Pioneer zone geo-ecological change: Observations ...

Catena 135 (2015) 219–230

Contents lists available at ScienceDirect

Catena journal homepage: www.elsevier.com/locate/catena

Pioneer zone geo-ecological change: Observations from a chronosequence on the Storbreen glacier foreland, Jotunheimen, southern Norway John A. Matthews a,⁎, Amber E. Vater b a b

Department of Geography, College of Science, Swansea University, Singleton Park, Swansea SA2 8PP, UK UK Environmental Observation Framework, Natural Environment Research Council, Polaris House, Swindon SN2 1EU, UK

a r t i c l e

i n f o

Article history: Received 3 April 2015 Received in revised form 24 June 2015 Accepted 20 July 2015 Available online xxxx Keywords: Pioneer zone Glacier foreland Geo-ecological succession Cryptogamic crust Stone pavement Biotic and abiotic processes

a b s t r a c t The first 33 years of primary geo-ecological succession is investigated in the pioneer zone of the Storbreen glacier foreland using the chronosequence approach. Pitfall trapping of invertebrates and the sampling of higher and lower plants and habitat factors from quadrats were used on three replicate transects across a till plain accurately dated by annually monitored glacier front variations combined with the mapping of annual moraine ridges. Unstable, saturated sediments deglacierized for b1 year are colonized first by very large numbers of Collembola and a small number of epigeal beetles and spiders. Improved drainage, loss of fine matrix by pervection and frost sorting lead to the development of an active stone pavement after 6–21 years, which is colonized by sparse herbaceous perennials, a slowly-developing cryptogamic crust dominated by mosses, and moderately abundant epigeal beetles, spiders and the glacier harvestman (Mitopus morio). Further soil development and stabilization of the stone pavement lead, via a transition phase (21–26 years), to a fast developing ecosystem (26–33 years) in which the cover of most of the plants and pitfall catches of invertebrate groups are increasing rapidly (including a resurgence in Collembola catches and the spread of Racomitrium moss, terrestrial lichens and shrubs). Spatial heterogeneity reflects gradual successional trajectories related to small variations in physical habitat conditions. The sequence of changes is summarized in a conceptual geo-ecological model in which abiotic and biotic processes combine to drive the pioneer stages of both invertebrate and plant succession with little evidence of highly integrated biotic communities. © 2015 Elsevier B.V. All rights reserved.

1. Introduction Newly deglacierized terrain in front of retreating glaciers has been a major source of insights into the classical concepts of plant succession and soil development (Crocker and Major, 1955; Matthews, 1992; Nagy and Grabherr, 2009; Walker and del Moral, 2003). These aspects of ecological change continue to be widely investigated in the context of glacier forelands (e.g., Darmody et al., 2005; Egli et al., 2006; Garibotti et al., 2011; Jones and del Moral, 2005a, 2005b, 2009; Jones and Henry, 2003; Mori et al., 2006, 2008, 2012; Prach and Rachlewicz, 2012; Raffl et al., 2006; Robbins and Matthews, 2009, 2010, 2014; Vilmundardóttir et al., 2014; Whittaker, 1993). The underlying reason for this continuing interest lies in the pattern of increasing terrain age with distance from the snout of a retreating glacier, which produces a chronosequence — a spatial pattern at one point in time that is representative of change through time (Cutler et al., 2008; Johnson and Miyanishi, 2008; Lawrence et al., 2010; Stevens and Walker, 1970). Chronosequences represent ‘natural experiments’ ⁎ Corresponding author. E-mail addresses: [email protected] (J.A. Matthews), [email protected] (A.E. Vater).

http://dx.doi.org/10.1016/j.catena.2015.07.016 0341-8162/© 2015 Elsevier B.V. All rights reserved.

(Deevey, 1969; Diamond, 1986; Diamond and Robinson, 2010; Fukami and Wardle, 2005) that permit the investigation of ecological changes over longer timescales than can be conveniently studied by real-time observation and field experiment. Such space-for-time substitution (Pickett, 1988) is effective because, as the terrain age varies, other environmental factors are relatively invariant and the chronosequence signature can be distinguished clearly from other forms of environmental variation. Other aspects of ecosystems that have been investigated intensively in glacier–foreland chronosequences include insect and arachnid succession (Kaufmann, 2001, 2002; Kaufmann et al., 2002; Hodkinson et al., 2001, 2002, 2004; Skubała and Gulvik, 2005; Gobbi et al., 2006a, 2006b, 2007, 2010; Gobbi, 2014; Hågvar et al., 2009; Hågvar, 2010a, 2012; Gereben-Krenn et al., 2011; Bråten et al., 2012; Ingimarsdóttir et al., 2012; Vater, 2012; Flø and Hågvar, 2013; Hågvar and Ohlson, 2013; Vater and Matthews, 2013, 2015; Brambilla and Gobbi, 2014; Raso et al., 2014), and the presence and possible roles of microorganisms, including blue-green algae (cyanobacteria), bacteria and fungi (Bardgett and Walker, 2004; Bardgett et al., 2005; Bradley et al., 2014; Carlson et al., 2010; Kaštovská et al., 2005; Knelman et al., 2012; Nemergut et al., 2007; Nicol et al., 2005; Ohtonen et al., 1999; Schmidt et al., 2015; Sigler and Zeyer, 2002; Tscherko et al., 2003, 2005).

220

J.A. Matthews, A.E. Vater / Catena 135 (2015) 219–230

Considerable knowledge has therefore accumulated relating to the biological aspects of glacier–foreland ecosystem development. Relatively little is known, however, about how the various biological components of the ecosystem interact. There has been even less consideration of the interactions between the biological components and the physical components of the wider geo-ecosystem (i.e., the ecosystem in its landscape context). The pioneer zone, wherein the earliest stages of ecosystem development take place, has the potential to yield important new information on geo-ecological change. This information includes the biological drivers of change, such as dispersal ability, establishment and competition between species, and the possible geo-dynamic drivers of the abiotic habitat, such as hydrological change and cryoturbation (ground disturbance by freezing and thawing). Although the pioneer zone may appear, at first sight, to be almost devoid of life, it has considerable advantages in the context of investigating geo-ecological change. Three main advantages should be emphasised: first, terrain age can often be established accurately using available data on the rate of glacier retreat; second, the flora and fauna are relatively simple and co-exist in a relatively uniform and severe physical environment; and, third, the earliest phases of ecosystem succession take place rapidly, producing strong time-dependent patterns in the landscape and affording limited opportunity for environmental change to have affected different parts of the chronosequence in different ways during its short history. Geo-ecological change may be more difficult to unravel in more complex and/or longer chronosequences.

Thus, this paper aims to explore geo-ecological succession in the pioneer zone of the Storbreen glacier foreland, using the chronosequence approach. Specific objectives are: • to describe the patterns and changes in plant cover (including cryptogams), and in selected invertebrate animal groups (by pitfall trapping of surface-active beetles, spiders, harvestmen and springtails), over the first 33 years of the chronosequence; • to describe certain associated aspects of the physical habitat – including substrate texture, drainage conditions and disturbance levels – which have the potential to affect pioneer life during ecological succession; • to infer likely interactions between these biotic and abiotic components of the pioneer-zone geo-ecosystem, and to develop a conceptual model of the geo-ecological drivers of change.

2. Study area Storbreen (8°35′E; 60°35′N), glacier number 2636 in the Inventory of Norwegian Glaciers (Andreassen and Winsvold, 2012), with an area of 5.22 km2, is one of the largest glaciers in western Jotunheimen, central southern Norway. The glacier is located on the eastern slope of Smørstabbtindan massif draining towards Leirdalen. The pioneer zone was investigated to the south-east of the glacier snout at an altitude of about 1420 m above sea level (Fig. 1). Here, the glacier has retreated across an almost horizontal till plain with little relief apart from small

Fig. 1. The pioneer zone of Storbreen glacier foreland showing transects and sites in relation to dated annual moraine ridges.


221

ridges from 1988, 1989, 1996 and 1998 are accounted for by having been overridden by glacier advances in later years. The sparsity of moraine-ridge formation after 1999 is accounted for by the generally accelerating rate of glacier retreat during recent years. 4. Research design and methods

Fig. 2. Cumulative annual glacier front variations of Storbreen AD 1975–2010.

(mostly b 0.5 m high) moraine ridges deposited annually since the late 1970s (see below). The study area is located about 400 m above the local tree line, within the mid-alpine belt dominated by lichen heath and snowbed communities (Dahl, 1986; Moen, 1999). Based on the closest meteorological station (Sognefjell, 1413 m a.s.l.), the mean annual air temperature at this location is about − 3.1 °C (July mean, + 13.4 °C; and January mean, −10.7 °C) with a mean annual precipitation of 860 mm (Aune, 1993; Førland, 1993). The present lower altitudinal limit of discontinuous permafrost in this area of Jotunheimen lies at about 1500 m a.s.l. (Etzelmüller and Hagen, 2005; Hipp et al., 2014; Lilleøren et al., 2012). The study area is therefore characterised by a severe seasonal periglacial environment with a deep seasonal ground freezing and thawing regime (cf. Thorn et al., 2008). The substrate consists of glacial diamicton (till), an unsorted sediment with characteristically mixed grain sizes ranging mainly from silt to boulders with a dominant matrix of sand and silt. This has been derived from the local bedrock, which is predominantly pyroxene-granulite gneiss (Lutro and Tveten, 1996). On deglacierization, the local till is initially close to neutral in reaction but is rapidly acidified (Mellor, 1985; Messer, 1988). 3. Chronology of the pioneer zone Terrain age was accurately established by combining measurements of glacier front variations with the position of the annual moraine ridges. The annual retreat or advance of the glacier between 1975 and 2010, as determined by the Norwegian Polar Institute and the Norwegian Water Resources and Energy Directorate (e.g., Kjøllmoen, 2011), is summarized in Fig. 2. Distance from a single fixed point to the glacier margin was measured at the end of the ablation season in most years. Cumulative net retreat between 1975 and 2010 was 146 m; small net advances of 1–10 m occurred in 1989, 1990, 1997, 1999 and 2005. The moraine ridges were formed by annual winter advances of the glacier snout when the glacier retreat rate was generally decelerating or more-or-less stationary between 1980 and 1999 (Hiemstra et al., in press). Dates for individual ridges in Fig. 1 were assigned by ‘counting back’ from the position of the glacier snout in 2010 using the glacier front variations shown in Fig. 2. The moraine ridges deposited before 1990 are largely degraded but their position and alignment were still clear in 2010. The most prominent ridges (dating from 1990 and 1999) correspond with two or more years of net annual advance. ‘Missing’

Our methodology and the resulting variables selected were chosen to enable a meaningful investigation of geo-ecological succession given the nature of the biota and the habitat in relation to the practicalities of sampling and measurement during a limited period of fieldwork. Three transects (A, B and C) were set out across the chronosequence and a total of 72 sites (24 per transect) were located for recording vegetation, invertebrates and abiotic habitat factors (Fig. 1). Along each transect, sets of three replicate sites were located a few metres apart on terrain deglacierized in 2010, 2005, 1999, 1990, 1987, 1985, 1980 and 1978. Terrain age of these sites is established to the nearest year, with the possible exception of the 1990 sites on transects B and C, the age of which may be slightly overestimated because of overlapping moraine ridges. The aim was to obtain representative samples from the pioneer zone with particular reference to terrain age. The precise location of each site was constrained by the necessity to maintain comparable topographic and other physical environmental conditions while avoiding major disturbances by streams and mass movement processes, and fully representing the terrain ages from 1 to 33 years. Flat, well-drained sites between annual moraine ridges were preferred and areas of non-representative substrate (patches of well-sorted glaciofluvial gravel and glaciolacustrine silt) were avoided. A pitfall trap, consisting of a plastic cup (diameter 7 cm; lip flush with the ground surface) containing 25 ml of white vinegar saturated with salt and a few drops of washing-up liquid, was positioned at the centre of each site. The 72 traps were operational simultaneously and collections were made for two periods of four days in mid-August 2011. Counts were made of the total number of individual invertebrates caught in each trap during each collection but only epigeal (surface active) Coleoptera (beetles) and Arachnida (spiders and harvestmen) were identified to species level as pitfall trapping is best suited to these groups. The numbers of Collembola (springtails) were also counted as a group without further differentiation. Percentage cover of plant species around each trap was recorded in 1 m2 quadrats. Vascular plants and the most commonly occurring mosses (except for the cryptogamic crust) and terricolous (ground dwelling) lichens were identified to species level. Percentage cover of cryptogamic crust, which develops on the ground surface between stones and appears to be composed mainly of tiny unidentified mosses, was recorded as an undifferentiated group. The percentage cover and diameter of crustose epilithic lichens (grey Lecidea spp. and yellowgreen Rhizocarpon subgenus) which grow on the surfaces of stones but are not part of the terricolous succession, were measured for use as indicators of the stability of the ground surface. Substrate texture (percentage ground-surface cover) was recorded in three grain-size categories: (1) boulders and cobbles (particle size N 64 mm diameter), (2) pebbles (b 64 mm, N 4 mm), and (3) fines (b4 mm). Fine percentage was used as an index of disturbed ground resulting mainly from surface wash and cryoturbation (frost churning). Presence or absence of standing surface water was used as an indicator of whether or not surface sediments were saturated with water. A drainage-rate index was provided by the time (in seconds) taken for 30 ml of water to drain away when poured onto the ground surface. 5. Results 5.1. Plants The plant taxa recorded are summarized as both mean cover values across the three transects (Table 1) and maximum cover values in any

222


Table 1 Average percentage cover (plant taxa) and number of individuals trapped (invertebrates taxa) on three transects in the pioneer zone at Storbreen (+ denotes cover b 0.5%). Sub-categories include: graminoids (G), forbs (F), shrubs (S) and a clubmoss (C); mosses (M) and terricolous lichens (L); spiders (Araneae, A), beetles (Coleoptera, C) and a harvestman (Opiliones, O). Species

Terrain age (years) 1

Higher plants Arabis alpina (F) Saxifraga cespitosa (F) Cerastium cerastoides (F) Poa alpina (G) Trisetum spicatum (G) Poa vivipara (G) Festuca ovina (G) Saxifraga rivularis (F) Epilobium anagallidifolium (F) Festuca vivipara (G) Luzula arcuata (G) Saxifraga oppositifolia (F) Oxyria digyna (F) Cerastium alpinum (F) Salix glauca (S) Deschampsia alpina (G) Minuartia biflora (F) Veronica alpina (F) Saxifraga stellaris (F) Ranunculus glacialis (F) Phleum alpinum (G) Salix herbaceae (S) Cardamine bellidifolia (F) Gnaphalium supinum (F) Saxifraga nivalis (F) Epilobium latifolium (F) Luzula spicatum (G) Sedum rosea (F) Salix lanata (S) Lycopodium selago (C) Empetrum hermaphroditum (S)

12

21

24

26

4 1 1 1 1 + + + + + +

1 2 1 1 2 1 + + +

2 2 + 2 1 + 1 +

1 1 1 1 2 1 1 +

1 1 2 1 1 1 + +

31

33

1 1 1 1

+ 1 + 1 1

3 + +

1

1 + + + + + + + + + +

+ + +

+ +

+ + + + + +

+ + + +

1 1 + + +

1 + 1 1

2 1 +

+ + + +

+

+

1

+

+

+

+ +

+ +

1

5.2. Invertebrates

+ + + +

Lower plants Polytrichum sexangulare (M) Racomitrium canescens (M) Cetraria nivalis (L) Stereocaulon alpinum (L) Solorina crocea (L) Cetraria islandica (L) Alectoria ochraleuca (L) Cryptogamic crust Invertebrates Erigone arctica (A) Nebria nivalis (C) Bembidion fellmanni (C) Mitopus morio (O) Geodomicus longipes (C) Bembidion sp. (C) Amara quenseli (C) Nebria sp. (C) Erigone longipalpis (A) Collembola spp.

6

+

1

2 +

+ 1 + 1 +

2 12 1 3 + +

+

2 2 1

986

3

4

5

13

19

21

7

9 2 1 9 3 2 4 1

6 2

13

13 1

41

14 2 1 33 14 2 2 3 1 224

2 4 2 1

71

9

2 9 9

1

2

10

16

Trisetum spicatum, but none exceed a mean cover value of 4% and maximum cover of all these species together remains low (b 15%) at all points across the chronosequence. (2) Cryptogamic crust develops slowly with a high degree of local variation, reaching 3–5% mean cover (maximum b 10%) after 6–21 years. Thereafter, it increases more rapidly in area attaining a mean of 13% cover (maximum N 30%) on terrain age 24 years, but cover declines to a mean of only 4% (maximum 16%) at terrain age 33 years. (3) Mosses distinct from the cryptogamic crust (especially Racomitrium canescens) and terricolous lichens (especially Stereocaulon alpinum) rarely occur on terrain younger than 20 years but then rapidly increase in abundance on terrain ages N 26 years. These two species form relatively extensive mats, attaining mean cover values of 18% and 7%, respectively, after 33 years of development (the maximum cover attained by R. canescens is 28%). (4) Woody plants, which are rarely encountered in the pioneer zone, are the slowest colonizing plant group. The earliest occurrence is on 12 year-old terrain, the maximum cover recorded for all woody species combined is 4% on 31 year-old terrain, and Salix glauca and Salix herbaceae are the only woody species to attain a mean cover of 1% (after 31 years).

9 11 1 1 4 114

1 18 1 7 + + + 4

5 3 62 3 3 2 1 374

one transect (Fig. 3A). Maximum values show the plant patterns more clearly than the mean values and also give information on the considerable variability present in the data. The following patterns in species composition and cover-abundance can be recognised across the chronosequence: (1) Herbaceous perennials, the earliest colonizers amongst the higher plants, are absent from the youngest sites (deglacierized for 1 year). They occur sporadically but are more conspicuous than the lower plants and cryptogamic crust on terrain ages of 6–21 years. The commonest species include the forbs, Arabis alpina and Saxifraga cespitosa, and the grasses, Poa alpina and

Notable patterns in the average pitfall catches of invertebrates across the chronosequence (Table 1 and Fig. 3B) are as follows: (1) Springtails (Collembola) are extremely active at the sites on the youngest ground (terrain age 1 year). Almost 1000 individuals were caught in the traps at these sites and, although variability was high, large numbers were caught in all the traps. Catches drop to b 100 individuals on terrain deglacierized for 6 years and fall further to a minimum of 10–20 individuals on terrain age 21 years before rising steadily thereafter to N 370 individuals on the oldest ground. (2) Harvestmen (Opiliones) are represented by one species – Mitopus morio (the glacier harvestman) – which is the commonest trapped larger epigeal invertebrate on the Storbreen glacier foreland as a whole (cf. Vater, 2012). Although absent from the youngest ground, it is consistently present (4–9 individuals trapped) on terrain ages of 6–26 years, and catches rise steadily thereafter to 62 individuals on the oldest ground. (3) Spiders (Araneae) and beetles (Coleoptera) exhibit similar patterns. Both groups were trapped in low numbers on all terrain ages. Overall numbers (24 individual beetles from 4–5 taxa and 15 spiders from two taxa) appear to attain a maximum at 31 years with a subsequent reduction in catches on the oldest ground. (4) The species number (richness) of Coleoptera and arachnids and higher plants exhibit similar patterns across the chronosequence (Fig. 3C). In both cases, close to maximum species richness is achieved within 12 years of deglacierization, whereas species richness of the lower plants (excepting non-identified species in the cryptogamic crust) exhibits a slower start and is continuing to rise on the oldest terrain examined.

5.3. Habitat factors and stability indicators Patterns in the mean values of physical habitat factors (Fig. 4A) and the maximum sizes and total cover of epilithic lichens used as stability indicators (Fig. 4B) may be summarized as follows: (1) Apart from areas immediately adjacent to pools of standing water encountered on the youngest ground, there is no clear


223

Fig. 3. Biotic components of the geo-ecosystem at Storbreen across the chronosequence: (A) Cover-abundance of plant groups across the chronosequence: maximum percentage ground-surface cover of each plant group is shown (each data point is the highest average percentage cover for the three quadrats from a single transect). (B) Catches of invertebrate groups across the chronosequence: total number of individuals caught from each invertebrate group is shown (each data point is the sum of the individuals caught in two collections from a total of nine traps from the three transects). (C) Species number across the chronosequence: species richness is shown for each taxonomic group (each data point represents the total number of species recorded in all transects, collections, quadrats and/or traps).

trend in the drainage rate, which consistently averages 5–9 s across the chronosequence, indicating well-drained sites. (2) Substrate texture exhibits significant variations. Fines (b4 mm) comprise about 40% of the surface on the 1-year old terrain, falling rapidly to b15% and remaining below this value for the remainder of the chronosequence (terrain ages 6–33 years). Minimum cover of fines occurs at 31 years, which corresponds with maximum vegetation cover (Fig. 4A). (3) Initially, pebbles (4–64 mm) cover about 30% of the surface, a proportion that rises rapidly to about 55% at sites deglacierized for 6 years. This results in a stone pavement, which characterises the remainder of the chronosequence, though the pavement becomes less conspicuous after about ~ 24 years as it is partly overgrown by the cryptogamic crust and other vegetation.

(4) Cobbles and boulders (N 64 mm) slowly become an increasingly important component of the surface sediment over the first 20–24 years, rising from b 20% to N 30%. Although these particles contribute to the stone pavement, they are too large to be overgrown by small plants; hence their percentage cover does not fall significantly on the relatively old terrain. (5) Epilithic lichens are not visible on the surface of pebbles, cobbles and boulders at sites exposed for b 24 years but increase consistently in size on these surfaces once stabilized (Fig. 4B). The inferred growth rate of the Rhizocarpon subgenus over 7 years between terrain ages 24–31 years is about 1.4 mm yr−1, while that of Lecidea spp. is much faster (possibly as high as 9 mm yr−1 on terrain deglacierized for between 24 and 26 years).

224


Fig. 4. (A) Properties of the habitat across the chronosequence: percentage cover values are shown (each data point represents the average of a total of nine quadrats from the three transects). (B) Epilithic lichens across the chronosequence: maximum diameter of Rhizocarpon subgenus and Lecidea spp., and total epilithic lichen cover.

6. Discussion Our discussion focuses on the inference of geo-ecological interactions and possible biotic and abiotic drivers of successional dynamics within the pioneer zone. The scope for such inferences is necessarily limited by the nature of our data – largely descriptive with little replication – resulting in small sample sizes in relation to sparse populations in a heterogeneous landscape, with little possibility of statistical analysis. Nevertheless, by combining the data from the three transects, patterns have been revealed in relation to plants, invertebrates and habitat factors, which allow a first attempt at a geo-ecological approach to succession in the pioneer zone. 6.1. Assumptions First, the chronosequence approach assumes that all sites started from identical initial environmental conditions (Cutler et al., 2008; Johnson and Miyanishi, 2008; Lawrence et al., 2010; Matthews, 1992). Although all sites at time zero could not have been identical in every respect – small differences in substrate texture and microtopography, for example – our sampling design ensures that they were closely similar. Terrain deglacierized in 2010 is therefore considered to be a close approximation to the initial conditions at the commencement of succession at all of the sites. The second major assumption underlying the chronosequence approach is that each site in the chronosequence had an identical

environmental history during succession. In the pioneer zone, small environmental differences would have been associated with variations in the rate of glacier retreat. When the glacier retreat rate slowed and small net glacier advances occurred (1990–1999; Fig. 2), the newly deglacierized sites would have been close to the glacier snout for longer than when the glacier was retreating rapidly. Consequently, sites deglacierized for 12–21 years would, in this case, have experienced such factors as cold air drainage from the glacier, glacier winds and snowbeds banked against the glacier snout for a relatively long period of time. There may also be a direct effect of recent climate change. Kaufmann (2002) has demonstrated, for example, that an increase in summer temperature of 0.6 °C may approximately double the speed of initial colonization by surface-active invertebrates in the Austrian Alps. Close proximity of our sites in space and the relatively small differences in terrain age involved in the pioneer zone nevertheless mean that the environmental history of each site is likely, in most respects, to have been closely similar to the environmental history that would have affected a single site during succession. 6.2. Initial environmental conditions (terrain age 0 year) Initially, the substrate at time zero (deglacierized a few months before fieldwork was carried out in summer 2011) is an unsorted diamicton that is saturated with water from glacial meltwater, melting snow and the thawing of seasonally-frozen ground, and is therefore unstable (in the sense of being mobile). The largely


unweathered sediment, being freshly deposited till, is close to neutral in reaction (Messer, 1988; Vater and Matthews, 2015) due to the high base saturation despite a low cation exchange capacity in the absence of a clay–humus complex (Matthews, 1992; Ugolini, 1966). On exposure from beneath the retreating glacier, the terrain may also be considered devoid of life and hence deglacierization represents the initiation of a true primary succession (Matthews, 1999; but see La Farge et al., 2013). However, microbial life may occur in subglacial sediments (Moiroud and Gonnet, 1975; Skidmore et al., 2000) and bryophytes have been known to survive glacial overriding and later exposure in proglacial areas (La Farge et al., 2013). Moreover, ancient carbon released from melting glacier ice may contribute to the food resources that are available for earlycolonizing microflora (Bardgett et al., 2007) and invertebrates (Hågvar and Ohlson, 2013), as well as for downstream microbial life (Singer et al., 2012). 6.3. Very early rapid geo-ecosystem changes (terrain age 0–6 years) Following six years of glacier retreat, the source of the first of the three water sources (glacier ice) becomes removed from the site but the latter two (snow and seasonally frozen ground) remain effective, at least in the spring. Thus, as terrain age increases, the substrate becomes better drained and consolidates (Boulton and Paul, 1976; Levy et al., 2015), it acidifies as a result of leaching, and other changes occur to sediment texture during the early development of the embryonic soil (Matthews, 1992). The most rapid changes to the texture of the substrate occurring in these early years are the large reduction in percentage fines and the large increase in pebbles at the surface (Fig. 4A). Down-washing of fine particles, especially silt, from the surface layers – the process of pervection (Paton, 1978) – has been widely recognised (Boulton and Dent, 1974; Frenot et al., 1995; Romans et al., 1980) and proceeds at its fastest rate within 10 years of deglacierization. This would further improve site drainage as well as leaving a lag deposit, in the form of a stone pavement at the surface. A similar effect may also be produced by frost sorting in response to freezing and thawing of the substrate (see below). However, an increase in the surface cover of pebbles over the very short time interval of six years is likely due mainly to the removal of the surrounding finer material by pervection, assisted by surface wash and wind deflation. Disturbance levels are likely to be at a maximum in the first few years of the chronosequence (Matthews, 1999). Saturation of the fines-rich sediment during spring snowmelt or summer rainstorms produces loss of strength and sediment flows can occur even over low-angle slopes (Lawson, 1982). This is likely to be the main process that degrades the annual moraines (cf. Sharp, 1984; Welch, 1970). Wetting and drying results in the state of the sediments alternating between a thixotrophic (porridge-like) condition in the spring and a hardened condition during summer drought. Additional disturbance may be attributed to the migration of meltwater channels and to frost heaving and frost sorting. Such high levels of disturbance are not conducive to colonization of the recently-deglacierized terrain by pioneer plants, which require some level of substrate stability in addition to an ability to reach the site. It is no surprise, therefore, that no higher or lower plants were recorded in the youngest sites of the chronosequence (Fig. 3A). This seems therefore, to rule out any major effect, at least at this initial stage, from the glacier acting as a collecting area for seeds and spores, which acts as a propagule bank that promotes plant succession on the glacier foreland (cf. Smith, 1993). Several invertebrate taxa are, however, present on terrain deglacierized for around 1 year (Fig. 3B). Collembola, in particular, are far more abundant on the youngest terrain than at any other sites. Although Collembola are flightless, they are highly mobile jumping micro-arthropods, can resist desiccation by moving into

225

micro-environments with high humidity, inhabit glaciers and icefields, and can be active under snow (Christiansen et al., 2009; Coulson and Midgley, 2012; Hågvar, 2010b). Their occurrence within a few years of deglacierization seems widespread (Hågvar, 2010a, 2012; Hodkinson et al., 2004; Kaufmann et al., 2002). The water-saturated environment of the most recently deglacierized terrain is therefore no barrier to this group and their extremely small size (~1 mm) certainly aids their dispersion by strong winds both close to the ground in the open landscape (Flø and Hågvar, 2013; cf. Coulson et al., 2003) and at higher levels in the atmosphere as part of the so-called ‘aerial plankton’ (Gressitt and Yoshimoto, 1974; Hågvar, 2012). Collembola presumably reproduce rapidly once they reach newly deglaciated terrain. According to Hågvar and Ohlson (2013) pioneer Collembola feed mainly on mosses or biofilm with diatom algae, the latter being the most likely on the youngest terrain. The smaller numbers of crawling Coleoptera and Arachnidae found on the youngest terrain (Fig. 3B) appear to exist largely independently of plant life, feeding on each other, Collembola, vagrant flying insects (such as Diptera and Hymenoptera) and/or wind-blown detritus (Hågvar, 2012). This constitutes the so-called ‘predator-first paradox’ (Hodkinson et al., 2001, 2002, 2004) whereby heterotrophs proceed autotrophs in succession. The analysis of the gut contents of pioneer species from glacier forelands in both Norway (Hågvar and Ohlson, 2013) and the Alps (Raso et al., 2014) support this proposition. Most of the species collected from our sites are carnivores (cf. Vater, 2012; Vater and Matthews, 2015), though Amara quenseli is an omnivore (Hågvar, 2012). The dwarf spiders (Erigone arctica and Erigone longipes) seem to be adapted to dispersal by ‘ballooning’ — i.e., release of silk threads, which are caught by the wind and may transport the spider over vast distances (Crawford and Edwards, 1986). 6.4. Unstable stone pavement with slowly developing cryptogamic crust (terrain age 6–21 years) Six years after deglacierization, the stone pavement is only partially formed. The proportion of cobbles and boulders in the pavement continues to increase slowly over the first 24 years of the chronosequence to a maximum of N 40% surface cover (Fig. 4A). Taking account of the cover of pebble-sized material, the total cover of stones at the surface on terrain ages between 6 and 21 years, remains more-or-less constant at 79–85%: on the younger terrain it is b50% and on older terrain it falls progressively from 65% to 46%. The steady rise in the cobble and boulder percentage is almost certainly due mainly to frost sorting, whereby large particles are raised towards the surface faster than smaller particles by ‘frost-pull’ during seasonal freezing and thawing of the ground (cf. Harris and Matthews, 1984). Relatively large particles adhere to lenses of segregation ice and are lifted as the ice lenses grow parallel to the ground surface during freeze-back. During subsequent thaw consolidation, the cobble or boulder is unable to settle back fully to its former position. Various types of patterned ground have been shown to develop by this and related processes at Storbreen and on other glacier forelands in Jotunheimen (Ballantyne and Matthews, 1982, 1983; Haugland, 2004, 2006; Matthews et al., 1998). Continuing instability of the ground surface is also indicated by two other observations: (1) the limited vegetation development (Fig. 3A) despite 19 species of higher plants colonizing within 12 years (Fig. 3C); and (2) the absence of visible epilithic lichens on the stones forming pavement surfaces up to 21 years (Fig. 4B). The relatively large number of higher plant species recorded suggests, moreover, that ability to tolerate the edaphic and climatic site conditions of the fresh soil and open, disturbed terrain, rather than specific dispersal adaptations, is the main factor affecting their establishment (cf. Ryvarden, 1971). These species are almost all ‘typical’ pioneers: small, perennial forbs and grasses adapted to rapid growth in a short growing season, with a high incidence of vegetative reproduction and/or seeds that are

226


easily dispersed by strong winds (Jumpponen et al., 1999; Matthews, 1978a, 1978b; Robbins and Matthews, 2009; Stöcklin and Bäumler, 1996; Whittaker, 1993). Low emergence rates and high seedling mortality rates result from the high levels of disturbance (cf. Helm and Allen, 1995; Marteinsdóttir et al., 2010; Mori et al., 2006). The most prominent aspect of vegetation development at this stage is the slowly developing cryptogamic crust (cf. Belnap and Lange, 2003; Breen and Lévesque, 2006, 2008; Worley, 1973), the cover of which rises from 3% but remains b 10% on terrain ages between 6 years and 21 years (Fig. 3A). Although the crust at Storbreen appears to consist mainly of mosses and has not been investigated in detail, it is likely also to include microbial assemblages of bacteria and blue-green algae, which have been shown to form raft-like, mucilaginous coatings on frost-disturbed deglacierized soils in the Antarctic (Davey and Rothery, 1993; Wynn-Williams, 1993). The cryptogamic crust is seen, therefore, as resisting disturbance as well as indicating the significant level of frost disturbance characterising the unstable stone pavement. The presence of such a crust may also aid the establishment of other components of the ecosystem, not only through ability to retain water, increase organic matter, trap fine mineral material, and fix nitrogen from the atmosphere and make it available to higher plants (Breen and Lévesque, 2008; Elbert et al., 2012; Schmidt et al., 2015) but also as a food source for Collembola (Hågvar and Ohlson, 2013). Amongst the invertebrates, the catches of Collembola plummet by an order of magnitude to b 100 individuals at terrain age 6 years and fall further to only 10 individuals at terrain age 21 years (Fig. 3B). This may be accounted for by the absence of standing water and the reduced moisture availability associated with the stone pavement but may also be affected by the somewhat higher numbers of predatory Coleoptera and arachnids, including species of the genera, Amara, Bembidion, Mitopus and Nebria (here including both Nebria nivalis and Nebria rufescens) which are common pioneers on glacier forelands in Norway and in the Alps (Kaufmann, 2001; Gobbi et al., 2006a; Bråten et al., 2009; Gereben-Krenn et al., 2011; Vater and Matthews, 2015) and include both specialists and generalists (Hågvar, 2012). However, Hågvar and Ohlson (2013) found that few Collembola were eaten by M. morio or N. nivalis at Hardangerjøkulen, southern Norway. Although the number of beetle and spider taxa rose from 5 to 8 on terrain ages of 6 and 12 years, respectively (Fig. 3C), and the total number of trapped individuals doubled to 30 (Fig. 3B), there are no general trends in the species number or surface activity of invertebrates with increasing terrain age across this part of the chronosequence. This may be accounted for by their continuing immigration, either as part of the aerial plankton or by crawling at ground level, or a failure to reproduce in the disturbed habitat with low resource availability. Moreover, the analysis of a limited number of traps with collections representing a limited period of time cannot fully describe the sparse macro-invertebrate fauna on pioneer ground. 6.5. Transition to stable stone pavement with rapid development of cryptogamic crust (terrain age 21–26 years) Between 21 and 26 years, there is a substantial increase in vegetation cover from 10% to N25%, most of which is accounted for by a steep increase in the area covered by cryptogamic crust (Fig. 4A). However, the other plant groups, the most important of which, in terms of cover, is the herbaceous perennials (12% maximum cover at 24 years) all seem to elicit a small response. Terricolous lichens, the moss R. canescens, and the woody shrub S. herbaceae notably appear for the first time (Fig. 3A; Table 1). Although there may be a small upturn in the species number of higher plant species (Fig. 3C), several of the relatively common pioneer herbs – particularly A. alpina, S. cespitosa and Poa vivipara – appear to exhibit a decline in cover (Table 1). These plant population changes, if real, are unlikely to be due to competition from other higher plant species because their plant cover is still very low and there is no reason to doubt sufficient safe sites remain available.

Although crust development may facilitate or inhibit particular species, such changes are perhaps more likely due to abiotic environmental changes. These include deflation, which is probably more important than on younger terrain because of reducing moisture availability (cf. Boulton and Dent, 1974; Munroe et al., 2015; Thorn and Darmody, 1980), and soil acidification as evidenced by the general tendency for pH to fall on terrain of increasing age (cf. Matthews, 1992; Messer, 1988; Vater and Matthews, 2015). Apart from the glacier harvestman (Opiliones), there is seemingly a parallel increase in the catches of individuals from the invertebrate groups – including the Collembola, beetles and spiders (Fig. 3B) – but with little increase in species richness (Fig. 3C). The upturn in Collembola numbers may be associated with the increasing availability of plant food, and the increasing numbers of Collembola may themselves provide food for increasing populations of the epigeal beetles and spiders, most of which are carnivores (Vater, 2012; Vater and Matthews, 2015). Thus, relatively complex food webs may be developing at this stage of the succession – or possibly earlier (cf. Hågvar and Ohlson, 2013). The patterns in the biota coincide with an increase in the stability of the stone pavement indicated by the uninterrupted and accelerating growth of crustose lichens on the stones themselves (Fig. 4B). The inferred increase in the diameter of thalli of the Rhizocarpon subgenus over this time interval (1.4 mm yr−1) is in full agreement with direct lichenometric growth rate measurements made in real time at Storbreen on stable moraine surfaces over the last 25 years (Trenbirth and Matthews, 2010). Furthermore, there is little change in the boulder and cobble cover (Fig. 4A), indicating reduced disturbance from the upheaval of relatively large particles, probably in response to continuing reduced moisture availability. At the same time, pebble cover is declining (Fig. 4A) as the smaller stones are increasingly overgrown by cryptogamic crust and other vegetation. 6.6. Diversification and spatial structuring of the geo-ecosystem (terrain age 26–33 years) Further increasing stability characterises the remaining part of the chronosequence where the greatest change amongst the plant groups is the increasing cover of R. canescens. The cover of this mat-forming moss reaches nearly 30% in a relatively dry and exposed area on one of the transects (Fig. 3A). On other transects, terricolous lichens (mainly S. alpinum), reach up to 12%, the herbaceous perennials up to 14% and the woody shrubs (mainly S. herbaceae and S. glauca) up to 4%. These plant groups spread at the expense of the cryptogamic crust which still covers up to 33%. As a result, the average vegetation cover of all groups (including crypotogamic crust) attains a value of about 50% on the oldest parts of the pioneer zone (Fig. 4A). Amongst the invertebrate groups, the Collembola and glacier harvestman (M. morio) appear to increase consistently in numbers across the chronosequence between 26 years and 33 years (Fig. 3B), in line with the increasing cover of R. canescens and the terricolous lichens (Fig. 3A). In contrast, the catches of individual beetles and spiders follow the pattern exhibited by the cryptogamic crust (and possibly the herbaceous perennials and woody shrubs) with peak values associated with terrain age 31 years. Although these differences could be affected by the small sample sizes, and therefore should be treated with care, the apparent existence of two different sets of temporal patterns is indicative of diversification of the geo-ecosystem. This is, in turn, interpreted as reflecting the development of a spatial mosaic of both floral and faunal components (cf. ‘habitat-binding’; Gereben, 1994, 1995). This spatial structuring can be linked to differences in the physical habitat in moisture availability, exposure and substrate texture. Apart from moss-eating Collembola (Hågvar, 2012), however, there seems to be little direct dependence between the invertebrate catches and the plant succession. As shown by Vater (2012) and Vater and Matthews (2015), most of the caught epigeal beetles and all the arachnids are carnivorous, with very few herbivorous or omnivorous


227

Fig. 5. Conceptual model of geo-ecological succession in the glacier–foreland pioneer zone. (A) Pictorial representation of interacting abiotic and biotic components of the geo-ecosystem across the chronosequence. (B) Schematic relative importance of major abiotic processes across the chronosequence. (C) Relative importance of major plant and invertebrate groups across the chronosequence. Four sub-zones, which also represent phases of succession, are shown as shaded columns across the three parts of the figure.

macroinvertebrate taxa involved at Storbreen or other Norwegian alpine glacier forelands. Nevertheless, as the pioneer ecosystem develops, more complex food webs and other interactions become possible (cf. Albrecht et al., 2010; Hågvar and Ohlson, 2013; König et al., 2011; Raso et al., 2014). 6.7. Synthesis: a geo-ecological model A conceptual model of pioneer-zone geo-ecological succession is summarized in Fig. 5A–C. We use the term ‘geo-ecological’ (rather than ecological) succession for several reasons. First, it emphasises the importance of abiotic driving forces, which operate alongside the traditional biotic driving forces of succession. Second, it explicitly includes the landscape context of the ecosystem. Third, it recognises the space-for-time substitution inherent in the chronosequence approach as applied to the glacier–foreland landscape. Thus, a geoecological model gives greater attention than an ecological model to both the geological and geographical aspects of succession. Our model focuses on inferred interactions between the abiotic and biotic components of the geo-ecological system as it evolves (Fig. 5A). Four major successional phases are recognised as different sub-zones: (1) an ‘unstable’ sub-zone for the first ~ 6 years after deglacierization; (2) a sub-zone of ‘active stone pavement’ (~ 6–21 years); a sub-zone of ‘transition’ (~ 21–26 years); and (4) a relatively stable ‘fast-developing’ sub-zone (~ 26 years and older). The pattern

and sequence can also be viewed as a complex gradient of largely abiotic disturbances (Fig. 5B) that interact with biological processes, such as dispersion and establishment, to drive the geo-ecosystem from an initially very high level of instability towards a steadily developing ecosystem (Fig. 5C). In the unstable sub-zone, initially saturated till and standing water are the dominant factors of the habitat and Collembola dominate the biotic element of the ecosystem. They clearly have no difficulty reaching the site, may be as part of the aerial plankton or by active migration. Their food is unknown, but Hågvar and Ohlson (2013) found that the pioneer species Agrenia bidenticulata living close to a receding glacier fed on diatom algae in biofilm. Epigeal beetles and dwarf spiders and plant propagules are also present, but the substrate is too disturbed for plants to establish. Thus, the ‘predator-first paradox’, highlighted by Hodkinson et al. (2002), can be supported and explained. As slopes stabilize, the sediment consolidates and soil moisture content declines, an overlapping sequence of abiotic processes – pervection, frost sorting and deflation – leads to the development of the active (in the sense of being initially unstable due to disturbance) stone pavement (Fig. 5B). Although these abiotic processes have been widely recognised on other glacier forelands, our model is the first attempt to indicate their changing rates in sequence. This evokes a varied biotic response. Cryptogamic crust dominated by tiny mosses develops slowly in the face of continuing disturbance of the substrate, and herbaceous perennials are now able to colonize a much more stable substrate

228


than in the previous sub-zone. Although there is a drastic reduction of Collembola numbers, possibly due to reduced moisture availability and/or predation by the moderate numbers of beetles, spiders and harvestmen that are present and appear to find shelter amongst the stones and cryptogamic crust. The transition sub-zone is triggered by the stone pavement becoming significantly less active as much of the fine matrix in the substrate has been removed by pervection, deflation (especially during periods of summer drought) and frost sorting, which is reducing in response to a combination of the removal of fines, reduced moisture and stone accumulation at the surface. The small increase in cover exhibited by Racomitrium moss, terrestrial lichens and shrubs (Fig. 5C), and the shift in species composition amongst the herbaceous perennials (Table 1), may all be accounted for by increasing acidity in response to continuing leaching under increasing stability combined with an increase in local seed production and dispersal. Cryptogamic crust, beetles and spiders seem to respond slightly quicker than Collembola, harvestmen and the other plant groups to these conditions (Fig. 5C). In the developing sub-zone, the trends identified in the preceding sub-zone continue at an accelerating rate under conditions of increasing stability as most disturbance processes are absent or continue to operate at a very low level (Fig. 5B). To use the terms introduced by Matthews (1999), direct glacial disturbance (caused by glacier contact) is no longer applicable, glacier-dependent disturbance (attributed to proximity of a glacier, such as erosion by glacial meltwater) and glacier-conditioned or paraglacial disturbance (attributed to the previous presence of a glacier, such as the high content of fines in a substrate susceptible to pervection and frost sorting) are much reduced. Furthermore, glacier-independent disturbance (unrelated to glaciers and hence not specific to deglacierized terrain, such as snow avalanches) appear to have been absent or ineffective (although they may occur in the future). On the oldest areas of the pioneer zone, therefore, spatial heterogeneity in the habitat takes over from disturbances as a major control on succession of both plants and invertebrates at particular sites. This enables the development of diverging successional trajectories, a mosaic of vegetation types and a variety of ecological niches for occupation by the invertebrates. The succession of plants and invertebrates appears, however, to take place in parallel. Although there is some evidence of interdependence – for example, the Collembola may eat mosses in the cryptogamic crust, and predators perhaps eat Collembola – there is little evidence of the formation of closely integrated biotic communities. 7. Conclusion (1) A novel, holistic approach has been applied to the chronosequence in the pioneer zone of the Storbreen glacier foreland. This emphasises the correlations and possible interactions between the plant and invertebrate elements of the biota, and biotic and abiotic components of the geo-ecosystem, and has led to the formulation of a conceptual geo-ecological model of the early stage of primary succession on terrain recently exposed by glacier retreat. Four subzones of the pioneer zone indicate four sub-stages of the pioneer stage: (i) unstable; (ii) active stone pavement; (iii) transition; and (iv) fast-developing ecosystem. (2) Initial conditions include the poorly-sorted, matrix-supported sediment (till) that is water saturated and consequently provides a highly unstable substrate. Pitfall trapping illustrates a very high initial surface activity of unidentified Collembola, and results in small catches of certain predatory macro-invertebrates (the beetles N. nivalis and Bembidion fellmanni and the dwarf spider E. arctica). However, plants are absent for several years until disturbance levels fall. (3) During the unstable sub-stage (0–6 years), drainage conditions are improving and a stone pavement starts to develop

with the rapid depletion of the fine matrix by downward percolation of water (pervection). After 6 years, catches of Collembola have already declined drastically accompanied by the first appearance of the carnivorous glacier harvestman (M. morio), a few more species of beetles, a diverse collection of isolated herbaceous perennial plants, and the early stages of a cryptogamic crust. Thus, there seems to be few restrictions on the ability of invertebrates or plant propagules to reach newly deglacierized terrain. (4) Six to 21 years after deglacierization, the active stone pavement is still developing while frost sorting leads to the further gradual build-up of cobbles and boulders in the surface layers. Continual disturbance results in little change to the low cover of herbaceous perennials or the catches of predatory epigeal invertebrates as the cryptogamic crust slowly increases its extent. The transitional sub-stage at 21–26 years after deglacierization is characterised by a more stable stone pavement, a small upturn in the cover of the cryptogamic crust and most other plants, and larger catches of invertebrate groups. (5) From 26–33 years, the fast-developing sub-zone exhibits further stabilization of the substrate, accelerating development and spatial differentiation of the ecosystem (notably now including R. canescens, terricolous lichens and woody shrubs) as the intensities of various disturbances fall further to very low levels. Total plant cover (including cryptogamic crust) increases considerably, catches of Mitopus moria increase steeply and catches of Collembola are resurgent, suggesting successful reproduction. (6) Geo-ecological succession in the pioneer zone of glacier forelands is therefore viewed as being driven by the interactions between abiotic and biotic factors and processes. Apart from the Collembola likely feeding on plant material, the successional trajectories of plants and invertebrates appear to be responding, largely independent of each other, to spatial variation and temporal changes in habitat conditions (such as moisture, exposure and substrate texture). Plant and invertebrate communities seem, therefore, to be developing with little evidence of the formation of highly integrated biotic communities.

Acknowledgements Fieldwork was carried out on the Swansea University Jotunheimen Research Expedition, 2011. We thank Mauro Gobbi and Adriano Zanetti for assistance with the identification of invertebrates, and Jennifer Hill and Sigmund Hågvar for constructive comments on the manuscript. Anna Ratcliffe prepared the figures for publication. This paper constitutes Jotunheimen Research Expeditions, Contribution No. 196. References Albrecht, M., Riesen, M., Schmid, B., 2010. Plant–pollinator network assembly along the chronosequence of a glacier foreland. Oikos 119, 1610–1624. Andreassen, L.M., Winsvold, H., 2012. Inventory of Norwegian Glaciers. Norwegian Water Resources and Energy Directorate (NVE), Oslo. Aune, B., 1993. Temperatur Normaler, Normalperiode 1961–1990. Den Norske Meterorologiske Institutt, Oslo (Rapport 02/93, in Norwegian). Ballantyne, C.K., Matthews, J.A., 1982. The development of sorted circles on recently deglaciated terrain, Jotunheimen, Norway. Arct. Alp. Res. 14, 341–354. Ballantyne, C.K., Matthews, J.A., 1983. Desiccation cracking and sorted polygon development, Jotunheimen, Norway. Arct. Alp. Res. 15, 339–349. Bardgett, R.D., Walker, L.R., 2004. Impact of coloniser plant species on the development of decomposer microbial communities following deglaciation. Soil Biol. Biochem. 36, 555–559. Bardgett, R.D., Bowman, W.D., Kaufmann, R., Schmidt, S.K., 2005. A temporal approach to linking aboveground and belowground ecology. Trends Ecol. Evol. 20, 634–641. Bardgett, R.D., Richter, A., Bol, R., Garnett, M.H., Bäumler, R., Xu, X., Lopez-Capel, E., Manning, D.A.C., Hobbs, P.J., Hartley, I.R., Wanek, W., 2007. Heterotrophic microbial communities use ancient carbon following glacial retreat. Biol. Lett. 3, 487–490. Belnap, J., Lange, O.L. (Eds.), 2003. Biological Soil Crusts: Structure, Function and Management. Springer, Berlin.

J.A. Matthews, A.E. Vater / Catena 135 (2015) 219–230 Boulton, G.S., Dent, D.L., 1974. The nature and rates of post-depositional changes in recently deposited till from south-east Iceland. Geogr. Ann. 56A, 135–145. Boulton, G.S., Paul, M.A., 1976. The influence of genetic processes on some geotechnical properties of glacial tills. Q. J. Eng. Geol. 9, 159–194. Bradley, J.A., Singarayer, J.S., Anesio, A.M., 2014. Microbial community dynamics in the forefield of glaciers. Proc. R. Soc. B 281, 20140882. http://dx.doi.org/10. 1098/rspb.2014,0882. Brambilla, M., Gobbi, M., 2014. A century of chasing the ice: delayed colonisation of icefree sites by ground beetles along glacier forelands in the Alps. Ecography 37, 33–42. Bråten, A.T., Flø, D., Hågvar, S., Hanssen, O., Mong, C.E., Aakra, K., 2012. Primary succession of surface active beetles and spiders in an alpine glacier foreland, central southern Norway. Arct. Antarct. Alp. Res. 44, 2–15. Breen, K., Lévesque, E., 2006. Proglacial succession of biological crusts and vascular plants: biotic interactions in the High Arctic. Can. J. Bot. 84, 1714–1731. Breen, K., Lévesque, E., 2008. The influence of biological crusts on soil characteristics along a High Arctic glacier foreland, Nunavut, Canada. Arct. Antarct. Alp. Res. 40, 287–297. Carlson, M.L., Flagstad, L.A., Gilet, F., Mitchell, E.A.D., 2010. Community development along a proglacial chronosequence: are above-ground and below-ground community structure controlled more by biotic than abiotic factors? J. Ecol. 98, 1084–1095. Christiansen, K.A., Bellinger, P., Janssens, F., 2009. Collembola (Springtails, Snow Fleas). In: Resh, V.H., Cardé, R.T. (Eds.), Encyclopedia of Insects, 2nd edition Academic Press, Amsterdam, pp. 206–210. Coulson, S.J., Midgley, N.G., 2012. The role of glacier mice in the invertebrate colonisation of glacial surfaces: the moss balls of the Fälljökull, Iceland. Polar Biol. 35, 1651–1658. Coulson, S.J., Hodkinson, I.D., Webb, N.R., 2003. Aerial dispersal of invertebrates over a high-Arctic glacier foreland: Midtre Lovénbreen, Svalbard. Polar Biol. 26, 530–537. Crawford, R.L., Edwards, J.S., 1986. Ballooning spiders as a component of arthropod fallout on snowfields of Mount Rainier, Washington, USA. Arct. Alp. Res. 18, 429–437. Crocker, R.L., Major, J., 1955. Soil development in relation to vegetation and surface age at Glacier Bay, Alaska. J. Ecol. 43, 427–448. Cutler, N.A., Belyea, L.R., Dugmore, A.J., 2008. The spatiotemporal dynamics of a primary succession. J. Ecol. 96, 231–246. Dahl, E., 1986. Zonation in arctic and alpine tundra and fellfield ecobiomes. In: Polumin, N. (Ed.), Ecosystem Theory and Application. Wiley, Chichester, pp. 35–62. Darmody, R.G., Allen, C.E., Thorn, C.E., 2005. Soil topochronosequences at Storbreen, Jotunheimen, Norway. Soil Sci. Soc. Am. J. 69, 1275–1287. Davey, M.C., Rothery, P., 1993. Primary colonization by microalgae in relation to spatial variation in edaphic factors in Antarctic fellfield soils. J. Ecol. 81, 335–344. Deevey, E.S., 1969. Coaxing history to conduct experiments. Bioscience 19, 40–43. Diamond, J., 1986. Overview: laboratory experiments, field experiments, and natural experiments. In: Diamond, J., Case, T.J. (Eds.), Community Ecology. Harper and Row, New York, pp. 3–22. Diamond, J., Robinson, J.A., 2010. Natural Experiments of History. Harvard University Press, Cambridge, MA. Egli, M., Wernli, M., Kneisel, C., Haeberli, W., 2006. Melting glaciers and soil development in the proglacial area Morteratsch (Swiss Alps): soil type chronosequence. Arct. Antarct. Alp. Res. 38, 499–509. Elbert, W., Weber, B., Burrows, S., Steinkamp, J., Büdel, B., Andreae, M.O., Pöschl, U., 2012. Contribution of cryptogamic covers to global cycles of carbon and nitrogen. Nat. Geosci. 5, 459–462. Etzelmüller, B., Hagen, J.O., 2005. Glacier–permafrost interaction in Arctic and alpine mountain environments with examples from southern Norway and Svalbard. In: Harris, C., Murton, J.B. (Eds.), Cryospheric Systems: Glaciers and Permafrost. Geological Society of London, Bath, pp. 11–27 (Geological Society Special Publication 242). Flø, D., Hågvar, S., 2013. Aerial dispersal of invertebrates and mosses close to a receding glacier in southern Norway. Arct. Antarct. Alp. Res. 45, 481–490. Førland, E.J., 1993. Nedbørnormaler, Normalperiode 1961–1990. Den Norske Meterorologiske Institutt, Oslo (Rapport 39//93, in Norwegian). Frenot, Y., Van Vliet-Lanoë, B., Gloaguen, J.-C., 1995. Particle translocation and initial soil development on a glacier foreland, Kerguelen Islands, Subantarctic. Arct. Alp. Res. 27, 107–115. Fukami, T., Wardle, D.A., 2005. Long-term ecological dynamics: reciprocal insights from natural and anthropogenic gradients. Proc. R. Soc. B 272, 2105–2115. Garibotti, I.A., Pissolito, C.L., Villalba, R., 2011. Spatiotemporal pattern of primary succession in relation to meso-topographic gradients on recently deglaciated terrain in the Patagonian Andes. Arct. Antarct. Alp. Res. 43, 555–567. Gereben, B.-A., 1994. Habitat-binding and coexistence of carabid beetles in a glacier retreat zone in the Zillertal Alps. In: Desender, K., Dufrene, M., Loreau, M., Luff, M.L., Maelfait, J.-P. (Eds.), Carabid Beetles: Ecology and Evolution. Kluwer, Dordrecht, pp. 139–144. Gereben, B.-A., 1995. Co-occurrence and microhabitat distribution of six Nebria species (Coleoptera: Carabidae) in an alpine glacier retreat zone in the Alps, Austria. Arct. Alp. Res. 27, 371–379. Gereben-Krenn, B.-A., Krenn, H.W., Strodl, M.A., 2011. Initial colonization of new terrain in an alpine glacier foreland by carabid beetles (Carabidae, Coleoptera). Arct. Antarct. Alp. Res. 43, 397–403. Gobbi, M., 2014. Application of the mean individual biomass of ground beetles (Coleoptera: Carabidae) to assess the assemblage successions along areas of recent glacier retreats. Eur. J. Entomol. 111, 537–541. Gobbi, M., De Bernardi, F., Pelfini, M., Rossaro, B., Brandmayr, P., 2006a. Epigean arthropod succession along a 154-year glacier foreland chronosequence in the Forni Valley (Central Italian Alps). Arct. Antarct. Alp. Res. 38, 357–362. Gobbi, M., Fontaneto, D., De Bernardi, F., 2006b. Influence of climate changes on animal communities in space and time: the case of spider assemblages along an alpine glacier foreland. Glob. Chang. Biol. 12, 1985–1992.

229

Gobbi, M., Rossaro, B., Vater, A., De Bernardi, F., Pelfini, M., Brandmayr, P., 2007. Environmental features influencing Carabid beetle (Coleoptera) assemblages along a recently deglaciated area in the Alpine region. Ecol. Entomol. 32, 682–689. Gobbi, M., Caccianiga, M., Cerabolini, B., De Bernardi, F., Luzzaro, A., Pierce, S., 2010. Plant adaptive responses during primary succession are associated with functional adaptations in ground beetles on deglaciated terrain. Community Ecol. 11, 223–231. Gressitt, J.L., Yoshimoto, C.M., 1974. Insect dispersal studies in northern Alaska. Pac. Insects 16, 11–30. Hågvar, S., 2010a. Primary succession of springtails (Collembola) in a Norwegian glacier foreland. Arct. Antarct. Alp. Res. 42, 422–429. Hågvar, S., 2010b. A review of Fennoscandian arthropods living on and in snow. Eur. J. Entomol. 107, 281–298. Hågvar, S., 2012. Primary succession on glacier forelands: how small animals conquer new land around melting glaciers. In: Young, S.S., Silvern, S.E. (Eds.), International Perspectives on Global Environmental Change. Intech Open Access Publisher, pp. 151–172 (Available at: http://www.intecopen.com). Hågvar, S., Ohlson, M., 2013. Ancient carbon from a melting glacier gives high 14C age in living pioneer invertebrates. Sci. Rep. 3, 2820. http://dx.doi.org/10.1038/srep02820. Hågvar, S., Solhoy, T., Mong, C.E., 2009. Primary succession of soil mites (Acari) in a Norwegian glacier foreland, with emphasis on orbatid species. Arct. Antarct. Alp. Res. 41, 219–227. Harris, C., Matthews, J.A., 1984. Some observations on boulder-cored frost boils. Geogr. J. 150, 63–73. Haugland, J.E., 2004. Formation of patterned ground and fine-scale soil development within two late Holocene glacial chronosequences: Jotunheimen, Norway. Geomorphology 61, 287–301. Haugland, J.E., 2006. Short-term periglacial processes, vegetation succession, and soil development within sorted patterned ground: Jotunheimen, Norway. Arct. Antarct. Alp. Res. 38, 82–89. Helm, D.J., Allen, E.B., 1995. Vegetation chronosequence near Exit Glacier, Kenai Fjords National Park, Alaska, U.S.A. Arct. Alp. Res. 27, 246–257. Hiemstra, J., Matthews, J.A., Evans, D.J.A., Owen, G., 2015. Sediment fingerprinting and the mode of formation of singular and composite annual moraine ridges at two southern Norwegian glaciers. The Holocene (in press). Hipp, T., Etzelmüller, B., Westermann, S., 2014. Permafrost in alpine rock faces from Jotunheimen and Hurrungane, southern Norway. Permafr. Periglac. Process. 25, 1–13. Hodkinson, I.D., Coulson, S.J., Harrison, J., Webb, N.R., 2001. What a wonderful web they weave: spiders, nutrient capture and early ecosystem development in the high Arctic — some counter-intuitive ideas on community assembly. Oikos 95, 349–352. Hodkinson, I.D., Webb, N.R., Coulson, S.J., 2002. Primary community assembly on land — the missing stages. Why are the heterotrophic organisms always first? J. Ecol. 90, 569–577. Hodkinson, I.D., Coulson, S.J., Webb, N.R., 2004. Invertebrate community assembly along proglacial chronosequences in the high Arctic. J. Anim. Ecol. 73, 556–568. Ingimarsdóttir, M., Caruso, T., Ripa, J., Magnúsdóttir, Ó.B., Miglioini, M., Hedlund, K., 2012. Primary assembly of soil communities: disentangling the effect of dispersal and local environment. Oecologia 170, 745–754. Johnson, E., Miyanishi, K., 2008. Testing the assumptions of chronosequences in succession. Ecol. Lett. 11, 419–431. Jones, C.C., del Moral, R., 2005a. Patterns of primary succession on the glacier foreland of Coleman Glacier, Washington, USA. Plant Ecol. 180, 105–116. Jones, C.C., del Moral, R., 2005b. Effects of microsite conditions on seedling establishment on the foreland of Coleman Glacier, Washington. J. Veg. Sci. 16, 293–300. Jones, C.C., del Moral, R., 2009. Dispersal and establishment both limit colonization during primary succession on a glacier foreland. Plant Ecol. 204, 217–230. Jones, G.A., Henry, G.H.R., 2003. Primary plant succession on recently deglaciated terrain in the Canadian High Arctic. J. Biogeogr. 30, 277–296. Jumpponen, A., Vare, H., Mattson, K.G., Ohtonen, R.S., Trappe, J.M., 1999. Characterization of ‘safe sites’ for pioneers in primary succession on recently deglaciated terrain. J. Ecol. 87, 98–105. Kaštovská, K., Elster, J., Stibal, M., Šantrůčková, H., 2005. Microbial assemblages in soil microbial succession after glacial retreat in Svalbard (High Arctic). Microb. Ecol. 50, 396–407. Kaufmann, R., 2001. Invertebrate succession on an alpine glacier foreland. Ecology 82, 2261–2278. Kaufmann, R., 2002. Glacier foreland colonisation: distinguishing between short-term and long-term effects of climate change. Oecologia 130, 470–475. Kaufmann, R., Fuchs, M., Gosterxeirer, N., 2002. The soil fauna of a glacier foreland: colonisation and succession. Arct. Antarct. Alp. Res. 34, 242–250. Kjøllmoen, B., 2011. Glaciological Investigations in Norway in 2010. In: Kjøllmoen, B. (Ed.)Norwegian Water Resources and Energy Directorate (NVE), Oslo (Report 2011: 3). Knelman, J.E., Legg, T.M., O'Neill, S.P., Washenberger, C.L., González, A., Cleveland, C.C., Nemergut, D.R., 2012. Bacterial community structure and function change in association with colonizer plants during early primary succession in a glacier forefield. Soil Biol. Biochem. 46, 172–180. König, T., Kaufmann, R., Scheu, S., 2011. The formation of terrestrial food webs in glacier foreland: evidence for the pivotal role of decomposer prey and intraguild predation. Pedobiologia 54, 147–152. La Farge, C., Williams, K.H., England, J.H., 2013. Regeneration of Little Ice Age bryophytes emerging from a polar glacier with implications of totipotency in extreme environments. Proc. Natl. Acad. Sci. 110, 9839–9844. Lawrence, L.R., Wardle, D.A., Bardgett, R.D., Clarkson, B.D., 2010. The use of chronosequences in studies of ecological succession and soil development. J. Ecol. 98, 725–736.

230


Lawson, D.E., 1982. Mobilization, movement and deposition of active subaerial sediment flows, Matanuska Glacier, Alaska. J. Geol. 90, 279–300. Levy, A., Robinson, Z., Krause, S., Waller, R., Weatherill, J., 2015. Long-term variability of proglacial groundwater-fed hydrological systems in an area of glacier retreat, Skeiđarársandur, Iceland. Earth Surf. Process. Landf. 40, 981–994. Lilleøren, K., Etzelmüller, B., Schuler, T.V., Ginås, K., Humlum, O., 2012. The relative age of mountain permafrost — estimation of Holocene permafrost limits in Norway. Glob. Planet. Chang. 92–93, 209–223. Lutro, O., Tveten, E., 1996. Geologisk kart over Norge, bergrunnskart Årdal M 1:250,000. Norges Geologiske Undersøkelse, Trondheim. (in Norwegian) Marteinsdóttir, B., Svavarsdóttir, K., Thórhallsdóttir, T., 2010. Development of vegetation patterns in early primary succession. J. Veg. Sci. 21, 531–540. Matthews, J.A., 1978a. Plant colonization patterns on a gletschervorfeld, southern Norway: a meso-scale geographical approach to vegetation change and phytometric dating. Boreas 7, 155–178. Matthews, J.A., 1978b. An application of non-metric multidimensional scaling to the construction of an improved species plexus. J. Ecol. 66, 157–173. Matthews, J.A., 1992. The Ecology of Recently-Deglaciated Terrain: a Geoecological Approach to Glacier Forelands and Primary Succession. Cambridge University Press, Cambridge. Matthews, J.A., 1999. Disturbance regimes and ecosystem response on recently-deglaciated substrates. In: Walker, L.R. (Ed.), Ecosystems of Disturbed Ground. Elsevier, Amsterdam, Amsterdam, pp. 17–37. Matthews, J.A., Shakesby, R.A., Berrisford, M.S., McEwen, L., 1998. Periglacial patterned ground on the Styggedalsbreen glacier foreland, Jotunheimen, southern Norway: microtopographic, paraglacial and geoecological controls. Permafr. Periglac. Process. 9, 147–166. Mellor, A., 1985. Soil chronosequences on Neoglacial moraine ridges, Jostedalsbreen and Jotunheimen, southern Norway: a quantitative pedogenic approach. In: Richards, K.S., Arnett, R.R., Ellis, S. (Eds.), Geomorphology and Soils. George Allen and Unwin, London, pp. 289–308. Messer, A.C., 1988. Regional variation in rates of pedogenesis and the influence of climatic factors on moraine chronosequences, southern Norway. Arct. Alp. Res. 20, 31–39. Moen, A., 1999. National Atlas of Norway: Vegetation. Norwegian Mapping Authority, Hønefoss. Moiroud, A., Gonnet, J.F., 1975. Jardins des Glaciers. Editions Allier, Grenoble (in French). Mori, A.S., Osono, T., Iwasaki, S., Uchida, M., Kanda, H., 2006. Topographical variation in initial recruitment and establishment of vascular plants and microhabitat conditions along a slope of the recently-deglaciated moraine in Ellesmere Island, High Arctic Canada. Polar Biosci. 19, 85–95. Mori, A.S., Osono, T., Uchida, M., Kanda, H., 2008. Changes in the structure and heterogeneity of vegetation and microsite environments with the chronosequence of primary succession on a glacier foreland in Ellesmere Island, High Arctic Canada. Ecol. Res. 23, 363–370. Mori, A.S., Uchida, M., Kanda, H., 2012. Non-stochastic colonization by pioneer plants after deglaciation in a polar oasis of the Canadian High Arctic. Polar Sci. 7, 278–287. Munroe, J.S., Attwood, E.C., O'Keefe, S.S., Quackenbush, P.J.M., 2015. Eolian deposition in the alpine zone of the Uinta Mountains, Utah, USA. Catena 124, 119–129. Nagy, E., Grabherr, G., 2009. The Biology of Alpine Habitats. Oxford University Press, Oxford. Nemergut, D.R., Anderson, S.P., Cleveland, C.C., Martin, A.P., Miller, A.E., Seimon, A., Schmidt, S.K., 2007. Microbial community succession in an unvegetated, recently deglaciated soil. Microb. Ecol. 53, 110–122. Nicol, G.W., Tscherko, D., Embley, T.M., Prosser, J.I., 2005. Primary succession of soil Crenarchaeota across a receding glacier foreland. Environ. Microbiol. 7, 337–347. Ohtonen, R., Fritze, H., Pennanen, T., Jumpponen, A., Trappe, J., 1999. Ecosystem properties and microbial community changes in primary succession on a glacier forefront. Oecologia 119, 239–246. Paton, T.R., 1978. The Formation of Soil Material. George Allen and Unwin, London. Pickett, S.T.A., 1988. Space-for-time substitution as an alternative to long-term studies. In: Likens, G.E. (Ed.), Long-term Studies in Ecology: Approaches and Alternatives. Springer, New York, pp. 110–135. Prach, K., Rachlewicz, G., 2012. Succession of vascular plants in front of retreating glaciers in central Spitsbergen. Polish Polar Res. 33, 319–328. Raffl, C., Mallaun, M., Mayer, R., Erschbaumer, B., 2006. Vegetation succession pattern and diversity changes in a glacier valley, Central Alps, Austria. Arct. Antarct. Alp. Res. 38, 421–428. Raso, L., Sint, D., Mayer, R., Plangg, S., Recheis, T., Brunner, S., Kaufmann, R., Traugott, M., 2014. Intraguild predation in pioneer predator communities of alpine glacier forelands. Mol. Ecol. 23, 3744–3754. Robbins, J.A., Matthews, J.A., 2009. Pioneer vegetation on glacier forelands in southern Norway: emerging communities? J. Veg. Sci. 20, 889–902.

Robbins, J.A., Matthews, J.A., 2010. Regional variation in successional trajectories and rates on glacier forelands in south-central Norway. Arct. Antarct. Alp. Res. 42, 351–361. Robbins, J.A., Matthews, J.A., 2014. Use of ecological indicator values to investigate successional change in boreal to high-alpine glacier–foreland chronosequences, southern Norway. The Holocene 24, 1453–1464. Romans, J.C.C., Robertson, L., Dent, D.L., 1980. The micromorphology of young soils from south-east Iceland. Geogr. Ann. 62A, 93–103. Ryvarden, L., 1971. Studies in seed dispersal I. Trapping of diaspores in the alpine zone at Finse, Norway. Nor. J. Bot. 18, 215–226. Schmidt, S.K., Reed, S.C., Nemergut, D.R., Grandy, A.S., Cleveland, C.C., Weuintraub, M.N., Hill, A.W., Costello, E.K., Meyer, A.F., Neff, J.C., Martin, A.M., 2015. The earliest stages of ecosystem succession in high-elevation (5000 metres above sea level), recently-deglaciated soils. Proc. R. Soc. B 275, 2793–2802. Sharp, M., 1984. Annual moraine ridges at Skálafellsjökull, south-east Iceland. J. Glaciol. 30, 82–93. Sigler, W.V., Zeyer, J., 2002. Microbial diversity and activity along the forefields of two receding glaciers. Microb. Ecol. 43, 397–407. Singer, G.A., Fasching, C., Wilhelm, L., Niggemann, J., Steier, P., Dittmar, T., Battin, T.J., 2012. Biogeochemically diverse organic matter in alpine glaciers and its downstream fate. Nat. Geosci. 5, 710–714. Skidmore, M.L., Foght, J.M., Sharp, M.J., 2000. Microbial life beneath a High Arctic glacier. Appl. Environ. Microbiol. 66, 3214–3220. Skubała, P., Gulvik, M., 2005. Pioneer oribatid mite communities (Acari, Oribatida) in newly exposed natural (glacier foreland) and anthropogenic (post-industrial dump) habitats. Pol. J. Ecol. 53, 395–407. Smith, R.I.L., 1993. The role of bryophyte propagule banks in primary succession: case study of an Antarctic fellfield soil. In: Miles, J., Walton, D.W.H. (Eds.), Primary Succession on Land. Blackwell Scientific Publications, Oxford, pp. 55–78. Stevens, P.R., Walker, T.W., 1970. The chronosequence concept and soil formation. Q. Rev. Biol. 45, 333–350. Stöcklin, J., Bäumler, E., 1996. Seed rain, seedling establishment and clonal growth strategies on a glacier foreland. J. Veg. Sci. 7, 45–56. Thorn, C.E., Darmody, R.G., 1980. Contemporary aeolian sediments in alpine zone, Colorado Front Range. Phys. Geogr. 1, 162–171. Thorn, C.E., Darmody, R.G., Allen, C.E., 2008. Ground temperature variability on a glacier foreland, Storbreen, Jotunheimen, Norway. Nor. Geogr. Tidsskr. 62, 290–302. Trenbirth, H.E., Matthews, J.A., 2010. Lichen growth rates on glacier forelands in southern Norway: preliminary results from a 25-year monitoring programme. Geogr. Ann. 92A, 19–39. Tscherko, D., Rustemeier, J., Richter, A., Wanek, W., Kandeler, E., 2003. Functional diversity of the soil microflora in primary succession across two glacier forelands in the central Alps. Eur. J. Soil Sci. 54, 685–696. Tscherko, D., Hammesfahr, H., Zeltner, G., Kandeler, E., Böcker, R., 2005. Plant succession and rhizosphere microbial communities in a recently deglaciated alpine terrain. Basic Appl. Ecol. 6, 367–383. Ugolini, F.C., 1966. Soils. In: Mirsky, A. (Ed.), Soil Development and Ecological Succession in a Deglaciated Area of Muir Inlet, Southeast Alaska. State University Research Foundation, Columbus, Ohio, pp. 29–72. Vater, A.E., 2012. Insect and arachnid colonization on the Storbreen glacier foreland, Jotunheimen, Norway: persistence of taxa suggests an alternative model of succession. The Holocene 22, 1123–1133. Vater, A.E., Matthews, J.A., 2013. Testing the ‘addition and persistence’ model of invertebrate succession on a subalpine glacier–foreland chronosequence, Fåbergstølsbreen, southern Norway. The Holocene 23, 1151–1162. Vater, A.E., Matthews, J.A., 2015. Succession of pitfall-trapped insects and arachnids on eight Norwegian glacier forelands along an altitudinal gradient: patterns and models. The Holocene 25, 108–129. Vilmundardóttir, O.K., Gísladóttir, G., Lal, R., 2014. Early stage development of selected soil properties along the proglacial moraines of Skaftafellsjökull glacier, SE-Iceland. Catena 121, 142–150. Walker, L.R., del Moral, R., 2003. Primary Succession and Ecosystem Rehabilitation. Cambridge University Press, Cambridge. Welch, D.M., 1970. Substitution of space for time in a study of slope development. J. Geol. 78, 234–239. Whittaker, R.J., 1993. Plant population patterns in a glacier foreland succession: pioneer herbs and later-colonizing shrubs. Ecography 16, 117–136. Worley, I.A., 1973. The “black crust” phenomenon in upper Glacier Bay, Alaska. Northwest Sci. 47, 20–29. Wynn-Williams, D.D., 1993. Microbial processes and initial stabilization of fellfield soil. In: Miles, J., Walton, D.W.H. (Eds.), Primary Succession on Land. Blackwell Scientific Publications, Oxford, pp. 17–32.