Climate Change Impacts in Alpine Environments

Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x

Climate Change Impacts in Alpine Environments Georg Grabherr1*, Michael Gottfried1 and Harald Pauli2 1Department of Conservation Biology, Vegetation and Landscape Ecology, University of Vienna, Vienna, Austria 2Institute of Mountain Research: Man and Environment, Austrian Academy of Sciences, Vienna, Austria

Abstract Alpine ecosystems (alpine tundra) occur at a range of air density, water availability and seasonality worldwide on the treeless high terrain of mountains. They vary along geographic scales: boreal dwarf-shrub heaths, temperate sedge heaths, subtropical dwarf shrubs and tussock grasslands, and tropical giant forblands. Along local topographic gradients plant cover changes from windswept dwarf-shrub heath, to dense grass-sedge heath, to snowbank vegetation. These cold and relatively little exploited alpine ecosystems, nonetheless, are among those where climate warming impacts are forecast to be pronounced and detectable early on. We ﬁrst review alpine life conditions and organism traits as a background to understanding climate impact related processes. Next, we provide an account of how alpine ﬂora and vegetation have been impacted by recently observed climate change. Finally, a global network for long-term monitoring of climate-induced changes of vegetation and biodiversity in alpine environments is described.

Alpine Environments – Deﬁnition, Distribution, Elevation, Zonation Alpine environments (Figure 1), occur in a low temperature climate where growing season means in general do not exceed 6–8 C; this temperature limit marks the lower distribution limit of the alpine zone worldwide (Ko¨rner and Paulsen 2004). However, there is a large variability with respect to altitude (air density), water availability, and seasonality across the globe (Figure 2). Accordingly, alpine is a rather broad term that encompasses a number of designations biogeographers have proposed (Nagy and Grabherr 2009, Table 1.1). Nonetheless ‘alpine’ is commonly used in a broad sense for the treeless areas above a low-temperature determined treeline in the high reaches of mountains (Grabherr et al. 2003; Ko¨rner 1995, 2003; Nagy and Grabherr 2009; Wielgolaski 1997). This area can be divided into at least two zones: alpine sensu stricto and nival. The alpine zone (or alpine tundra) may extend over an elevation interval of 1000 m (Grabherr et al. 1995) where species-rich closed plant communities dominate the landscape (e.g. heath, fell-ﬁelds, grasslands, pa´ramo, puna; Figure 3). These zonal communities form a landscape matrix (Figure 5a) that might be interspersed to varying degrees with specialist habitats, such as rock faces, screes, glaciers, snowbeds, and marshes. At the upper limit of the alpine zone, vegetation becomes open (Figure 4a); nonetheless many plant and animal species live in favourable niches at higher altitudes. It is the so-called nival zone (Fig- ure 4), expanding another c. 1000 m of elevation to the limit of higher plant life. The highest growing vascular plants have been found above 6000 m in the Himalayas (Miehe 1997, 2004; Webster 1961), and lichens at 7400 m (Miehe 2004). Bryophyte-dominated ecosystems around steam vents near the top of Volcan Socompa (6060 m) in the Andes

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Fig. 1. Piz Linard (3411 m), Switzerland, shows impressively the elevational zonation of a mountain, where the zone beyond the treeline is considered as ‘‘alpine’’ throughout the globe. Major subdivisions are alpine sensu stricto for the vegetated but treeless zone, nival for the region of rock, scree and snow that still hosts vascular plants, and aeolian above where only a few organisms of microbes, lichens, or arthropods exist (not occurring at Piz Linard with thirteen vascular plant species at the very top).

Fig. 2. The main environmental factors that differentiate mountains in an ecological perspective. Examples are: Ruwenzoris (aseasonal wet tropics), Cordillera Blanca (seasonal tropical), Tibesti (dry subtropical), Alborz (Mediterra- nean), Hohe Tauern (Alps; temperate), Franz Joseph Land (polar region). (modiﬁed after Nagy and Grabherr 2009). represent an extreme outpost for a complex biotic community (Halloy 1991), in an otherwise bare desert environment. Thirty-six taxa of mosses and lichens, some insects, a small rodent (Phyllotis darwinii rupestris) and a bird (Sicalis olivaceus) form isolated ‘islands of

ª 2010 The Authors Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x Journal Compilation ª 2010 Blackwell Publishing Ltd Climate change impacts in alpine environments 1135

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Fig. 3. The main zonal alpine biota worldwide: (a) Giant rosette formation (pa´ ramo, giant forb lands) of tropical humid mountains (Lobelia rhynchopetala; Bale Mts., Ethiopia). (b) Tussock grasslands of the seasonal tropical puna region (Cordillera Blanca, Peru). (c) Spiny cushion formation of Mediterranean mountains (Alyssum spinosum; Atlas, Morocco). (d) Northern hemisphere mountain grasslands (Kobresia ⁄ Carex community; alpine tundra, alpine steppe; Tienshan, Kyrgyzstan).

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Fig. 4. Nival biota and their plant life forms: (a) Assemblage of nival plants from the Austrian Alps (3100 m). (b) Cushion, a ‘‘heat collecting’’ growth form (Androsace alpina, Austrian Alps). (c) Mesophytic forb Ranunculus glacialis can survive 33 months under snow (Austrian Alps). (d) Grass Poa ruwenzorensis stays frozen every night (5100 m, Ruwenzori, Uganda).

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Fig. 5. Typical alpine landscape of the Central Alps and life strategy of the dominant Carex curvula: (a) The ele- ments of alpine environments sensu stricto: zonal grassland, glacier foreﬁelds, rocks, snowbeds; note that leaf tips are withering which is obligatory in this species. A leaf grows for about 3 years from the base and withers from the end. (b) Individual of Carex curvula, about 30-years-old. (c) Fairy ring of a 60-year-old individual. (d) Clonal population of Carex curvula in late successional state. The chaotic pattern suggests that the ramets belong to a few genets germinated some hundreds years ago if not more. A fairy ring of about 40 years is visible as a computer simulation suggests (right above). Circles: tillers with leafs; Dots: without leafs (modiﬁed after Grabherr 1997). life in the sky’ (Halloy 1991). In temperate mountains such as the Alps, or the Rocky Mountains, the limit of higher plant life lies at around 3000–4000 m; in boreal and arctic mountains it drops below 2000 m, and to 1000 m, respectively. Above lies the aeolian zone with barren rocks, debris, ice and snow. Small animals and microbes characterize the aeolian zone (Swan 1992) where organic material (detritus, wind-blown organisms originating from lower altitudes), deposited by wind, provides most of the food for scav- enging and predatory animals.

Variability of Alpine Environments Altitude (air density), water availability, and seasonality (Figure 2) are speciﬁc to each mountain region. These factors determine, besides the available ﬂora and fauna, the altitudinal zonation, the structure and functioning of the ecosystems. No two mountain systems are identical.

EFFECTS RELATED TO CHANGING ELEVATION (TEMPERATURE, AIR DENSITY DECREASE) Mountains with an alpine zone occur at all latitudes, from the wet tropics to the polar regions (Figures 3 and 12). Apart from a steady decrease of temperature with increasing elevation at an average rate of 0.60 C⁄100 m (Nagy and Grabherr 2009, p. 23), air pressure also decreases. The latter becomes particularly relevant in mountains such as the Himalayas where the highest peaks reach beyond 8000 m. Low oxygen might be one of the causes for the absence of many animal groups from the high grounds or their generally low diversity

ª 2010 The Authors Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x Journal Compilation ª 2010 Blackwell Publishing Ltd Climate change impacts in alpine environments 1137 compared to the lowlands (Nagy and Grabherr 2009, p. 59). Contrarily, low carbon dioxide pressure seems to have no limiting effect on plants; other factors such as low temperatures set the limits (Ko¨rner 2003.)

EFFECTS RELATED TO SEASONALITY The macroclimate of the life zone to which a mountain region belongs to determines the climatic conditions in its alpine zone, e.g. the aseasonal climate regime of the wet tropics is also evident at high altitudes. Plants are permanently in an active state in the tropics, such as the Lobelia spp. and Dendrosenecio spp. in Africa, and the Espeletia spp. in tropical South America (Beck et al. 1982; Squeo et al. 1991; Figure 3a), whereas alpine and nival plants (Figures 4 and 5) under seasonal climates undergo winter dormancy and survive long winters under snow protection, or are frost resistant. Plants such as Saxifraga oppositifolia or Silene acaulis can tolerate extreme temperatures in winter (e.g. both species survived immersion into liquid nitrogen at )196 C; Kainmu¨ller 1975). Species that are sensitive to frost require permanent snow protection, and as a result, have developed a remarkable snow tolerance. For example the nival zone Ranunculus glacialis (Figure 4c) in the Alps is known to be able to survive up to 33 months permanently under snow (Moser et al. 1977). Animals on the high grounds may overwinter either by hibernating (e.g. Marmota spp.), or they may stay active under deep snow cover (e.g. Thomomys spp., Ochotona spp.). Some alpine animal traits, especially of insects, such as reduced body size, melanism, increased pubescence, prolonged life cycle, thermoregulation, or freezing tolerance may be related to adaptation to low temperatures (Sømme 1997).

Life Forms, Life Cycles The diversity of alpine climates might be one reason that no speciﬁc single alpine life strategy exists (Ko¨rner 1995). Alpine and nival plant communities are composed of a vari- ety of life forms (Figures 3–5; Halloy and Mark 1996; Ko¨rner 1995, 2002). One of the few common characters alpine plants share is longevity. Annuals are nearly absent from all alpine environments, even short-lived species are of minor importance. Most species are long-lived. Individuals of the cushion plant Silene acaulis were calculated to be older than 300 years (Morris and Doak 1998). Tropical giant rosettes can grow over 100 years (Rundel and Witter 1994; Young 1994). Graminoids, in particular, form ‘eternal’ clonal populations (>1000 years), for example, Carex curvula, a sedge, which dominates the zonal grasslands in the Central Alps (Figure 5; Grabherr 1997; Grabherr et al. 1978; Steinger et al. 1996). In contrast, the life span of alpine animals is much shorter (Molau 2003). For example, the European Ibex (Capra ibex), considered long-lived, reaches just over 20 years as the maximum.

Ecotones The major ecotones on mountains indicate the transition between the different biocli- matic zones along elevation. They extend for about 200–300 m altitude, and are obvious landmarks in many mountain landscapes. Ecotones are the places where species turnover (=beta diversity) is highest, and therefore, climate change effects on species composition, on population size and structure, become detectable most apparently.

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THE TREELINE ECOTONE The treeline ecotone (or timberline ecotone), which demarcates the lower end of the alpine zone (Holtmeier 2009) is the visually most conspicuous ecotone. It spans from the limit of closed forest (timber or forest line) up to the tree species line at the uppermost outposts of adult trees often forming krummholz or wind-shaped dwarf shrubs (Butler et al. 2009; Holtmeier 2009; Holtmeier and Broll 2005); not so in the tropics where krummholz-forming processes such as seasonal strong winds and snow blast are largely absent (Troll 1961). In the tropics and also in subtropical and Mediterranean type mountains, ﬁre might also play an important role in shaping the treeline ecotone (Bader et al. 2007). The causal mechanisms acting at the treeline ecotone may differ in the various mountain regions. Ko¨rner (1998, 2008) postulated a sink dependent effect, i.e. that the cool soil temperatures set the limit for tissue forming processes (Grace et al. 2002). This was backed up by evidence from soil temperature measurements at treeline sites across the world (Ko¨rner and Paulsen 2004) as well as from a local permafrost site in the montane forest zone in the Swiss Jura Mountains (Ko¨rner and Hoch 2006). Conversely, Malanson et al. (2009) considered the vegetation pattern within the treeline ecotone as driven by complex processes where the successful growth of a seedling into a sapling might be the bottleneck. For this process photosynthetic gain is essential, implying that treeline advances might be source limited. For example, clusters of krummholz provide safe sites for establishment and growth, creating a positive feedback whereas the sink hypothesis postulates a negative feedback as the shadow of established trees lowers soil temperatures. In mountains of deserts or subtropical dry regions forests can only grow where condensa- tion clouds at middle elevations provide some precipitation in the form of rain or fog. Higher up, increasing dryness, not low temperature, sets the limit. Studying water relations at the dry Pinus canariensis treeline at Mt. Teide (Canary Islands), Gieger and Leus- chner (2004) concluded that drought would not affect mature trees but that there are ‘multiple limitations at the seedling stage’. Tree species identity is also of great importance. For example, on Haleakala, Hawai’i subalpine native shrublands form a kind of treeline ecotone. At the same altitude the alien Eucalyptus globulus planted 100 years ago can grow to trees (Hosmer Grove, 2850 m; Medeiros et al. 1998).

THE ALPINE–NIVAL ECOTONE Compared with the treeline ecotone, physiognomically less visible is the change from closed alpine zonal vegetation to the open rock- and scree-ﬁelds of the nival zone (Figure 6), which is commonly set at the permanent snow line. Such a hypothetical line is rather intricate as outpost patches of alpine vegetation fragments can be found in shel- tered and sunny places far above. For example, giant rosettes covered with snow are found at 4600 m near to the tropical Ruwenzori-glaciers.

LIMITS TO PLANT LIFE Outposts of vascular plants have been recorded from extreme altitudes. At such low-temperature limits of higher plant life snow protection during cold spells in summer plays a crucial role for survival, as few plants are able to tolerate frosts below )5to)8 C during the growing season (Larcher et al. 2010; Taschler and Neuner 2004). In New Zealand and the Andes of central Chile plants exhibit a higher tolerance, i.e. <)8 Cto)19 C

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Fig. 6. Mt. Schrankogel (3497 m) in the Tyrolean Alps shows all the components of a nival landscape: glacier and periglacial morphologies such as side morains; scree ﬁelds and wide expanses of rock; then grassland fragments up to middle elevations represent the alpine–nival ecotone. Above follows the nival zone where still about six to ten vascular plant species are found in the summit area of Schrankogel. Nival plants plus ⁄ minus restricted to this zone are Androsace alpina, Poa laxa, and Ranunculus glacialis; Cerastium uniﬂorum, Saxifraga bryoides, and Saxifraga oppositifolia have their centre of distribution at the alpine–nival ecotone. If conditions allow, e.g. in cold air drain- age sites, they can occur also at somewhat lower elevations.

(Bannister et al. 2005; Sierra-Almeida et al. 2009) which accords with that for tropical species (Beck 1994). Early season might be the most sensitive period as ﬂowers can be killed during clear frosty nights (Inouye 2008). Although nival species beneﬁt from and tolerate snow cover (Figures 7 and 8; Gottfried et al. 2002) even in mid summer, they require a mild late summer season for fruit setting and ripening; this however may be interrupted by early snow fall (Ladinig and Wagner 2007, 2009). Frost and the shortness of the vegetation period set the distribution limits of many alpine species at the alpine–nival ecotone and of nival specialists at their upper range margins. Both source and sink phe- nomena are important constraints: late snow cover reduces light for photosynthesis and therefore the photosynthetic gain, while soils are cold and often frozen (Moser 1973), which reduces tissue forming processes independently of photosynthetic resources (Ko¨rner 2008).

Alpine Biota as Indicators of Climate Change

A HISTORICAL PERSPECTIVE Alpine biota have evolved under long-term climate change. During the Pleistocene most of today’s alpine areas were covered by a continuous ice sheet interspersed with so-called nunataks, i.e. ice free outcrops. Many species of the pre-Pleistocene or interglacial mountain ﬂoras and faunas survived at such nunataks or at the fringe of the mountain systems; these sites later acted as source areas for reinvasion (Harris 2007; Scho¨nswetter et al.

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Fig. 7. Projection of warming effects on the distribution of suitable sites for the nival plant Androsace alpina based on a spatial explicit model: (a) Digital Elevation Model of Mt. Schrankogel (resolution 1 m2). (b) Setting of 1 m2 permanent plots in transects (see yellow markings in (a) for deriving environmental envelopes (microtopography, soil temperatures, snow duration) for representative alpine and nival species. (c) Warming scenarios for Androsace alpina. Note that even under a +5 K scenario some refugia remain (red spots in the upper part).

Fig. 8. Realized niches for snow cover and temperature of alpine and nival species at Mt. Schrankogel ⁄ Tyrol; nival species occupy colder habitats with extended snow lie. Warming in combination with less snow might be the most effective driver for change; y-axis: probability of a species’ presence (p); x-axis: nighttime temperatures ⁄ snowcover length of June–July (Gottfried et al. 2002).

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2005). Some taxa persisted in their refugia and did not expand. Many such true relict species are restricted to azonal habitats, such as rock faces; others have been constrained by the lack of efﬁcient means of migration. In contrast to tree distributions and migration during and after the Ice Age, little is known about how alpine or nival plants reoccupied the extensive areas left free by the melting ice sheets, and how today’s communities established. Pollen records from the Swiss Alps suggested a steady increase in plant diversity in the Lateglacial that levelled out at 8000 years before present (Ammann 1995). Alpine vegetation might not have changed since, as evidenced from the highest peat bog in the Eastern Alps (Rofenberg, 2760 m; Bortenschlager 1993). In the Scandes, however, alpine heath appears to have expanded during the warm period from 7000 to 4000 years before present (BP) then contracted under a moister and cooler climate after 4000 years BP (Seppa¨ et al. 2002).

EXPLORING POTENTIAL EFFECTS How patterns of vegetation and species distributions in an alpine–nival environment might change under climate warming has been presented by a high resolution spatial explicit model for a temperate mountain, Mt. Schrankogel, Tyrol, Austria, based on temperature data for different microhabitats (Gottfried et al. 1998, 1999). According to this model, suitable habitats for the nival flora decrease under warming, dramatically, if temperatures increase in excess of 3 C (Figure 7). However some locations may remain with conditions where nival plants grow today even under a +5 C warming scenario. The importance of micro-refugia was also suggested recently by a fine-scaled modelling approach in the Alps of Valais, Switzerland (Randin et al. 2009). For the same region the role of dispersal for plant distribution was explored by Engler et al. (2009). Based on estimates of realistic dispersal distances of 287 mountain plants, model scenarios showed closer similarities of the realistic approach to the assumed unlimited dispersal than to no dispersal. In fact, overall biodiversity, vascular plant diversity in particular, will increase at high altitudes if climate becomes warmer. Less snow in combination with warming are the most effective drivers of change (Figure 8). The floras (and faunas) adapted to the uppermost reaches will lose most of their habitats. Alpine plants – not unlike others – may react rather individualistically to climate change as has been shown for a snowbed flora in the Alps (Scho¨b et al. 2009), and as experimentally documented for meadow plants, dwarf shrubs, and pioneers at glacier forefields (Erschbamer 2007; Kudernatsch et al. 2008; Kudo and Suzuki 2003; Lambrecht et al. 2006; Wada et al. 2002). Species may not change and not move in association with each other as whole communities. Some growth forms may act as nurse for others such as documented for cushion plants in the Andes of Central Chile (Cavieres et al. 2002, 2005), or the boreal Scandes (Antonsson et al. 2009). Structural matrix-forming species determine the character of some complex plant communities, e.g. Carex curvula communities of the Alps (Figure 5; Grabherr 1989, 1997). This sedge contributes most of the vascular plant biomass (>50%), other species such as Veronica bellidioides or Phytheuma hemisphaericum much less. Carex curvula forms a dense root mass (ratio of above- to below-ground biomass = 1:18; Ma¨hr and Grabherr 1983); the density of individuals, therefore, is determined by intraspecific competition (Grabherr 1989). The associated species are restricted to a few gap sites. As the Carex forms clonal populations, sometimes several thousands of years old (Grabherr 1997; Steinger et al. 1996), it may take a long time for a mature community to form. On the moraines of the Little Ice Age – the oldest

ª 2010 The Authors Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x Journal Compilation ª 2010 Blackwell Publishing Ltd 1142 Climate change impacts in alpine environments being from about 1600 – no mature Carex curvula community can be found and the many succession studies on glacier foreﬁelds which are limited to a period of <400 years only provide a partial picture of the successional sequence. A plant community such as the sedge heaths of the Alps may also be rather resistant to invaders, including shrubs. Dullinger et al. (2004), for example, showed this for subalpine prostrate pine (Pinus mugo) establishment. Their modelling study has indicated that in late successional communities clear signals (e.g. change in species composition) of climate change effects might be detectable only in the very long-term. Projected shifts of the zonal biota as a unity – as some conceptual models predict (e.g. Halpin 1995; Loarie et al. 2009; Ozenda and Borel 1990) – must therefore be viewed with scepticism. Slow vegetation change was also documented from the southern hemisphere by a unique 50-year-old permanent plot study in New Zealand alpine cushion⁄ tussock communities (Mark and Wilson 2005). In conclusion, for observing climate induced changes a ﬁne scale approach concentrating on ecotones, i.e. the treeline, the alpine–nival ecotone or the upper limits of vascular plants might be better suited than studies of zonal alpine biota (Pauli et al. 2004). In densely populated mountain regions, however, recent and ⁄or historical impacts need careful interpretation (Vittoz et al. 2009), at treelines in particular (Nagy 2006).

Observed Impacts Mean annual surface temperatures have increased by about 0.74 C over the past 100 years on a global average with an increasing rate of warming over the last 25 years (Solomon et al. 2007). Eleven of the twelve warmest years on record have occurred in the past 12 years (Solomon et al. 2007) and were most probably not exceeded during the past millennium. Winters are milder today, hot summers more frequent than before. How have alpine biota reacted to this warming? Ecologists and biogeographers are in an unfortunate situation as long-term series of reliable observations, such those for weather data since the 1850s are not available. The few cases, however, where photo- graphic evidence, old records of vegetation patterns or species composition in permanently marked plots are available, all imply a change, correlating with the observed warming.

CHANGES AT TREELINES Convincing examples that climate change has affected treeline ecotones have been provided by comparing dated historic photographs with recent ones. In the Southern and Northern Urals the treeline ecotone has become more densely wooded (Figure 9) during the past century by enhanced recruitment and growth of the treeline trees (Picea abies ssp. obovata, Betula pubescens ssp. tortuosa) (Moiseev and Shiyatov 2003). In the Southern Urals winters have become warmer by about 3 C, summers by about 0.6 C. In the Glacier National Park, Montana, USA, the same process was evident from the analysis of sequential air photography, spanning a time interval of 46 years (Fagre 2009; Klasner and Fagre 2002; see also Butler et al. 1994). Malanson et al. (2007), summarising the results of their detailed research of the treeline ecotone in the Glacial National Park, concluded that change at treelines is a rather complex phenomenon. The reaction to climate depends on local habitat conditions, in particular on the interplay between temperature and precipitation.

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Fig. 9. Examples of evidences that treeline ecotones have been affected by climate warming during the past century: (a) Iremel Mts. in the southern Urals, Russia, in the early 20th century. (b) Filling of the treeline ecotone and upward movement of tree species in the late 20th century (with permission from Pavel Moiseev and Stepan Shiyatov; Ekaterinburg, Russia); Note that this area has never been grazed by domestic animals; the horses are expedition horses.

There is a long series of direct observations on treelines in the Swedish mountains (Kullman 2001, 2004, 2007). Betula pubescens and other trees (Picea abies, Pinus sylvestris, Sorbus aucuparia, Salix spp.) have advanced since the early 1950s. Saplings of the decidu- ous Ulmus glabra, Quercus robur, Acer platanoides, Alnus glutinosa, Betula pendula have been found 500–800 m altitude higher at sites from where they have been absent for more than 8000 years, since the Holocene optimum (Kullman 2008). At the study site of Syrl- ana, Sweden, 29 vascular plant species showed increases in their altitude distribution limits by an average of 165 ± 20 m over the past 50 years. However, local factors such as wind can locally limit upward establishment as was shown for Betula pubescens. Detailed population studies on Pinus sylvestris for the period 1973–2005 indicated that population size increased which could be related to lowered mortality rates. Filling of treeline ecotones and moving of treelines has also been reported from the Alps and the Western Scandes which was mainly linked to reinvasion of formerly cleared forests (Byrne 2008; Gehrig- Fasel et al. 2007; Ro¨ssler et al. 2008). Gehrig-Fasel et al. (2007), analysing Swiss land use statistics, found that only 4% of the altitude increases could be interpreted with certainty as an effect of climate change when upward advances of trees across the potential treeline was taken as proof. Ro¨ssler et al. (2008) related all of the changes observed at treeline

ª 2010 The Authors Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x Journal Compilation ª 2010 Blackwell Publishing Ltd 1144 Climate change impacts in alpine environments sites in middle Norway to reinvasion of abandoned land. At this site on the oceanic slope of the Scandes no upward movement was detected and only winter temperatures and moisture have increased.

CHANGES IN ALPINE PLANT COMMUNITIES For alpine plant communities such as alpine grasslands, dwarf shrub heath, pa´ramo, or puna large scale photography is insensitive to detect changes from one type of non- woody vegetation to another. Observations based on permanent plots are rare. Dwarf- shrub cover has been observed to has increased at the upper end of a mountain transect in Northern Sweden during the past 20 years (temperature increase: 2 C) but no species was detected to move up the gradient (Wilson and Nilsson 2009). Best evidence for changes comes from snowbed studies. Virtanen et al. (2003) compared plots of seven alpine sites in Finland and central Norway. All studied communities (different dwarf- shrub heath, snowbeds, alpine mires) showed a decrease in lichens and mosses, in number of species as well as in cover in the 1990s in comparison with that documented in the 1920s. In snowbeds, characteristic species declined and grasses increased. The authors related the decrease in cryptogams to the increasing numbers of reindeer that feed on them. The decline of snowbed species, however, can also be interpreted as an effect of snow cover change during the warm 1990s. Grasses advancing into snowbeds were also reported from alpine grass heath, where the age structure of the populations of the grass Nardus stricta in Salix herbacea snowbeds showed a clear bias towards young individuals (Grabherr 2003). In the Taisetsusan Mountains (Hokkaido, Japan) the dwarf bamboo Sasa kurilensis advanced into snowbeds during the past 20 years (G. Kudo, pers. comm.). Closed vegetation types from the alpine zone have, so far, been considered as rather resistant to climate change; based on the argument that particularly the dominant species are long-lived and allow only few gaps for establishing new species (Grabherr 2003; Ko¨rner 2003). Recent studies from Scotland (Britton et al. 2009) and Switzerland (Vittoz et al. 2009), however, suggest that climate change is going to alter also closed grassland and dwarf shrub communities. At both study regions alpine species declined during the past 20–50 years, whereas lowland generalists increased. Though the changes observed were signiﬁcant, the typical vegetation structure and composition of species has been maintained. Both studies, however, are somewhat special cases. The Swiss sites are former pasture land at potentially forest land, and most of the changes relate to secondary succession. In Scotland, alpine communities are not as rich in species as those, e.g. from the Alps (Grabherr et al. 1995), and factors such as airborne nitrogen might have been effective as the decrease of lichens indicated.

CHANGE AT THE ALPINE–NIVAL ECOTONE AND IN THE NIVAL ZONE UP TO THE LIMITS OF PLANT LIFE As a result of warming the uppermost outposts of vascular plants should retreat to elevations higher than those pre-warming. For example, the highest record of a vascular plant in the Alps had been held for a long time by Ranunculus glacialis at 4270 m at Mt. Fins- teraarhorn, Switzerland until an individual of Saxifraga biflora was reported from Mt. Dom de Mischabel, Switzerland at 4450 m (Anchisi 1986). However, as there is no systematic search behind the above figures they might be regarded as incidental. Upward range expansion of alpine plants, leading to the enrichment of summit floras as a consequence of warming was already recognised by Klebelsberg (1913) in the Austrian Alps. Braun- Blanquet (1955, 1957, 1958) provided some proofs from the Central Swiss Alps in the

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1950s. Later, evidence for an increase in species richness on high alpine summits was reported by Grabherr et al. (1994), who compared botanical records for 25 high summits (>2900 m) in the Swiss, Austrian and Italian Alps. These summits have reliable early records, the earliest from 1835. Species richness increased on eighteen summits between observations, as opposed to seven summits with no increase or a small decrease. The highest numbers in increase (e.g. Piz dals Lejs from eleven species in 1907 to 34 in 1992) were found on rocky summits where ridges offer stable pathways for a propagule trans- port. On that ridges, crevices, filled with debris and soil substrate, provide safe sites for germination and plant establishment. Piz Linard (3411 m), the summit with the oldest record, showed no increase in species richness since 1947, however, populations of the plant species present in 1947 have increased significantly (Pauli et al. 2003). Piz Linard and other summits with small increases mostly consisted of unstable and erosion prone slopes where establishment is difficult, or of block fields which present a barrier to migration. Microtopography plays a crucial role for migration and establishment in these extreme environments. Increase in species richness in high alpine areas was also reported from other sites in the Alps (Bahn and Ko¨rner 2003; Erschbamer et al. 2009; Hofer 1992; Holzinger et al. 2008; Vittoz et al. 2008) and the Scandes (Klanderud and Birks 2003). Walther et al. (2005) found an accelerated increase of species richness between 1985 and 2003. How- ever, population structure might remain rather stable in some nival plants (Diemer 2002). Changes in the species composition of zonal alpine ecosystems are influenced by biotic interactions between plants, wildlife and domestic animals and microbes (Bowman and Seastedt 2001; Diemer 1996; Ko¨rner 2003; Nagy and Grabherr 2009). Plant communities differ in their resistance to invasion (Dullinger et al. 2003). In very high altitudes facilitation might be important (Callaway et al. 2002). Dullinger et al. (2007) studied small- scaled species associations using a large Europe-wide data set, and found no clear evidence of increasing facilitation along elevation. Klanderud (2004) found that experimental removal of the dwarf-shrub Dryas octopetala had significant positive effects on associated species at Finse, Norway, indicating competition in northern alpine Dryas heath. Changes of abiotic conditions may affect the lower distribution of nival plants directly. A detailed permanent plot study at Mt. Schrankogel, Tyrolean Alps, Austria showed that nival species declined between 1994 and 2004 which was mainly an effect of changing abiotic conditions related to the observed warming (Figure 10; Pauli et al. 2007). The decrease in nival species cover indicates a higher mortality rate and⁄ or a less vigorous growth. Higher mortality could result from more frequent exposure to lethal frosts when the protective snowcover declines in the course of warming. Moreover, alpine species that benefit from an elongated growing season could outcompete nival species where plant cover becomes high.

Long-term Study Initiatives It appears certain that alpine vegetation has been affected by climate change observed in the twentieth century. Experimental exposure to climatic conditions such as those pre- dicted by climate change scenarios support this assumption (Erschbamer 2007; Kudernatsch et al. 2008; Kudo and Suzuki 2003; Lambrecht et al. 2006; Wada et al. 2002). Alpine biodiversity appears to decline under ongoing climate change, at least locally. However, most of the evidence is pieced together from studies that used method- ologies not based on direct observation. Airborne surveillance does not provide the resolution needed for meaningful data on alpine plant communities, in particular in relation

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(a) (b)

Fig. 10. Changes of alpine and nival species between 1994 and 2004 at Mt. Schrankogel, Tyrol. (a) (left): the nival species Cerastium uniﬂorum in 1994 (mid) and 2004 (bottom) showed a drastic decline; (b) (right): the alpine species Silene exscapa in 1994 (mid) and 2004 (bottom) was increasing in cover. to biodiversity loss. Only ﬁeld studies can provide a clear picture of just how endangered or not alpine biodiversity might be. The above facts and considerations were a stimulus and the motivation for establishing the worldwide research initiative Global Observation Research Initiative in Alpine Environments (GLORIA, http://www.gloria.ac.at). GLORIA aims at providing long-term observation series on the state of alpine biota (Pauli et al. 2004, 2009). The basic approach is the surveillance of plant assemblages along summits of four different elevations, representative of a particular mountain region. The

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Fig. 11. The GLORIA programme (Global Observation Research Initiative in Alpine Environments) aims to establish and to maintain a worldwide monitoring network for detecting climate change effects on alpine biodiversity. On each study site (target region), four summit areas are selected for long-term observation of alpine vegetation. The elevation gradient is given by the summits of different altitudes which should, ideally, be positioned in one of the ecotones. For details see Pauli et al. (2004); http://www.gloria.ac.at. summits are selected at ecotones established along an elevation gradient: a treeline summit, a summit at the transition from low to high alpine, one reaching to the alpine– nival ecotone, and one to the uppermost limits of plant life (Figure 11). Temperature loggers are planted in the soil to obtain a time series of temperatures. Snow cover duration can be derived from these measurements. The design of this so-called Multi-Summit Approach is simple and cheap. Establishing permanent observation plots should be possible under expedition conditions on a low budget. An established site is readily

Fig. 12. The GLORIA network; distribution of study sites (target regions) in 2009.

ª 2010 The Authors Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x Journal Compilation ª 2010 Blackwell Publishing Ltd 1148 Climate change impacts in alpine environments rerecorded. Since alpine and nival plants are persistent and long-lived the intervals of resurveys can be as long as 5–10 years; shorter intervals might disturb the vegetation by trampling. This basic general approach that provides sound knowledge about climate change effects in the long term may be developed further to equip sophisticated research stations with suitable instrumentation and personnel for in-depth studies. Such studies may include observation or experimental work on organisms other than plants, such as insects, microbes or fungi, may be extended to detailed meteorological observations, or may focus on physiological or population processes to explain the observed change. GLORIA is a network (Figure 12) of research groups that share a common interest. Applying a standardised methodology allows a comparison of the regions, and the formu- lation of a regional to global view of how climate change affects natural biota (Pauli et al. 2009). The network currently consists of about 60 working groups and of permanent observation sites in more than 75 mountain regions on ﬁve continents. Reports from the ﬁrst recording campaign in Europe in 2001⁄2002, containing site descriptions and projec- tions, were presented by Kanka et al. (2005; High Tatra), Stanisci et al. (2005; Central Apennines), Coldea and Pop (2004; Romanian Carpathians), Kazakis et al. (2006; Lefka Ori, Crete), and from other continents by Mark et al. (2006; New Zealand), Pickering et al. (2008, 2009; Snowy Mountains, Australia), and Swerhun et al. (2009; Vancouver Island and Coast Range of south-western British Columbia, Canada).

OUTLOOK Alpine plants display trends by integrating the climatic effects of several years on their growth. This makes them a valuable research tool for learning about consequences of climate change. Monitoring alpine biota in the long-term will provide (i) deep knowledge on how climate affects alpine biota, and (ii) how diversity changes. The latter will serve as an early warning whether species may become threatened. Long-term studies on alpine ecosystems have the advantage over other ecosystems of using a set of indicators in a near-natural environment. There are not many other opportunities where climate change effects can be studied in a natural setting.

Acknowledgement We thank Laszlo Nagy for reading our manuscript, and for his many useful suggestions. The GLORIA-programme has been supported by the Austrian Academy of Sciences, the University of Vienna, the Austrian Ministry of Science and Research, and the MAVA- Foundation (Switzerland).

Short Biographies Georg Grabherr is Full Professor in the Department of Conservation Biology, Vegetation and Landscape Ecology at the Vienna University, Austria. His main focus of research has been vegetation studies in alpine environments, assessment of naturalness of forests, and conservation evaluation. Currently he concentrates on climate change effects on alpine ecosystems. He is chair of GLORIA, the Global Observation Research Initiative in Alpine Environment. Michael Gottfried is Assistant Professor in the Department of Conservation Biology, Vegetation and Landscape Ecology at the Vienna University, Austria. He has been

ª 2010 The Authors Geography Compass 4/8 (2010): 1133–1153, 10.1111/j.1749-8198.2010.00356.x Journal Compilation ª 2010 Blackwell Publishing Ltd Climate change impacts in alpine environments 1149 involved in alpine climate impact research for many years, and is one of the key persons for GLORIA, mainly involved in data analysis and ﬁeld work. Harald Pauli is Senior Scientist at the Institute of Mountain Research: Man and Envi- ronment of the Austrian Academy of Sciences, Vienna, Austria. He is an experienced mountain ecologist pioneering climate change research in alpine environments. Within GLORIA he is active in the scientiﬁc coordination of the network, in data acquisition and analysis.

Note * Correspondence address: Georg Grabherr, Department of Conservation Biology, Vegetation and Landscape Ecol- ogy, University of Vienna, Rennweg 14, A-1030 Vienna, Austria. E-mail: [email protected].

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