheets and glaciers, permafrost covered much of the landscape of northern and western Europe, and aeolian sands were widespread. The permafrost is believed to have extended down to 40° N latitude (CGMW-ANDRA, 1999). Farther south, however, areas remained relatively ice-free and probably supported relict soils. This applies particularly to the three peninsulas of southern Europe (Iberian, Italian and Balkan) (Ehlers & Gibbard, 2003).

Figure 1.

 During the Pleistocene ice ages, large areas of northern Europe were covered by ice-sheet (hatched), and glaciers and ice fields developed in many mountain regions of central and southern Eurasia (also hatched). At the last glacial maximum (LGM), beyond the ice sheets and glaciers, the landscape of much of northern and western Europe was covered in permafrost (light grey) (CGMW-ANDRA, 1999). The southern European peninsulas (Iberian, Italian and Balkan) (dark grey) are considered to have acted as full-glacial refugia for many species. However, recent fossil and genetic evidence suggests that a number of species persisted close to the boundary of the ice-sheet within the permafrost landscape, much farther north of the southern European peninsulas. The spots on light grey background suggest a continuous gradient in northerly refugia related to the north–south environmental gradient; and arrows indicate more northerly locations of refugia for many species than commonly believed.

Palaeoclimatic simulations indicate that strong climatic gradients existed across Europe during the last glacial maximum (LGM), with a north–south gradient from arctic to cold temperate climates north of the trans-European mountain barrier and a west–east transition from the maritime Atlantic climate to the continental climate of eastern Europe (Barron & Pollard, 2002). This resulted in strong regional differences in surface temperatures. Barron & Pollard’s (2002) estimates suggest that winter temperatures in northern Europe were up to 10–20°C cooler than they are today, in southern Europe and parts of central Europe they were 7–10°C cooler, whereas in more south-westerly regions such as Spain they were only 2–4°C cooler. There was also a strong east–west gradient in winter and summer precipitation, bringing more precipitation to central and south-eastern Europe than to the three southern peninsulas of Europe (Barron et al., 2003).

The suggested location of plants and animals in Europe during the last full-glacial has traditionally favoured a ‘southerly refugial model’, which proposes that temperate fauna and flora survived in the three southern peninsulas of Europe (Bennett et al., 1991). This model is based on the premise that the apparently inhospitable climate and soils of central and northern Europe would have rendered these areas incapable of supporting woody temperate vegetation and the fauna associated with this vegetation (Huntley & Birks, 1983; Bennett et al., 1991). Much interest (fossil and genetic) has therefore been focused on the impact of glacial isolation on populations in these three southern peninsulas. There is now considerable evidence to support the survival and genetic isolation of populations of both plants and animals in these peninsulas, usually in isolated pockets (e.g. south-facing slopes), and often in apparently very small populations (Willis, 1996; Hewitt, 2000; Tzedakis et al., 2002).

More recently, however, some studies (fossil and genetic) have indicated that more northerly regions, including areas in central and eastern Europe, may also have supported small populations of plants and animals (Willis & Whittaker, 2000; Willis et al., 2000; Davison et al., 2001; Stewart & Lister, 2001; Vernesi et al., 2002; Babik et al., 2004; Willis & Van Andel, 2004; Kotlik et al., 2006). These refugia are often referred to as ‘cryptic northern refugia’ (Stewart & Lister, 2001) and are suggested to have been located in small microenvironmentally favourable sites – although some of the evidence from the macrofossil charcoal records suggests a more diffuse distribution of trees across the central European landscape (Willis & Van Andel, 2004). With a growing body of recent literature providing evidence (both fossil and genetic) arguing for the survival of species in northerly refugia (Petit et al., 2003; Lascoux et al., 2004; Terhurne-Berson et al., 2004; Deffontaine et al., 2005; Kotlik et al., 2006), the time is ripe to ask whether there are any obvious biogeographical differences between those species known to have persisted only in southerly refugia and those that not only survived in the south but also appear to have had populations farther north and east in Europe. We define northerly refugia as areas north of the southerly European peninsulas (Iberian, Italian and Balkan) but south of the LGM ice-sheet boundary (Fig. 1). We do not suggest that species that persisted in northerly refugia were distributed in northerly locations alone – they could also have survived in the south. However, species that have evidence of survival only in southerly refugia at the full-glacial would have been restricted to the southern peninsulas of Europe. Our focus is on the ‘ability’ of certain plant and animal species to persist in northerly locations under full-glacial conditions.

In this study we therefore pose the question: did species that demonstrate evidence for full-glacial refugial persistence in northern Europe possess certain traits that enabled their survival? If the northerly refugia were microenvironmentally favourable habitat patches as assumed in the literature (Stewart & Lister, 2001), did the trees that persist in these patches have long-range dispersal ability, i.e. small seeds (e.g. Jacquemyn et al., 2003)? Plants with small seeds and the ability to reproduce vegetatively are suggested to be common in the present day in the harsh environments of northern latitudes (e.g. Welling et al., 2004). Did the species associated with northerly refugia have the ability to reproduce vegetatively under harsh environmental conditions? For animals that persisted in northerly refugia, did the restricted habitat only allow the persistence of animals with small home ranges and small body sizes (e.g. Crooks, 2002)? It has also been recently suggested that in northern latitudes animals tend to be small and have high metabolic rates to cope with harsh environmental conditions (e.g. Li & Wang, 2005). This is in contrast with Bergmann’s rule, which suggests an increase in the body size of a species towards higher latitudes and lower temperatures (Bergmann, 1847; Smith et al., 1995). Bergmann’s rule is also suggested to be applicable at interspecific (e.g. Freckleton et al., 2003) and assemblage (e.g. Blackburn & Hawkins, 2004) levels. However, the literature also suggests many examples where Bergmann’s rule does not apply (e.g. Ashton & Feldman, 2003; Meiri & Dayan, 2003; Blanckenhorn & Demont, 2004). It appears, therefore, that the factors that may have been responsible for species persistence in northerly refugia are confounding. This demands a critical analysis of plant and animal traits. The overall aim of this work, therefore, is to explore a number of traits of plant and animal species that survived in the Pleistocene glacial refugia of Europe. We ask whether the ability of some species to apparently persist in northerly locations was a matter of chance or biogeographical traits, and examine which traits were important in their northerly survival.

Methods

A literature search was undertaken for studies that presented fossil and/or genetic evidence for the survival of plant and animal species in Europe in the LGM using the key words ‘glacial refugia’, ‘Pleistocene refugia’ and ‘Europe’. Where evidence was contradictory the most recent reference was used, assuming that the later reference presented more reliable evidence (particularly in the case of genetic studies, owing to developments in the techniques used). Where evidence for more than one species was presented in one publication (e.g. Taberlet et al., 1998; Hewitt, 1999; Stewart & Lister, 2001) each species was treated separately. We ensured that the fossil evidence for plant species presence, where possible, came from plant macrofossils, as well as macrofossil charcoal and pollen. It has been suggested that the presence of pollen alone does not provide strong evidence for the presence of the plant species because of long-distance pollen movement (e.g. Jackson et al., 2000). It has also been demonstrated that pollen production is greatly reduced in cold conditions, especially when there is also a reduction in atmospheric carbon dioxide (Loehle, 2007). Therefore, in the studies reviewed, where fossil evidence came from pollen we ensured that it was supported by the presence of macrofossils. For inclusion in our analysis we chose studies that dealt with species of perennial woody plants and vertebrates. This resulted in a sample of 34 woody plant species (including angiosperms and gymnosperms) and 56 vertebrate species (including herptiles, birds and mammals). Forty-seven of these species (23 woody plants and 24 vertebrates) had fossil evidence, and the remaining 43 species (11 woody plants and 32 vertebrates) had only genetic evidence. Each of these 90 species was scored for presence or absence of a number of biogeographical traits (Table 1). We use the term ‘biogeographical trait’ (or ‘trait’ in short) to refer to various geographical (geographical distribution), ecological (habitat preference) and life-history traits (generation time, body size, mobility, seed size, vegetative reproduction). The present-day northerly geographical distribution further encompasses a number of physiological adaptations, and habitat preference encompasses a number of ecological adaptations.

Table 1.   Biogeographical traits scored for the woody plant and vertebrate species surveyed.
TraitAnimal (A), plant (P)Presence (= 1) or absence (= 0) of traits that may have enabled northerly survival of species
  1. Flora Europaea (Tutin et al., 1964), Atlas Florae Europaeae (Jalas & Souminen, 1972–94) and Fauna Europaea (Fauna Europaea Web Service, 2004) were used to score traits.

Geographical
 Geographical distributionA, PPresent-day northerly distribution = 1; present-day southerly distribution = 0 (where northerly distribution > 60° N)
Habitat
 Habitat preferenceA, PHabitat generalist species = 1; habitat specialist species = 0 (habitat preferences determined from species accounts in Flora Europaea and Fauna Europaea)
Life history
 Generation timeA, PShort-lived species = 1; long-lived species = 0 (where generation time for short-lived species < 5 years)
 Body sizeASmall-bodied species = 1; large-bodied species = 0 (where body mass for small-bodied species < 5 kg)
 Seed sizePSmall-seeded species = 1; large-seeded species = 0 (where seed mass for small-seeded species < 100 mg)
 MobilityASpecies with high mobility = 1; species with low mobility = 0 (mobility determined from species accounts in Fauna Europaea)
 Vegetative reproductionPSpecies able to reproduce vegetatively = 1; species unable to reproduce vegetatively = 0 (ability to reproduce vegetatively determined from species accounts in Flora Europaea)

The present-day geographical distribution was considered important because a more northerly distribution is related to the species’ ability to survive in cooler climates (Portner, 2002). Habitat preference was also considered important because habitat-generalist species by definition have a greater tolerance to a wide range of environmental conditions than do habitat-sensitive species (e.g. Cooper & Gessaman, 2004). The life-history trait we considered important for both woody plants and vertebrates was generation time – short generation times would allow rapid breeding and dispersal in harsh environments (e.g. Clark et al., 2001). For vertebrates, body size was considered important. Although Bergmann’s rule (Bergmann, 1847) suggests an increase in body size towards higher latitudes and lower temperatures, the habitats in northerly refugia are believed to have been patchy and restricted to microenvironmentally favourable locations (Stewart & Lister, 2001). This means that the habitats may not have been large enough to support vertebrates with large home range and body size. Furthermore, vertebrates with small body size have higher metabolic rates, enabling their survival in cold climates (e.g. Li & Wang, 2005). Therefore, small body size was considered important for persistence in northerly glacial refugia. In addition, mobility was considered an important factor because highly mobile vertebrates may have had an advantage when surviving in refugia surrounded by a permafrost landscape (e.g. Andreev, 1999). For woody plants, seed size was considered important. If northerly refugia were patchy and at microenvironmentally favourable locations (Stewart & Lister, 2001), long-range dispersal would have been an important factor in the persistence of species at such sites. Furthermore, in permafrost landscapes, where the levels of soil nutrients and energy are both low, plants with smaller seeds are better adapted for survival (e.g. Welling et al., 2004) because small seeds have the ability to persist better in soil seed banks than do large seeds (Thompson, 1987; Thompson et al., 1993; Opik & Rolfe, 2005). The ability for vegetative reproduction was also considered important for northerly survival because plants able to reproduce vegetatively are better adapted to surviving harsh climatic conditions (e.g. Whitehill & Schwabe, 1975). Vegetative reproduction represents any form of reproduction without sexual recombination; this includes clonal spread from roots, stems, or leaves (Koop, 1987). However, many boreal species are known to reproduce through vegetative buds under harsh climatic conditions because sexual reproduction is limited or non-existent (Bonan & Shugart, 1989). We refer specifically to this ability of vegetative reproduction under harsh environmental conditions. In terms of reproductive traits in plants there are therefore at least two responses to cooler climatic conditions, namely vegetative reproduction and smaller seed size. Both have been shown to enable survival in arctic and alpine conditions (Welling et al., 2004).

We used Flora Europaea (Tutin et al., 1964), Atlas Florae Europaeae (Jalas & Souminen, 1972–94) and Fauna Europaea (Fauna Europaea Web Service, 2004) to score all biogeographical traits (Table 1). The present-day geographical distribution was considered northerly if the species was distributed north of 60° N latitude. Generation time for woody plants and vertebrates was considered short if longevity was <5 years. Body size was considered small if body mass was below 5 kg, and seed size was considered small if seed mass was below 100 mg. Habitat preference of woody plants and vertebrates, mobility of vertebrates and the ability for vegetative reproduction of woody plants were determined from species accounts in Flora Europaea (Tutin et al., 1964) and Fauna Europaea (Fauna Europaea Web Service, 2004).

Species were divided into (1) those that had confirmed fossil evidence for survival in southerly or northerly refugia (47 species: 23 woody plants and 24 vertebrates); and (2) those that had only genetic evidence for presumed survival (43 species: 11 woody plants and 32 vertebrates) (Tables 2–5).

Table 2.   List of woody plant species known to have survived in European glacial refugia confirmed through the presence of fossil (pollen, plant macrofossil, macroscopic charcoal) evidence and genetic evidence (where present).
No.Scientific name (acronym)Common nameGlacial refugia (north N, south S)Fossil evidenceGenetic evidenceBiogeographical traits
Present-day northerly distributionHabitat generalistShort generationSmall seedsVegetative reproduction
  1. In column ‘Glacial refugia’, S denotes survival only in southerly refugia and N denotes persistence in northerly refugia (in addition to southerly survival). In column ‘Biogeographical traits’, scores are based on criteria described in Table 1.

 1Abies alba (abialb)Fir, SilverNTerhurne-Berson et al. (2004); Müller et al. (2007)00011
 2Alnus glutinosa (alnglu)Alder, BlackNWillis & Van Andel (2004)King & Ferris (1998)11011
 3Betula pendula (betpen)BirchNWillis et al. (2000)Palme et al. (2003)11010
 4Carpinus betulus (carbet)HornbeamSWillis et al. (2000)Grivet & Petit (2003)00000
 5Carpinus orientalis (carori)HornbeamSTzedakis (1993)Grivet & Petit 2003)00000
 6Castanea sativa (cassat)Chestnut, SweetSKrebs et al. (2004)00000
 7Fagus sylvatica (fagsyl)Beech, CommonNMagri et al. (2006)Magri et al. (2006)00000
 8Fraxinus excelsior (fraexc)Ash, CommonNWillis & Van Andel (2004)Heuertz et al. (2004)00011
 9Juniperus communis (juncom)JuniperNWillis & Van Andel (2004)10011
10Picea abies (picabi)Spruce, NorwayNRavazzi (2002)10011
11Picea omorika (picomo)SpruceNRavazzi (2002)00011
12Pinus cembra (pincem)PineNWillis & Van Andel (2004)01011
13Pinus mugo (pinmun)PineNWillis & Van Andel (2004)01011
14Pinus sylvestris (pinsyl)Pine, ScotsNWillis & Van Andel (2004); Feurdean et al. (2007)Cheddadi et al. (2006)10011
15Quercus macranthera (quemac)OakSPetit et al. (2002a)Petit et al. (2002b)00000
16Quercus petraea (quepet)OakSPetit et al. (2002a)Kremer et al. (2002)00000
17Quercus pubescens (quepub)OakSPetit et al. (2002a)Petit et al. (2002b)00000
18Quercus pyrenaica (quepyr)OakSPetit et al. (2002a)Petit et al. (2002b)00000
19Quercus robur (querob)OakSPetit et al. (2002a)Cottrell et al. (2002)00000
20Quercus sp. (quesp1)OakSPetit et al. (2002a)Chiang (2000)00000
21Quercus sp. (quesp2)OakNStewart & Lister (2001)00000
22Quercus sp. (quesp3)Oak, DeciduousSBrewer et al. (2002)Brewer et al. (2002)00000
23Salix sp. (salspp)WillowNWillis et al. (2000)11011
24Taxus baccata (taxbac)YewNWillis & Van Andel (2004)11010
Table 3.   Woody plant species surveyed in the literature for which only genetic evidence for survival in European glacial refugia is available.
No.Scientific name (acronym)Common nameGlacial refugia (north N, south S)Genetic evidenceBiogeographical traits
Present-day northerly distributionHabitat generalistShort generationSmall seedsVegetative reproduction
  1. In column ‘Glacial refugia’, S denotes survival only in southerly refugia and N denotes persistence in northerly refugia (in addition to southerly survival). In column ‘Biogeographical traits’, scores are based on criteria described in Table 1.

 1Calluna vulgaris (calvul)HeatherNRendell & Ennos (2002)11111
 2Corylus avellana (corave)HazelNPalme & Vendramin (2002)11000
 3Frangula alnus (fraaln)Buckthorn, AlderNHampe et al. (2003)01000
 4Hedera sp. (hedspp)Ivy, CommonSGrivet & Petit, (2002)11001
 5Ilex aquifolium (ileaqu)Holly, EnglishSRendell & Ennos (2003)11000
 6Populus nigra (popnig)Poplar, BlackSCottrell et al. (2005)00011
 7Prunus spinosa (pruspi)PrunusSMohanty et al. (2002)01001
 8Quercus canariensis (quecan)OakSPetit et al. (2002b)00000
 9Quercus faginea (quefag)OakSPetit et al. (2002b)00000
10Quercus frainetto (quefra)OakSPetit et al. (2002b)00000
11Quercus ilex (queile)Oak, HolmSFineschi et al. (2005)00000
Table 4.   List of vertebrate species known to have survived in European glacial refugia confirmed through the presence of fossil evidence and genetic evidence (where present).
No.Scientific name (acronym)Common nameGlacial refugia (north N, south S)Fossil evidenceGenetic evidenceBiogeographical traits
Present-day northerly distributionHabitat generalistShort generationSmall bodyHigh mobility
  1. In column ‘Glacial refugia’, S denotes survival only in southerly refugia and N denotes persistence in northerly refugia (in addition to southerly survival). In column ‘Biogeographical traits’, scores are based on criteria described in Table 1.

 1Alces alces (alcalc)MooseNSommer & Nadachowski (2006)11001
 2Alopex lagopus (alolag)Fox, ArcticNSommer & Benecke (2005a)11001
 3Aquila adalberti (aquada)Eagle, Spanish ImperialSFerrer & Negro (2004)01001
 4Canis lupus (canlup)WolfNSommer & Benecke (2005a)11001
 5Capreolus capreolus (capcap)Deer, RoeNSommer & Nadachowski (2006)Vernesi et al. (2002)11001
 6Castor fiber (casfib)BeaverNSommer & Nadachowski (2006)10000
 7Cervus elaphus (cerela)Deer, RedNLister (1984); Stewart & Lister (2001); Sommer & Nadachowski (2006)11001
 8Clethrionomys glareolus (clegla)Vole, BankNNadachowski (1989)Deffontaine et al. (2005); Kotlik et al. (2006)00110
 9Cricetus cricetus (cricri)Hamster, European CommonN(Hir 1997)Neumann et al. (2005)11110
10Dicrostonyx torquatus (dictor)Lemming, CollaredNStewart & Lister (2001)10111
11Felis sylvestris (felsyl)Cat, wildSSommer & Nadachowski (2006)10001
12Gulo gulo (gulgul)WolverinesNSommer & Nadachowski (2006)11001
13Lutra lutra (lutlut)Otter, EurasianSSommer & Benecke (2004)10000
14Lynx lynx (lynlyn)Lynx, EurasianNSommer & Nadachowski (2006)11001
15Lynx pardinus (lynpar)Lynx, IberianSFerrer & Negro (2004)01001
16Martes martes (marmar)Marten, PineNSommer & Nadachowski (2006)Davison et al. (2001)10110
17Meles meles (melmel)Badger, EurasianSSommer & Benecke (2004); Sommer & Nadachowski (2006)11000
18Microtus oeconomus (micoec)Vole, RootNChaline (1987)Brunhoff et al. (2003)11110
19Rana arvalis (ranarv)Frog, MoorNVenczel (1997)Babik et al. (2004)10110
20Rangifer tarandus (rantar)ReindeerNSommer & Nadachowski (2006)11001
21Strix aluco (stralu)Owl, TawnySPavia (2001)Brito (2005)11001
22Sus scrofa (susscr)Boar, wildSSommer & Nadachowski (2006)11001
23Ursus arctos (ursarc)Bear, BrownNSommer & Benecke (2005b); Sommer & Nadachowski (2006)10001
24Vulpes vulpes (vulvul)Fox, RedNSommer & Benecke (2005a)11001
Table 5.   Vertebrate species surveyed in the literature for which only genetic evidence for survival in European glacial refugia is available.
No.Scientific name (acronym)Common nameGlacial refugia (north N, south S)Genetic evidenceBiogeographical traits
Present-day northerly distributionHabitat generalistShort generationSmall bodyHigh mobility
  1. In column ‘Glacial refugia’, S denotes survival only in southerly refugia and N denotes persistence in northerly refugia (in addition to southerly survival). In column ‘Biogeographical traits’, scores are based on criteria described in Table 1.

 1Apodemus flavicollis (apofla)Fieldmouse, Yellow-neckedSMichaux et al. (2004)11110
 2Bombina bombina (bombom)Toad, Fire-belliedSHewitt (2001)01110
 3Bufo calamita (bufcal)Toad, NatterjackNRowe et al. (2006)11110
 4Crocidura suaveolens (crosua)Shrew, EurasianSDubey et al. (2006)11110
 5Erinaceus concolor (ericon)HedgehogSSeddon et al. (2001)01110
 6Erinaceus europaeus (erieur)Hedgehog, EuropeanSSeddon et al. (2001)01110
 7Fringilla coelebs (fricoe)Chaffinch, CommonSGriswold & Baker (2002)11111
 8Gypaetus barbatus (gypbar)Vulture, BeardedSGodoy et al. (2004)00001
 9Lacerta schreiberi (lacsch)Lizard, IberianSPaulo et al. (2001)00110
10Lemmus lemmus (lemlem)Lemming, NorwegianNFedorov & Stenseth (2001)11111
11Lepus europaeus (lepeur)Hare, BrownSKasapidis et al. (2005)11111
12Lissotriton boscai (lisbos)SalamanderSMartińez-Solano et al. (2006)00110
13Microtus agrestis (micagr)Vole, FieldNJaarola & Searle (2002)11110
14Microtus arvalis (micarv)Vole, CommonNHeckel et al. (2005)11110
15Milvus milvus (milmil)Kite, RedSRoques & Negro (2005)00001
16Miniopterus schreibersii (minsch)Bat, Large bentwingSBilgin et al. (2006)00111
17Mustela putorius (musput)PolecatNDavison et al. (2001);
Sommer & Benecke (2004)
10111
18Myotis myotis (myomyo)Bat, Greater Mouse-earedSCastella et al. (2001)00111
19Nyctalus noctula (nycnoc)Bat, NoctuleSPetit et al. (1999)10111
20Oryctolagus cuniculus (orycun)Rabbit, EuropeanSFerrer & Negro (2004)11111
21Oxyura leucocephala (oxyleu)Duck, White-headedSMuńoz-Fuentes et al. (2005)00001
22Perdix perdix (perper)Partridge, GreySLiukkonen-Anttila et al. (2002)01000
23Rana lessonae (ranles)Frog, PoolNSnell et al. (2005)10110
24Sorex araneus (sorara)Shrew, CommonNBilton et al. (1998)11110
25Sorex minutus (sormin)Shrew, PygmyNBilton et al. (1998)11110
26Triturus carekini (tricai)Newt, Southern CrestedSTaberlet et al. (1998)00110
27Triturus carnifex (tricax)Newt, Italian CrestedSTaberlet et al. (1998)00110
28Triturus cristatus (tricri)Newt, CrestedSHewitt (2001)10110
29Triturus marmoratus (trimar)Newt, MarbledSTaberlet et al. (1998)00110
30Triturus pygmaeus (tripyg)Newt, Pygmy MarbledSTaberlet et al. (1998)00110
31Vipera aspis (vipasp)Viper, AspNUrsenbacher et al. (2006b)00110
32Vipera berus (vipber)AdderNUrsenbacher et al. (2006a)00110

Hierarchical cluster analysis (HCA) was used to classify species based on their biogeographical traits. This numerical procedure identifies relatively homogeneous groups of species based on selected characteristics, using an algorithm that starts with each species in a separate cluster and combines clusters until only one is left (Anderberg, 1973). The procedure was implemented in spss 14. The Euclidean distance measure was used, and clustering was performed with between-group linkage. The dendrogram was drawn on a 0–25 scale because spss 14 rescales the Euclidean distances and presents them as distance-cluster combinations.

Analysis of similarities (anosim) was used to examine if there is a significant difference (1) between the HCA groups based on biogeographical traits; and (2) between species groups based on evidence for (a) survival only in southerly and (b) persistence in northerly refugia. anosim allows statistical testing of whether there is a significant difference between two or more groups. The past software package (Hammer et al., 2001) was used to perform this analysis, and the Euclidean distance measure was employed.

Non-metric multi-dimensional scaling (NMDS) was used to examine patterns observed between and within groups classified by HCA. This numerical technique assigns species to specific locations in a low-dimensional space such that the ranked distances between points in the low-dimensional space match the ranked dissimilarities as closely as possible. Therefore, the more dissimilar species are in their traits, the farther apart in low-dimensional space they appear; conversely, species with similar traits are positioned together. The alscal algorithm in spss 14 (Johnson & Wichern, 1982) allowed the NMDS of presence–absence data in two dimensions. The Euclidean distance measure was used, and the analyses were run with default criteria, namely S-stress convergence 0.001, minimum S-stress value 0.005, and maximum iterations 30. S-stress is a measure of the mismatch between the original ranked Euclidean distances and the actual ranked distances between species (dissimilarity). Therefore, the lower the S-stress value, the closer the match between the two sets of ranked distances (Palmer, 2006).

Results

Woody plant species

Out of a total of 23 woody plant species that have confirmed fossil evidence, seven are needle-leaved, coniferous gymnosperms and 16 are broad-leaved angiosperms. The dendrogram produced by HCA divides the woody plant species into two groups (Fig. 2).

Figure 2.

 Dendrogram showing the results of a hierarchical cluster analysis of biogeographical traits of woody plant species. The data matrix of presence (1) or absence (0) of traits is used (Table 2). The clustering is based on between-group linkage, and the Euclidean distance measure is used. Acronyms for species that have evidence for persistence in northerly refugia are highlighted in grey. Scientific names corresponding to each acronym are provided in Table 2. Clusters are named after common characteristics of a majority of the group members.

Group 1. Small-seeded, wind-dispersed angiosperms and gymnosperms

The fossil evidence for all 12 species in this group suggests that they persisted in northerly refugia. These species are either broad-leaved trees or shrubs or coniferous trees that are cold-tolerant, have present-day northerly distributions, and small, wind-dispersed seeds. Many of these species are habitat generalists and have the ability to reproduce vegetatively. These species possess a wide range of traits and form a quite dissimilar group (Fig. 2).

Group 2. Large-seeded, animal-dispersed angiosperms

The fossil evidence for 10 out of 11 species surveyed in this group suggests that they survived only in southerly refugia. Only one species, Fagus sylvatica (acronym highlighted in grey), has evidence for survival in northerly refugia. All these species are broad-leaved, thermophilous and habitat-specialist trees that have large seeds, and they are unable to reproduce vegetatively. These species are extremely similar to each other in their traits and form a closely knit group (Fig. 2).

The two HCA groups are statistically significantly different from each other (anosim, = 0.685, < 0.0001). When all species are grouped into (a) those that survived only in southerly refugia; and (b) those that persisted in northerly refugia, anosim once again shows a statistically significant difference (= 0.543, = 0.002) between the two groups.

The NMDS plot of woody plant species for which fossil evidence is available shows a clear separation between the two groups (Fig. 3) classified by HCA. When all species, including those that have genetic evidence alone, are included in the NMDS analysis, the two groups are still separated from one another; however, a number of species for which only genetic evidence is available contradict the pattern (Fig. 4). Populus nigra, similar in all traits to other species in Group 1, survived only in southerly refugia (according to genetic evidence alone; dashed grey circle). Moreover, species such as Hedera sp. (a woody climber), Ilex aquifolium (a small tree) and Prunus spinosa (a shrub), all of which survived only in southerly refugia (according to genetic evidence alone; solid grey circles), are, in fact, closer in traits (except for their large seeds) to some species that persisted in northerly refugia (Group 1).

Figure 3.

 Non-metric multi-dimensional scaling plot of woody plant species for which fossil evidence is available. The data matrix of presence (1) or absence (0) of traits is used (Table 2). The S-stress convergence is 0.001, the minimum S-stress value is 0.005, the maximum number of iterations is 30, and the Euclidean distance measure is used. Group 1, demarcated by a dashed line, consists mainly of small-seeded, wind-dispersed gymnosperms and angiosperms, all of which have fossil evidence for persistence in northerly refugia. Group 2, demarcated by a solid line, consists of large-seeded angiosperms, all of which except Fagus sylvatica have fossil evidence for survival only in southerly refugia.

Figure 4.

 Non-metric multi-dimensional scaling plot of all woody plant species. The data matrices of presence (1) or absence (0) of traits are used (Tables 2 and 3). The S-stress convergence is 0.001, the minimum S-stress value is 0.005, the maximum number of iterations is 30, and the Euclidean distance measure is used. Group 1, demarcated by a dashed line, consists mainly of small-seeded, wind-dispersed gymnosperms and angiosperms that have fossil evidence for persistence in northerly refugia (Fig. 3). This group also consists of species that contradict this pattern: a small-seeded species that has evidence for survival in southerly refugia (genetic evidence only; dashed grey circle) or large-seeded species, closer in other traits to species in this group but have evidence for survival only in southerly refugia (genetic evidence only; solid grey circles). Group 2, demarcated by a solid line, consists mainly of large-seeded angiosperms that have fossil evidence for survival only in southerly refugia (Fig. 3). This group also consists of a species that contradicts this pattern: a large-seeded angiosperm that has evidence for persistence in northerly refugia (dashed grey circle).

Vertebrate species

Out of a total of 24 vertebrate species that have confirmed fossil evidence 16 are large-bodied mammals, two are large-bodied birds, five are small-bodied mammals, and one is an amphibian. The dendrogram produced by HCA divides the vertebrate species into two groups (Fig. 5).

Figure 5.

 Dendrogram showing the results of a hierarchical cluster analysis of biogeographical traits of vertebrate species. The data matrix of presence (1) or absence (0) of traits is used (Table 4). The clustering is based on between-group linkage, and the Euclidean distance measure is used. Acronyms for species that have evidence for persistence in northerly refugia are highlighted in grey. Scientific names corresponding to each acronym are provided in Table 4. Clusters are named after common characteristics of a majority of group members.

Group 1. Small-bodied mammals and an amphibian

The fossil evidence for all five small mammals and the one amphibian (Rana arvalis) in this group suggests that they persisted in northerly refugia. These species are small-bodied and have shorter generation times relative to other species in their taxonomic group. They also are cold-tolerant, have present-day northerly distributions, and most of them are habitat generalists (Fig. 5).

Group 2. Large mammals and birds

The fossil evidence for seven out of the 18 large mammals and birds surveyed suggests that they survived only in southerly refugia. Apart from being large-bodied, these species have long generation times relative to other species in their taxonomic group. They are thermophilous, and have present-day southerly distributions. The remaining 11 species have fossil evidence for survival also in northerly refugia. Although these species are large-bodied, they are cold-tolerant and therefore have present-day northerly distributions. Many of the species in this group are habitat specialists, but some are generalists. Therefore, this group is composed of species that display a mixture of traits (Fig. 5).

The two HCA groups are statistically significantly different from each other (anosim, = 0.429, < 0.0001). However, when species are grouped into (a) those that survived only in southerly refugia; and (b) those that persisted in northerly refugia, anosim does not show a statistically significant difference (= −0.160, = 0.850) between the two groups owing to the mixed composition of Group 2 (large-bodied mammals and birds).

The NMDS plot of vertebrate species for which fossil evidence is available shows separation between the two groups (Fig. 6) classified by HCA. When all species are included in the NMDS analysis, the two groups are still separated from one another. However, a number of species for which only genetic evidence is available contradict the pattern (Fig. 7). A number of large-bodied mammal species belonging to Group 2 have evidence for survival in northerly refugia according to genetic evidence (Fig. 7). Small mammal species such as Apodemus flavicollis and Crosidura suaveolens belonging to Group 1 survived only in southerly refugia (according to genetic evidence alone; dashed grey circles). Moreover, a number of herptiles, such as Lacerta schreiberi, Lissotriton boscai and Triturus cristatus, belonging to Group 1 survived only in southerly refugia (according to genetic evidence alone; solid grey circles).

Figure 6.

 Non-metric multi-dimensional scaling plot of vertebrate species for which fossil evidence is available. The data matrix of presence (1) or absence (0) of traits is used (Table 4). Group 1, demarcated by a dashed line, consists of small-bodied mammals and an amphibian (Rana arvalis), all of which have fossil evidence for persistence in northerly refugia. Group 2, demarcated by a solid line, consists of large-bodied mammals and birds, some of which have evidence for survival only in southerly and some in northerly refugia.

Figure 7.

 Non-metric multi-dimensional scaling plot of all vertebrate species. The data matrices of presence (1) or absence (0) of traits are used (Tables 4 and 5). Group 1, demarcated by a dashed line, consists mainly of small-bodied mammals that have fossil evidence for persistence in northerly refugia (Fig. 5). This group also consists of species that contradict this pattern: small-bodied mammals that have evidence for survival only in southerly refugia (genetic evidence only; dashed grey circles); and herptiles that also have evidence for survival only in southerly refugia (genetic evidence only; solid grey circles). Group 2, demarcated by a solid line, consists of large-bodied mammals and birds, some of which have fossil evidence for survival only in southerly refugia and some in northerly refugia (Fig. 5). The species that have evidence for persistence in northerly refugia are demarcated by dashed grey circles.

Discussion

Woody plant species in glacial refugia

The pattern for survival of large-seeded, broad-leaved, thermophilous angiosperm trees only in southerly refugia is clear, and the difference in traits between species that survived only in southerly refugia and those that had the ability to persist in northerly refugia is statistically significant. Both fossil and genetic evidence for a number of oak (Quercus spp.) species strongly suggests that they survived only in southerly refugia at the last full-glacial (e.g. Brewer et al., 2002; Petit et al., 2002a; de Heredia et al., 2007). Similarly, fossil evidence for Carpinus betulus (Willis et al., 2000) and Carpinus orientalis (Tzedakis, 1993) as well as genetic evidence (Grivet & Petit, 2003), and fossil evidence (Krebs et al., 2004) for Castanea sativa suggest that they also survived only in southerly refugia. An exception is Fagus sylvatica (Fig. 3; Fig. 4, Group 2, dashed grey circle), which shows fossil and genetic evidence for northerly survival (Magri et al., 2006).

The pattern for the persistence of small-seeded, wind-dispersed, coniferous and some broad-leaved trees in northerly refugia also appears to be clear. Both fossil and genetic evidence for Pinus sylvestris (Cheddadi et al., 2006), Abies alba (Terhurne-Berson et al., 2004; Müller et al., 2007), Picea abies and Picea omorika (Ravazzi, 2002) suggests persistence in northerly refugia. Fossil and genetic evidence for Fraxinus excelsior (Heuertz et al., 2004; Willis & Van Andel, 2004) and Alnus glutinosa (King & Ferris, 1998; Willis & Van Andel, 2004), both broad-leaved angiosperm trees with predominantly wind-dispersed seeds, also suggests their northerly persistence. Fossil (Willis et al., 2000) and genetic (Palme et al., 2003) evidence for the northerly persistence of Betula pendula, a wind-dispersed species (Wagner et al., 2004), is available. Fossil evidence (Willis & Van Andel, 2004) also exists for the northerly persistence of Taxus baccata. It is a common view that the present-day distribution of temperate European trees depends on their ability to disperse. Svenning & Skov (2004), for example, have demonstrated that European tree species with present-day northerly distributions have larger ranges than species with more southerly distributions. They have attributed this ‘filling of potential niche’ to the better dispersal ability of northerly species (e.g. Abies alba, Picea abies, Taxus baccata), compared with southerly species (e.g. Carpinus betulus, Castanea sativa, Quercus pyrenaica) (Svenning & Skov, 2004). Many tree species with northerly distributions are also known to be habitat generalists, able to persist in a wide range of habitat types in temperate regions (e.g. Essl, 2005). For instance, trees belonging to families such as Pinaceae, Salicaceae, and Betulaceae are able to grow directly in moraine soon after deglaciation, and even without an accumulated soil nutrient reserve (Vetaas, 1994; Mong & Vetaas, 2006; and references therein). Furthermore, most of these trees have the ability to reproduce vegetatively under harsh environmental conditions. Under such conditions, boreal species reproduce through vegetative buds because sexual reproduction is limited or non-existent (Bonan & Shugart, 1989).

When the analysis was carried out for species that had only genetic evidence for full-glacial distribution (i.e. no fossil evidence currently exists), the pattern is less clear. For example, Populus nigra (a broad-leaved angiosperm with wind-dispersed seeds) is thought to have survived only in southerly refugia based on genetic evidence (Cottrell et al., 2005). However, given its traits the NMDS analysis would suggest that this species should have been able to persist in northerly refugia (Fig. 4, Group 1, dashed grey circle). Unfortunately, there is no fossil evidence for P. nigra because fossil pollen of Populus is usually present in very low quantities in sediment cores (Li et al., 2005) and because it is not possible to distinguish the pollen of P. nigra from that of Populus alba and Populus tremula, both of which are more widely distributed and have more northerly distributions (Bremer & Ott, 1990; Roiron et al., 2004). Other species that display patterns contrary to the NMDS analysis include Corylus avellana and Frangula alnus (Fig. 4, Group 1, solid grey circle), both large-seeded species. For both of these species the only available evidence is genetic and it suggests northerly survival (Palme & Vendramin, 2002; Hampe et al., 2003). A possible explanation for this pattern is bird-mediated seed dispersal, allowing these species to persist in refugial populations (Hampe et al., 2003). However, without fossil evidence such an explanation remains speculative. Furthermore, genetic evidence suggests northerly survival of Ilex aquifolium (Rendell & Ennos, 2003), Hedera sp. (Grivet & Petit, 2002), and Prunus spinosa (Mohanty et al., 2002) – all large-seeded, animal-dispersed species, but closer in the remaining traits to species that have the ability to persist in northerly refugia (Fig. 4, Group 1, solid grey circle).

Vertebrate species in glacial refugia

The patterns displayed by vertebrates are not as clear-cut as those displayed by woody plants, possibly because of mobility compounded by adaptability to a wider range of environmental conditions. Although fossil evidence for large-bodied mammals and birds with large home ranges, such as Aquila adalberti, Felis sylvestris, Lutra lutra, Lynx pardinus, Meles meles, Strix aluco and Sus scrofa (Pavia, 2001; Ferrer & Negro, 2004; Sommer & Benecke, 2004; Brito, 2005; Sommer & Nadachowski, 2006), suggests that they were limited to southerly refugia, many other large-bodied mammals have evidence for northerly survival, for example Alces alces, Capreolus capreolus, Castor fiber, Cervus elaphus, Gulo gulo, Lynx lynx and Rangifer tardinus (Sommer & Nadachowski, 2006), Ursus arctos (Sommer & Benecke, 2005b), and Alopex lagopus, Canis lupus and Vulpes vulpes (Sommer & Benecke, 2005a) (Fig. 7, Group 2, dashed grey circles). Alopex lagopus is a cold-tolerant species with a present-day northerly distribution, whereas C. lupus and V. vulpes are habitat generalists able to exploit a wide variety of habitats (Sommer & Benecke, 2005a). These traits may have enabled the northerly survival of these three canids. For all other large-bodied species that show evidence for northerly survival, cold tolerance appears to be the key trait. Although it has been suggested that northerly refugia were in patchy microenvironmentally favourable locations (Stewart & Lister, 2001), this result implies that for some cold-tolerant species, such as those described above, a permafrost landscape may not have been a barrier to movement. It is possible, therefore, that the northerly refugia for these species were much more continuous than suggested (see below).

The small-bodied mammals for which fossil and genetic evidence for persistence in northerly refugia exists include Cricetus cricetus (Hir, 1997; Neumann et al., 2005), Clethrionomys glareolus (Nadachowski, 1989; Deffontaine et al., 2005; Kotlik et al., 2006), Dicrostonyx torquatus (Stewart & Lister, 2001), Martes martes (Davison et al., 2001; Sommer & Nadachowski, 2006) and Microtus oeconomus (Chaline, 1987; Brunhoff et al., 2003). Fossil and genetic evidence for northerly survival exists for only one amphibian, Rana arvalis (Venczel, 1997; Babik et al., 2004). This species has a present-day northerly distribution and an ability to tolerate cooler climates.

The small-bodied vertebrates that have only genetic evidence for a southerly survival include hedgehogs Erinaceus concolor and Erinaceus europaeus (Seddon et al., 2001), a toad Bombina bombina (Hewitt, 2001), a number of bat species [Miniopterus schreibersii (Castella et al., 2001), Myotis myotis (Bilgin et al., 2006) and Nyctalus noctula (Petit et al., 1999)] as well as a mouse Apodemus flavicollis (Michaux et al., 2004), a shrew Crocidura suaveolens (Dubey et al., 2006), a chaffinch Fringilla coelebs (Griswold & Baker, 2002), a hare Lepus europaeus (Kasapidis et al., 2005) and a rabbit Oryctolagus cuniculus (Ferrer & Negro, 2004). This genetic evidence does not fit the pattern suggested by NMDS analysis (Fig. 7, Group 1, dashed grey circles) which indicates that these species have the biogeographical traits that could have enabled them to persist also in northerly refugia.

Herptiles, which are small-bodied but have a low mobility have genetic evidence to suggest that they show signs of survival only in southerly refugia (Fig. 7, Group 1, solid grey circles), for example Triturus sp. (Taberlet et al., 1998), Lissotriton boscai (Martińez-Solano et al., 2006) and Lacerta schreiberi (Paulo et al., 2001). However, the genetic evidence for Vipera aspis (Ursenbacher et al., 2006b) and Vipera berus (Ursenbacher et al., 2006a) suggests northerly persistence. These vipers are known to be cold-tolerant species usually inhabiting high-altitude areas (Ursenbacher et al., 2006a,b).

Biogeographical traits, northerly survival and post-glacial migration

Our analyses suggest that the persistence of species in northerly glacial refugia was not just a matter of chance – biogeographical traits may have played a major role in species survival. The traits important for the northerly survival of woody plant species include short generation time, small seed size, and the ability to reproduce vegetatively under harsh environmental conditions. The traits of plants that are associated with northern refugia are those one may expect to find among early colonizers in glacier forelands after glacier retreats (Matthews, 1992). For vertebrate species, short generation time, small body size and high mobility are possibly important. In addition, a number of ecological adaptations in both woody plants and vertebrates that make them habitat generalists may be important for survival in harsh climatic conditions such as in northerly glacial refugia. Present-day geographical distribution is another important attribute, which results from the overall expression of a wide range of physiological adaptations. These adaptations may indicate the likelihood of woody plant and vertebrate species having persisted in northerly refugia.

From these analyses a number of interesting points emerge. First, where the analyses are based on both fossil and genetic evidence, clear distinctions in traits emerge between those species that survived only in southerly refugia and those that also persisted farther north. One of the most important traits for both woody plants and vertebrates determining their ability to persist in northerly glacial refugia appears to be present-day distribution (resulting from the overall expression of a wide range of adaptations). Thus, those species that have present-day northerly range limits (> 60° N) appear to have been able to persist in more northerly locations during the last full-glacial. This trait results from a large number of known ecological and physiological adaptations to cold conditions, and given this result it is questionable whether the northerly species were, in the strictest sense, even in refugia (i.e. small, isolated populations). Rather, they may have been widely dispersed across the landscape in smaller populations than present or, in some cases, in larger populations. We suggest that, in the case of vertebrates, some species such as the arctic fox (Alopex lagopus) could have thrived in these northerly full-glacial conditions and sustained larger populations than seen presently. A number of other large-bodied, cold-tolerant vertebrates also suggest the possibility of a similar scenario (see above). A speculative question, therefore, is whether the populations of these vertebrates are in current ‘warm-stage’ refugia. This question has significance for the conservation of these species in an increasingly warmer climate.

A second point to emerge is that, if species that have only genetic evidence of survival in refugia are included in the analyses, often the distinctions between traits become unclear. Whereas there are a large number of advantages of using phylogeographic analyses in the determination of refugial localities, we suggest that this result highlights one of the disadvantages, namely a lack of a detailed temporal framework in which to place these phylogeographic results. We suggest that a number of the species that appear as ‘outliers’ may well be displaying phylogeographic patterns resulting from post-glacial migration and population mixing, rather than full-glacial northerly isolation.

The determination of where species survived during the last full-glacial has a number of implications for understanding the present and future distributions of flora and fauna in Europe. These include calculation of migration rates in response to climate change and a determination of regions of greatest genetic diversity of species; both are important for the long-term persistence and conservation of European populations of flora and fauna in a changing climate. Traditional estimates of post-glacial migration rates of trees usually assume migration from southerly European refugia with migration rate estimates of up to 1–2 km year−1 (Huntley & Birks, 1983). However, it is likely that species with northerly refugial populations in Europe achieved post-glacial expansion from local dispersal from isolated populations, rather than the long-distance dispersal often invoked. Thus, for these species, post-glacial migration rates are probably greatly overestimated, and the ability of the species to track future climate change is overstated (see also Svenning & Skov, 2007). A similar conclusion was reached for several North American tree species (McLachlan et al., 2005) for which genetic and fossil evidence indicated full-glacial isolation much closer to the ice-sheets than previously assumed.

This apparent ‘slowness’ in the migratory ability of woody plants (and vertebrates) could be interpreted as providing yet more depressing evidence that many European species may not be able to keep up with future climate change (e.g. Ohlemuller et al., 2006). However, as pointed out by Pearson (2006), the evidence that small isolated refugial populations across the European landscape probably provided the source material for post-glacial expansion of many populations could also be regarded as a counter-balance to the ‘overly pessimistic predictions of extinction risk from climate change’ (Pearson, 2006, p. 113). Repopulation from small low-density isolated populations is a very different scenario from the large-scale distribution shifts suggested by bioclimatic envelope modelling, and is possibly a more realistic response to climate change (Del Barrio et al., 2006; Brooker et al., 2007). In addition, the fact that species can and have persisted through rapid changes in climate in small refugial populations in both northern and southern Europe suggests that the same could also occur with future climate change – as long as potential refugial localities and populations still exist.

Conclusions

Results from this study indicate that the northerly survival of species during the full-glacial may not just have been a matter of chance but also biogeographical traits. The ability to survive in cooler climates and inhospitable habitats as well as a number of life-history traits facilitating long-distance dispersal allowed some species to persist in northerly refugia. It is also possible that some species could have been more widespread during the full-glacial and may not have been ‘isolated’ in refugia – rather, their current distribution should be considered as ‘warm-stage’ refugia. The determination of where species survived during the last full-glacial has a number of implications for understanding the present and future distributions of flora and fauna in Europe. These include calculation of migration rates in response to climate change, and a determination of regions of greatest genetic diversity of species; both are important for the long-term persistence and conservation of European populations of flora and fauna in a changing climate. Thus, identification and conservation of refugial localities in southern and northern Europe using both fossil and genetic evidence should be seen as a priority.

Acknowledgements

We thank Ailsa Allen for preparing Fig. 1. We are grateful for comments and suggestions from M. B. Araújo, K. D. Bennett, H. J. B. Birks, A. Feurdean, J. Hortal, K. Triantis, A. Tribsch, O. Vetaas, R. J. Whittaker and two anonymous referees. S.A.B.’s work is funded by NERC and the Leverhulme Trust. K.J.W.’s travel and registration fees at the third biennial meeting of the International Biogeography Society (IBS) were funded by the IBS and the Spanish Government.

Biosketches

Shonil Bhagwat is a post-doctoral researcher in the Oxford Long-Term Ecology Laboratory. His research interests focus on understanding local, regional and global-scale species distribution patterns. He is interested in applying knowledge of the past to understanding the present and to predicting future patterns of diversity.

Kathy Willis is Professor of Long-Term Ecology at the University of Oxford. Her research interests focus on modelling the long-term relationship between vegetation dynamics and environmental change, and determining the role of past events in shaping the present-day distribution of fauna and flora. Her recent research has also focused on the applied use of long-term records in restoration ecology and biodiversity conservation.

Editor: Ole Vetaas

This paper arose from a paper presented at the third biennial meeting of the International Biogeography Society, held in Puerto de la Cruz, Tenerife, Canary Islands, 9–13 January 2007.

Ancillary