A discussion of different types of glacial refugia used in mountain biogeography and phylogeography

Authors


*Rolf Holderegger, WSL Swiss Federal Research Institute, Zürcherstrasse 111, CH-8903 Birmensdorf, Switzerland. E-mail: rolf.holderegger@wsl.ch

Abstract

With the recent rise of phylogeography, the biogeography of mountain species (species with their current main distribution above timber line), especially their glacial history, has attracted renewed interest. In particular, the question of where mountain species survived the ice ages has been approached in many phylogeographical studies. The terminology of glacial refugia of mountain species is often confusing, contradictory or counter-intuitive. Our aim is to clarify and simplify this terminology. First, we offer a general definition of the term glacial refugium for mountain species. Then, we discuss three main types of glacial refugia of mountain species, i.e. nunatak, peripheral and lowland refugia. We believe that the discrimination of these three types of glacial refugia is sufficient to describe the glacial survival of (most) mountain species. Finally, we argue that the terms in situ survival and ex situ survival and the term periglacial refugium should only be used to describe specific cases of glacial history. No simple classification system can adequately describe every kind of glacial refugium, but we propose that authors should focus on providing comprehensive descriptions of particular refugial situations instead of introducing new terminology.

Introduction

At the beginning of the 20th century, the biogeography of mountain systems received much scientific attention. Of particular interest was the question of where mountain species survived the ice ages, given the fact that mountain systems were often heavily glaciated. Early biogeographers asked questions such as: Did mountain species, defined as species whose current main distribution area is located above the timber line (i.e. alpine species sensuKörner, 2002), survive in glacial refugia outside the mountains, i.e. in the adjacent lowlands? Did they survive in refugia at the periphery of mountain areas? Were species even able to survive in refugia situated within the glaciated mountains, such as on the slopes of high peaks, which were snow-free at least during summer time? Early biogeographers eagerly debated the existence of different types of glacial refugia and discussed how the location of these refugia may have influenced the current distribution patterns of mountain species as well as the centres of species diversity in mountain areas (e.g. Christ, 1879; Chodat & Pampanini, 1902; Briquet, 1906; Brockmann-Jerosch & Brockmann-Jerosch, 1926; Holdaus, 1954). Unfortunately, they also introduced a complex and often inconsistent terminology for the different types of glacial refugia of mountain species.

One hundred years later, the glacial history of mountain species has attracted renewed interest due to the advent of molecular techniques that allow the detailed investigation of the biogeographical history or phylogeography of mountain species (Avise, 2004). Molecular analyses allow explicit hypotheses on the glacial survival of mountain species to be developed and tested, as undertaken in numerous phylogeographical studies on mountain plants and animals published during the last decade (for reviews see Soltis et al., 1997; Abbott & Brochmann, 2003; Comes & Kadereit, 2003; Schönswetter et al., 2005; Schmitt, 2007). These studies indicate that mountain species often did not survive in single major glacial refugia (i.e. macrorefugia sensuRull, 2008), but in several spatially restricted and isolated glacial refugia (corresponding to microrefugia sensuRull, 2008). Despite this impressive progress, the terminology for glacial refugia of mountain species remains confusing, or may even have become more confusing. Often, different authors use the same term to describe different types of glacial refugia (Stehlik, 2000; Schönswetter et al., 2004a). For instance, the term peripheral refugium has been used to designate a glacial refugium of a mountain species at the periphery, but still within a mountain system. But it has also been applied to glacial refugia of mountain species in the lowlands outside a mountain range or in other mountain systems of lower latitudes. Another example is the use of the term periglacial nunatak (Gugerli & Holderegger, 2001), which essentially refers to a peripheral refugium.

The aim of the present editorial is to clarify and simplify the use of several terms that are applied in relation to the glacial survival of mountain species. We discuss different types of glacial refugia of mountain species and show how they can best be adapted. Our evaluation is focused on the glacial history of mountain species and is most relevant for formerly glaciated mountains systems (Lomolino et al., 2006) outside the vast Arctic ice shields (Ehlers & Gibbard, 2004). For a discussion on refugia of other organisms, especially of tree species, see Rull (2008).

Discussion of terms often used for glacial refugia of mountain species

In the following, we first give a general definition of the term glacial refugium of mountain species in formerly glaciated mountain systems. We then discuss three types of glacial refugia, namely nunataks, peripheral refugia and lowland refugia. These three refugial types are geographically defined with respect to the mountain range considered. Then, we refer to three additional terms (in situ survival and ex situ survival as well as periglacial refugia) often used to describe the glacial history of mountain species. However, we argue that these three terms should only be used for the description of particular refugial situations.

Glacial refugia

Generally, a glacial refugium describes the location where a mountain species survived the ice ages, irrespective of the geographical position or spatial extent of the location. This implies that suitable unglaciated habitat was available during at least part of the ice ages. A given location could have acted as a glacial refugium during one to several glaciation cycles. As it is difficult or even impossible to infer the time periods when refugia served the survival of mountain species from molecular data (because of the inaccuracy of molecular clocks; Pulquério & Nichols, 2006) or fossil data (because of their scarcity), the term glacial refugia is generally used with reference to the last glaciation. However, we urge scientists to explicitly state the time-scale to which they refer when interpreting their results with respect to glacial refugia.

Nunatak glacial refugia

Nunataks (Blytt, 1882; Brochmann et al., 2003; Crawford, 2008) are glacial refugia on mountain peaks that protruded above the glaciers in the core of a mountain range. A nunatak has potentially harboured spatially restricted suitable habitat patches (i.e. microrefugia; Rull, 2008) that were snow-free, at least in the summer months during glaciation (e.g. steep southerly exposed slopes; Fig. 1). For example, all high mountain peaks above the glacial ice shield of the European Alps could have acted as nunataks. In the literature, the term central nunatak is sometimes used simply to stress the fact that a given nunatak was located within the ice shield in the central parts of a mountain system. As it is often not possible to locate single nunataks in phylogeographical studies due to low sampling density or insufficient resolution of molecular markers, only larger geographical regions of nunatak glacial survival can be identified. Authors dealing with this spatial uncertainty used the term nunatak region (Stehlik et al., 2002). The literature provides several examples of nunatak glacial refugia (Muster, 2000; Stehlik et al., 2002; Bettin et al., 2007).

Figure 1.

 Part of a glaciated mountain system and three types of glacial refugia (nunatak, peripheral and lowland refugia given in red) as seen from the adjacent lowlands during glaciation. Large valley glaciers (light grey) are flowing down into the unglaciated lowlands (grey hatching), while the high mountains within the mountain range are protruding above the ice shield. At the border of the mountain system, there are locations below the permanent glacial snow-line (broken line) but above the glaciers, which could serve as peripheral glacial refugia.

Peripheral glacial refugia

Peripheral glacial refugia of mountain species are those that were situated at the border of a mountain system (Tribsch & Schönswetter, 2003; Schönswetter et al., 2005; Schmitt et al., 2006; Haubrich & Schmitt, 2007) but still within that mountain system (Fig. 1). We do not consider their position with respect to the permanent glacial snow line or in relation to the extent of the ice sheet (see below). For instance, peripheral glacial refugia were located along the border of formerly glaciated mountain systems such as the Carpathians, Pyrenees or European Alps (Schönswetter et al., 2005; Schmitt et al., 2006; Ronikier et al., 2008; Schmitt & Haubrich, 2008). Note that the above definition of peripheral glacial refugia of mountain species is distinct from the use of the term peripheral refugia as applied for lowland species. For lowland species, a peripheral refugium simply refers to the fact that the glacial refugium was at the border of a species’ present distribution area (Taberlet et al., 1998; Petit et al., 2003; Hewitt, 2004).

Some authors have discriminated several types of peripheral glacial refugia of mountain species. For instance, Schönswetter et al. (2004a) used the term peripheral nunatak for high mountain peaks that were located at the border of a mountain system but still above the glaciers. While it is evident that such peripheral nunataks have existed, we believe that the use of the term adds unnecessary complexity: for biogeographical or phylogeographical analysis, it is principally relevant whether a species survived in the centre (i.e. nunatak refugia; see above) or at the periphery of a mountain system (i.e. peripheral refugia). Intuitively, most researchers view nunatak refugia to be located well within a glaciated mountain system. The term peripheral nunatak is therefore confusing. We thus recommend discarding the use of the term peripheral nunatak.

Lowland glacial refugia

Lowland glacial refugia are those areas supporting the species in question situated outside the mountain systems and beyond the limits of the ice shields (Fig. 1). They provided suitable habitat for organisms that occurred in the adjacent mountain systems prior to the onset of glaciation. For instance, lowland refugia in continental Europe have been detected for plant species of Scandinavian mountain systems (Gabrielsen et al., 1997; Ehrich et al., 2007). Similarly, the mountain plant Oxytropis campestris, currently growing throughout the European Alps, probably survived the ice ages in refugia of the adjacent lowlands (Schönswetter et al., 2004b). Schmitt & Hewitt (2004) provide an animal example of lowland refugia for an arctic-alpine burnet moth.

Phylogeographers have also used the term periglacial to designate lowland refugia. Glaciologists define periglacial areas as being outside an ice layer, but still under its direct influence (Cox & Moore, 1993). In this sense, the term periglacial refugia would imply an area in the immediate vicinity of a glacier. It would be almost impossible to detect such strict periglacial refugia by using biogeographical or phylogeographical methods. We therefore suggest the use of the general term lowland refugia in preference to the term periglacial refugia. In doing so, we stress the location of a glacial refugium in the lowlands outside a mountain system.

In situ glacial refugia

The use of the term in situ glacial refugium or survival is confusing, since it has different meanings to different researchers. From the perspective of a mountain organism, in situ survival implies that the organism survived at a location which it already occupied before glaciation. Such a location could therefore refer to a nunatak, a peripheral refugium or even to a lowland refugium (see above). In contrast, in studies at larger geographical scales, the term in situ glacial refugium is often used from the perspective of geography. Here, in situ simply implies an organism’s glacial survival somewhere within a given mountain system, irrespective of whether it occupied the particular site before glaciation. In situ glacial survival could thus have taken place on a nunatak or in a peripheral refugium. In practice, however, the term in situ is mostly used when referring to nunatak glacial refugia within a mountain system (Stehlik, 2003).

We argue that the use of the term in situ glacial refugium is often unnecessary. We thus propose to use it only when referring to a specific, deviating case. For instance, the arctic-alpine plant Arabis alpina survived, apart from glacial refugia within the European Alps, in lowland glacial refugia located between the ice shields of the European Alps and the Scandinavian glaciers (Ehrich et al., 2007). The sites of these lowland glacial refugia had already been occupied by A. alpina before the last glaciation. In this particular case, they thus acted as in situ lowland refugia of an alpine plant.

Ex situ glacial refugia

From the perspective of a mountain organism an ex situ glacial refugium refers to glacial survival at a location that the organism did not inhabit before glaciation. For many mountain species this would have been a peripheral refugium to which they migrated from the core of a mountain system at the beginning of glaciation. In contrast, from the perspective of geography, an ex situ glacial refugium implies glacial survival outside the focal mountain system, e.g. in lowland refugia. In both cases, the term ex situ implies emigration out of the former distribution range of a mountain organism into peripheral or lowland areas. While such emigration events certainly took place in mountain animals (Haubrich & Schmitt, 2007), the relevance of emigration for mountain plants is still debated. In practice, for mountain species the term ex situ is mostly used for lowland glacial refugia that are thought not to have been inhabited before glaciation.

Example

Consider a high mountain just at the very border of a larger mountain system. The mountain system was heavily glaciated during the last glaciation. Several large valley glaciers passed our border mountain and flowed out into the adjacent lowlands. However, the peak of the mountain rose above these glaciers. While the mountain’s summit was covered by permanent snow, its slopes were partly snow- and ice-free, at least during the summer months. Imagine that a mountain species A was growing on the slopes of this mountain before the ice ages and also survived glaciation there. For this species A, the mountain acted as a peripheral glacial refugium. Now imagine that a mountain species B was not growing on our mountain before glaciation, but migrated to it at the beginning of glaciation and survived the ice ages there. For this species B, the mountain equally acted as a peripheral glacial refugium (as it did for species A). The difference is that, from the species perspective, our mountain acted as an in situ glacial refugium for species A but as an ex situ glacial refugium for species B. In contrast, the mountain formed an in situ glacial refugium for both species when seen from the geographical point of view, as both species survived within the mountain system (see above). This example illustrates the ambiguity of the terms in situ and ex situ. We argue that, in reality, it would be impossible to discriminate between an in situ and an ex situ peripheral glacial refugium using the currently available biogeographical and phylogeographical methods (unless high-resolution fossil evidence for the species occurrence at the very location happened to be available). Therefore, not much is gained by the use of the terms in situ and ex situ refugia when referring to peripheral as well as to nunatak glacial refugia.

Concluding remarks

We suggest that only three types of glacial refugia, namely nunatak, peripheral and lowland refugia, are sufficient to describe the glacial survival of most mountain species, both with respect to the genetic structure of populations as well as to floristic and faunistic patterns. The discussion given above highlights these three types of glacial refugia and hopefully helps to clarify findings in the biogeography and phylogeography of mountain organisms. It is clear that such a simple classification system cannot cover all possible cases of glacial refugia. However, when a particular case does not fit one of the above three types of glacial refugia for mountain species, we would prefer that authors describe the particular refugial situation in explicit and comprehensible words than that they introduce new and potentially confusing terminology.

Acknowledgements

We thank all our colleagues working on the phylogeography of mountain species for many stimulating discussions and Thomas Schmitt, Ivana Stehlik, Robert Whittaker and an anonymous referee for helpful comments on the manuscript. We are also grateful to Valentí Rull for sharing his ideas with us.

Biosketches

Rolf Holderegger has research interests in conservation and landscape genetics, phylogeography and adaptive genetic variation in a wide variety of organisms.

Conny Thiel-Egenter studies patterns of genetic and species diversity in mountain systems. She is particularly interested in the comparative phylogeography of alpine plants.

Editor: Robert Whittaker

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