**3. Early plant colonization in glacier forelands as revealed by permanent plot studies**

After glacier retreat, new ground is provided for plant colonization. Substrate of the sample sites is variably rocky with amounts of rocks >6 cm between less than 25% to well over 80%. **Figure 3** portrays the early vegetation development in the glacier forelands of Goldbergkees and Lenksteinferner, showing basically similar trends concerning species numbers, individual numbers, ground cover, and life form composition.

At the initial survey in 2005, the A-sites immediately in front of the ice margin were entirely free of plants in both glacier forelands, while on the B-sites, a couple of species with very few individuals were already present. The early colonizers are the chamaephytes *Arabis alpina*, *Cerastium uniflorum*, *Saxifraga bryoides*, and *Saxifraga oppositifolia*; the herbs *Oxyria digyna* and *Veronica alpina*; as well as the grass *Poa alpina* on Goldbergkees and *A. alpina*, *Cerastium cerastoides*, *C. uniflorum*, the stoloniferous herb *Geum reptans*, and the grass *Poa laxa* on Lenksteinferner (**Figure 4**; for complete species lists of the two permanent plot studies, see Ref. [17]). Two years later also on the A-sites, the first individuals appear. On B-sites species and individual numbers exponentially increased, while ground cover is still low (**Figure 3**). The increasing trend continues during the first decade, slowing down slightly for species and individual numbers but accelerating for ground cover (**Figure 3**). In 2015, a total of more than 30 species are present on the permanent plots on Goldbergkees (median of individual A- and B-sites is 13 and 15, respectively) with over 1000 and 2000 individuals on the A- and B-sites, respectively. Somewhat lower are the values for the sample sites on Lenksteinferner with 22 species on the A-sites and 30 species on the B-sites (median of individual A- and B-sites is 8 and 11, respectively), with about half of the individual numbers of Goldbergkees (>500 on A-sites, just under 900 on B-sites).

Besides differences in absolute values concerning species numbers, individual numbers, and ground coverage (**Figure 3**), the permanent plot studies in the glacier forelands of Goldbergkees und Lenksteinferner prove a swift colonization of the bare ground and reveal generally similar trends in vegetation development. Vegetation dynamics in glacier forelands are controlled by three fundamental steps; all of them "may have, perhaps, the power to be the important limiting factor for succession and ecosystem development" [18]: step 1 is reaching the bare ground, step 2 is a successful establishment, and step 3 is growth and spreading.

**Figure 3.** Vegetation dynamics on permanent plots (A- and B-sites) in the glacier forelands of Goldbergkees (left) and Lenksteinferner (right) between 2005 and 2015. Development and variation between sites are shown by box and whisker plots for species numbers, individual numbers, and ground cover (for vascular plants only); at the bottom bar plots show mean life form spectra.

#### **3.1. Step 1 in primary succession: getting there**

number of dimensions and to make complex datasets with many species and samples interpretable. For the chronosequence data, unconstrained linear principal component analyses (PCAs) are employed. The graphic presentation of ordination analyses is by two-dimensional scatter plots displaying samples and/or species; explanatory environmental variables (if available) are displayed as arrows. The arrows point from the origin of ordinates in the direction of samples with above average values of the particular variable; the length represents the

After glacier retreat, new ground is provided for plant colonization. Substrate of the sample sites is variably rocky with amounts of rocks >6 cm between less than 25% to well over 80%. **Figure 3** portrays the early vegetation development in the glacier forelands of Goldbergkees and Lenksteinferner, showing basically similar trends concerning species numbers, individ-

At the initial survey in 2005, the A-sites immediately in front of the ice margin were entirely free of plants in both glacier forelands, while on the B-sites, a couple of species with very few individuals were already present. The early colonizers are the chamaephytes *Arabis alpina*, *Cerastium uniflorum*, *Saxifraga bryoides*, and *Saxifraga oppositifolia*; the herbs *Oxyria digyna* and *Veronica alpina*; as well as the grass *Poa alpina* on Goldbergkees and *A. alpina*, *Cerastium cerastoides*, *C. uniflorum*, the stoloniferous herb *Geum reptans*, and the grass *Poa laxa* on Lenksteinferner (**Figure 4**; for complete species lists of the two permanent plot studies, see Ref. [17]). Two years later also on the A-sites, the first individuals appear. On B-sites species and individual numbers exponentially increased, while ground cover is still low (**Figure 3**). The increasing trend continues during the first decade, slowing down slightly for species and individual numbers but accelerating for ground cover (**Figure 3**). In 2015, a total of more than 30 species are present on the permanent plots on Goldbergkees (median of individual A- and B-sites is 13 and 15, respectively) with over 1000 and 2000 individuals on the A- and B-sites, respectively. Somewhat lower are the values for the sample sites on Lenksteinferner with 22 species on the A-sites and 30 species on the B-sites (median of individual A- and B-sites is 8 and 11, respectively), with about half of the individual numbers of Goldbergkees (>500 on

Besides differences in absolute values concerning species numbers, individual numbers, and ground coverage (**Figure 3**), the permanent plot studies in the glacier forelands of Goldbergkees und Lenksteinferner prove a swift colonization of the bare ground and reveal generally similar trends in vegetation development. Vegetation dynamics in glacier forelands are controlled by three fundamental steps; all of them "may have, perhaps, the power to be the important limiting factor for succession and ecosystem development" [18]: step 1 is reaching the bare ground, step 2 is a successful establishment, and step 3 is growth and

relevance of the variable. Gradient analyses were performed with Canoco 4.5.

**3. Early plant colonization in glacier forelands as revealed by** 

ual numbers, ground cover, and life form composition.

**permanent plot studies**

130 Glacier Evolution in a Changing World

A-sites, just under 900 on B-sites).

spreading.

Reaching the bare ground is the first obstacle organisms have to conquer when colonizing new terrain. For this task, both a diaspore supply in the surroundings and the ability of a species to disperse from the seed source to the new ground are crucial. Concerning the former aspect, it makes a difference whether a glacier terminates within closed (sub)alpine vegetation with a rich diaspore supply or within sparsely vegetated scree slopes of the subnival belt. Several studies [19–22] have shown that recently deglaciated glacier forelands within the subalpine and lower alpine belt are colonized more quickly and more diverse concerning species numbers and life form composition than smaller glaciers terminating within the species poor upper alpine and subnival belts [1]. In addition, the few species present at higher elevations of the Alps do—despite small diaspores—not always possess high dispersal ability [5, 11], thus further impeding colonization. Seeding experiments, at least, have shown that artificial seed supply enhanced vegetation dynamics in glacier forelands and—what is even more important—that plant species are able to establish, which would hardly reach the bare

**Figure 4.** Characteristic early colonizers of central Alpine glacier forelands: *Arabis alpina* (a), *Cerastium uniflorum* (b), *Oxyria digyna* (c), *Saxifraga bryoides* (d), *Saxifraga oppositifolia* (e), stoloniferous *Geum reptans* (f), and *Poa alpina* (g) in the bulbil-producing ("viviparous") form.

ground by natural dispersal vectors [5, 11]. Nevertheless, commonly it does not take long until the first plant species in recently deglaciated high alpine glacier forelands (i.e., >2200 m a.s.l.) appear. Time frames reported range between 1 and 8 years [1, 21–24], and also the own survey attests a swift colonization with the first individuals appearing within 1–2 years [17]. The first colonizers are anemochorous taxa throughout, carried to the glacier foreland by valley winds from the surroundings and from lower elevations, too [25–27]. Thus, early colonizers are not only pioneer species sensu stricto (i.e., early colonizers not able to persist over time during succession, e.g., *S. oppositifolia*, *Saxifraga exarata*) but also early- to late-successional taxa (i.e., those that persist over time during succession but are able for early colonization as well, e.g., *A. alpina*, *C. uniflorum*, *O. digyna*, *S. bryoides*) and even those with ubiquitous behavior (e.g., *Leucanthemopsis alpina*, *Agrostis rupestris*, *P. alpina*; see Ref. [28]).

Chances for wind-dispersed early colonizers to reach the recently deglaciated glacier forelands are closely linked to the distance to seed sources. Even if taxa can be transported by wind over distances of up to a few kilometers (see Ref. [27]), highest seed rain is within a radius of several meters around the seed source [25, 27]. The longer the transport, the lower the chance to reach the new terrain, as the seeds may ground somewhere else or the diaspores are completely lost when carried to unsuitable sites for germination (water bodies, rocks, snow, dense established vegetation, etc.). The differences in species numbers, individual numbers, and ground cover values between the two study areas can be partly explained by differences in diaspore supply. Lenksteinferner is exposed to the North at a relatively high elevation (>2600 m a.s.l.) and surrounded by sparsely vegetated scree slopes with poor diaspore supply. More abundant seed sources are to be found at lower elevations from where seeds have to be carried up by valley winds. For instance, in 2015, a small larch seedling (*Larix decidua*) was encountered 300 vertical meters and more than 1 km away from the last conebearing adult Larch tree. Whether this seedling will survive remains to be seen; still, it highlights the relevance of long-distance dispersal for early colonization in glacier forelands. That Lenksteinferner is lagging behind Goldbergkees concerning species and individual numbers as well as groundcover values (**Figure 3**) most likely results from the larger distance to potential seed sources and thus the higher risk of diaspores getting lost. At Goldbergkees, located on lower elevation and in a more favorable exposure, last patches of closed alpine vegetation in the surrounding serve as seed sources for the colonization of the glacier foreland and are responsible for the higher species and individual numbers there. Besides wind, also water, avalanches, or mudflows might be locally important dispersal vectors for seeds or even whole plants into glacier forelands [26]. In addition, primary succession in glacier forelands might also be affected by seeds and plants originating from (debris-covered) glacier surfaces that are deposited in the glacier foreland after ice-melt [29–31].

#### **3.2. Step 2 in primary succession: establishing**

ground by natural dispersal vectors [5, 11]. Nevertheless, commonly it does not take long until the first plant species in recently deglaciated high alpine glacier forelands (i.e., >2200 m a.s.l.) appear. Time frames reported range between 1 and 8 years [1, 21–24], and also the own survey attests a swift colonization with the first individuals appearing within 1–2 years [17]. The first colonizers are anemochorous taxa throughout, carried to the glacier foreland by valley winds from the surroundings and from lower elevations, too [25–27]. Thus, early colonizers are not only pioneer species sensu stricto (i.e., early colonizers not able to persist over time during succession, e.g., *S. oppositifolia*, *Saxifraga exarata*) but also early- to late-successional

**Figure 4.** Characteristic early colonizers of central Alpine glacier forelands: *Arabis alpina* (a), *Cerastium uniflorum* (b), *Oxyria digyna* (c), *Saxifraga bryoides* (d), *Saxifraga oppositifolia* (e), stoloniferous *Geum reptans* (f), and *Poa alpina* (g) in the

bulbil-producing ("viviparous") form.

132 Glacier Evolution in a Changing World

The second important step of primary succession in glacier forelands is a successful establishment of plants. This is not guaranteed for all diaspores that reach the glacier foreland, and there are high interspecific differences in seedling recruitment and survival [26, 32–34]. A study [32] has shown that in some species chances for germination are highest within the first year but declining shortly thereafter. For *Artemisia genipi* and *Achillea moschata*, germination success within the first year was at 98.8% and 68.8%, respectively. For other species, e.g., *Linaria alpina* or *S. oppositifolia*, germination success within the first year was very low (0.4% and 2.0%, respectively) but much higher during the following years. Such taxa build up a seed bank waiting for the right conditions to sprout, with diaspore morphology and diaspore weight determining how long the seeds are able to survive. A higher weight and a more compact seed coat increase the chance for successful germination after some years of dormancy. Those differences in germination behavior are reflected by the species frequencies in the glacier forelands studied. Species which are able to sprout immediately after reaching the glacier foreland show a swift increase in individual numbers and ground cover (e.g., *O. digyna*, *G. reptans*, *C. uniflorum*, *A. alpina*), while others with low germination success without interim dormancy such as *L. alpina* are significantly underrepresented [17].

Once diaspores have germinated, the next obstacle is to survive the juvenile stage, which is a particularly sensitive phase and characterized by high mortality rates due to different potential threats [3, 5, 26, 35], which should be discussed next. Despite low contents of organic material, nitrogen, and phosphor, nutrient matter does not seem to be responsible for seedling mortality in glacier forelands. Just after ice retreat, the substrate has sufficient nutrients by atmospheric dust and N-depositions to instantly allow plant growth [28, 36–39]. Algae, cryptogams, and mosses might be involved but obviously do not play an important role in site melioration [17, 21, 40]. More important for the establishment of diaspores than nutrient matters are probably the prevailing substrate conditions. Glacier forelands are commonly regarded as unconsolidated, instable ground with a high amount of coarse rocks impeding colonization by plants. The permanent plots on Goldbergkees and Lenksteinferner locally feature a high amount of coarse material, but situated on more or less leveled ground this is remarkably solid [17]. Soil frost activity (solifluction, cryoturbation) is effectively suppressed by a long-lasting snow cover for 8–9 months and only rare freezing events during the snow-free season (late June/early July to late September/ early October). Thus substrate instability cannot be assumed a universal factor for seedling mortality in alpine glacier forelands. Also, a high amount of coarse boulders is no obstacle for colonization, a minimum of fine grained substrate provided for rooting and water supply. In fact, larger rocks provide safe sites with microclimatically more favorable conditions (shorter snow cover duration, pronounced warming, etc.), and a lack of such safe sites significantly enhances seedling mortality and slows down early colonization within glacier forelands [11]. Despite a high amount of precipitation, reduced evapotranspiration, and additional water supply by melting snow and ice, desiccation of the coarse-grained substrates could be another important reason for mortality in glacier forelands, in particular during seedling and early development stage [4, 41, 42]. In particular under longerlasting drought phases and/or reduced snow cover related to climate warming, desiccation might become a more important issue in the future. Concerning soil temperatures multiyear measurements in the root horizon of plants (−10 cm) show rather mild conditions within glacier forelands [17]. Despite high inter- and intra-annual variations (~50%) which are expressed primarily in the length of vegetation period and temperature sums, mean temperatures between 6 and 10°C were recorded during the snow-free period in the glacier forelands of Lenksteinferner and Goldbergkees. These are higher temperatures than at tree line, where the trees make themselves a cold root horizon by shadowing effects [43]. Freezing temperatures within the root horizon in the glacier forelands occur but are rare during the snow-free season. While seeds are rather unsusceptible to moderate freezing, seedlings are not [6]. Species investing primarily in aboveground biomass are particularly at risk, while those that invest mainly in below-ground biomass during the first year (e.g., *O. digyna*) are less vulnerable, show lower mortality rates, and are represented by higher individual numbers and ground cover values [17, 25]. Besides desiccation and freezing during the vegetation period, the winter months are the second crucial phase for the survival of seedlings. A snow cover lasting for too long can prevent successful establishment and carbon gain; if snow cover removal is too early, the risk of freezing damage to the seedlings is high, and in addition, periglacial processes may mechanically negatively affect the roots. In the glacier forelands of Goldbergkees and Lenksteinferner, seedling mortality in general is low, indicating that none of the mentioned potential threats is common or at least was common during the study period between 2005 and 2015.

#### **3.3. Step 3 in primary succession: grow up and spread**

in the glacier forelands studied. Species which are able to sprout immediately after reaching the glacier foreland show a swift increase in individual numbers and ground cover (e.g., *O. digyna*, *G. reptans*, *C. uniflorum*, *A. alpina*), while others with low germination success without

Once diaspores have germinated, the next obstacle is to survive the juvenile stage, which is a particularly sensitive phase and characterized by high mortality rates due to different potential threats [3, 5, 26, 35], which should be discussed next. Despite low contents of organic material, nitrogen, and phosphor, nutrient matter does not seem to be responsible for seedling mortality in glacier forelands. Just after ice retreat, the substrate has sufficient nutrients by atmospheric dust and N-depositions to instantly allow plant growth [28, 36–39]. Algae, cryptogams, and mosses might be involved but obviously do not play an important role in site melioration [17, 21, 40]. More important for the establishment of diaspores than nutrient matters are probably the prevailing substrate conditions. Glacier forelands are commonly regarded as unconsolidated, instable ground with a high amount of coarse rocks impeding colonization by plants. The permanent plots on Goldbergkees and Lenksteinferner locally feature a high amount of coarse material, but situated on more or less leveled ground this is remarkably solid [17]. Soil frost activity (solifluction, cryoturbation) is effectively suppressed by a long-lasting snow cover for 8–9 months and only rare freezing events during the snow-free season (late June/early July to late September/ early October). Thus substrate instability cannot be assumed a universal factor for seedling mortality in alpine glacier forelands. Also, a high amount of coarse boulders is no obstacle for colonization, a minimum of fine grained substrate provided for rooting and water supply. In fact, larger rocks provide safe sites with microclimatically more favorable conditions (shorter snow cover duration, pronounced warming, etc.), and a lack of such safe sites significantly enhances seedling mortality and slows down early colonization within glacier forelands [11]. Despite a high amount of precipitation, reduced evapotranspiration, and additional water supply by melting snow and ice, desiccation of the coarse-grained substrates could be another important reason for mortality in glacier forelands, in particular during seedling and early development stage [4, 41, 42]. In particular under longerlasting drought phases and/or reduced snow cover related to climate warming, desiccation might become a more important issue in the future. Concerning soil temperatures multiyear measurements in the root horizon of plants (−10 cm) show rather mild conditions within glacier forelands [17]. Despite high inter- and intra-annual variations (~50%) which are expressed primarily in the length of vegetation period and temperature sums, mean temperatures between 6 and 10°C were recorded during the snow-free period in the glacier forelands of Lenksteinferner and Goldbergkees. These are higher temperatures than at tree line, where the trees make themselves a cold root horizon by shadowing effects [43]. Freezing temperatures within the root horizon in the glacier forelands occur but are rare during the snow-free season. While seeds are rather unsusceptible to moderate freezing, seedlings are not [6]. Species investing primarily in aboveground biomass are particularly at risk, while those that invest mainly in below-ground biomass during the first year (e.g., *O. digyna*) are less vulnerable, show lower mortality rates, and are represented by higher individual numbers and ground cover values [17, 25]. Besides desiccation and freezing during the vegetation period, the winter months are the second crucial phase for the survival

interim dormancy such as *L. alpina* are significantly underrepresented [17].

134 Glacier Evolution in a Changing World

The third important step for a successful plant colonization of new ground is grow up and spread [18]. Many of the early colonizers are long-lived taxa, with a life expectancy of up to 50 years, in clonal and cushion plants even more [42]. Once established, plants occupy their sites for decades [44, 45], unless the site conditions change fundamentally. With water and nutrient supply ensured, established plants grow and gain ground cover under almost uncompetitive conditions. Like all perennial plants, also the high-elevation specialist alternates between phases of growth and phases of reproduction, which are subject to seasonal cycles [46]. Day length and/or a priori low-temperature period during winter ("vernalization") control the right timing of flowering. While after the cold stimulus and during early summer investment is mainly in reproductive plant parts, after fruiting biomass increase is again paramount (see Ref. [47] for *A. alpina*). Simultaneously with growth new individuals establish from both external seed sources and diaspore-bearing individuals on the sample sites itself. A synchronous operation of steps 1, 2, and 3 side by side is pushing forward succession. In consequence, a positive logarithmic or even exponential increase of species numbers, individual numbers, and ground coverage emerges as soon as the established individuals produce diaspores, which commonly happens the second year after establishment [25]. As most seeds are deposited in the immediate surrounding of the mother plant (leptokurtic diaspore dispersal behavior!), this direct diaspore input is superior to long-distance dispersal [5, 25, 27]. In addition, the ability for self-pollination in many taxa enhances the reproductive success, albeit at the expense of genetic variability.

Besides seed rain also vegetative propagation of capable species is relevant for increasing ground cover values and individual numbers of established plants [42, 45]. One of those species that perform both generative and vegetative propagations is the stolon-producing *G. reptans* (see **Figure 4**). The downside of reduced genetic variability is compensated by spread even in unfavorable years prohibiting generative propagation [48]. Another way of vegetative (clonal) reproduction is performed by *P. alpina* (**Figure 4**) which is producing bulbils in its pseudo-viviparous form. The development of genetically identical daughter plants instead of seeds is triggered by unfavorable site conditions and thus becomes more important under adverse conditions with higher elevation [42]. In the glacier forelands, the pseudo-viviparous form is much more common than the normal seed-producing form. The daughter plants are photosynthetically active already on the mother plant and after release are dispersed by wind. In doing so, a faster and more successful establishment within the glacier forelands is guaranteed compared to the development of diaspores with all the uncertainties during establishment. In preserving the genetic information, this strategy could even be a selective advantage for *P. alpina* in comparison to the non-viviparous form [49].

The permanent plot studies show a very dynamic colonization of recently deglaciated ground. Vegetation dynamics in general are governed by the relative favor or disfavor of a site, which is a function of many different interrelated factors such as elevation, exposure, snow cover duration, continentality, existence of safe sites, seed sources, etc. Despite differences in the absolute values, in general, a swift fill-up of empty niches is taking place during the first decade of the permanent plot study, promoted by the growth of established individuals as well as by a continuous colonization by new individuals. These are invasive populations according to Ref. [50] with young individuals prevailing. A more uniform ("Gaussian") distribution with many species of intermediate age and few young and old ones, which would indicate stable populations (see Ref. [45]), is not yet reached. Several species invest most of the resources in generative reproduction and are able to create persistent diaspore banks. Many of the early colonizers also show ruderal characteristics [51] such as fast increment, the ability for self-pollination, or anemochorous dispersal. Just like their lowland counterparts, alpine ruderals are able to colonize sites with a high disturbance frequency, unlike, however, is their much greater life expectancy [42, 45]. Most of the species encountered in the sample sites are far from their maximum age, explaining the low number of losses in the repeated surveys. If dropouts occur, they are compensated by newly established individuals of the same species, expressed in a general increase of groundcover and individual numbers. One notable exception is *A. alpina* with a life expectancy of only a couple of years. In both glacier forelands, this species is regularly present with diebacks during resurveys. *A. alpina*, however, as self-pollinating species [47] produces a high number of diaspores able for immediate germination and thus a high number of seedlings every year. The short life cycles of *A. alpina* causing a continuous dieback of individuals keep increase of individual numbers moderate compared to more long-lived species such as *O. digyna*, *C. uniflorum*, or *S. bryoides*. Only locally temporary setbacks in the overall vegetation development by disturbances are apparent [17]. Most common is the displacement of meltwater runoff over-pouring the sample sites for a while. The overdose of (cold) water, probably combined with a higher frequency and intensity periglacial processes in the substrate (solifluction, cryoturbation, needle ice, etc.) negatively impacts the life processes of the plants, which is expressed in diebacks of quite a number of individuals of different species in such cases. When the melt-out stops or the runoff is displaced again, progressive developments reemerge.
