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Community assembly following glacier regression in the high Arctic is poorly understood and quantitative studies documenting the development of communities along proglacial chronosequences are surprisingly absent. The importance of allochthonous energy and nutrients (living invertebrates and wind-blown detritus) for initial colonization of new substrates, in the high Arctic and elsewhere was emphasized recently (Hodkinson et al. 2001; Hodkinson, Webb & Coulson 2002). This paper describes the subsequent assembly of invertebrate communities on proglacial chronosequences at Kongsfjord, W. Spitsbergen, Svalbard, for which soil and plant community development are already characterized (Hodkinson, Coulson & Webb 2003). Outside the high Arctic, soil development and plant succession on glacier forelands is investigated widely (Matthews 1992; Chapin et al. 1994) but, with the exception of studies on Rotmoos Glacier, Austria (Kaufmann 2001, 2002; Kaufmann & Raffl 2002; Kaufmann, Fuchs & Gosterxeier 2002), detailed data on animal community assembly along glacial chronosequences are lacking. Limited data, however, are available for selected groups such as spiders (Zingerle 1999). By contrast, community assembly on other newly exposed substrates has been studied widely, usually at lower latitudes (e.g. Lindroth et al. 1973; Majer 1989; Ashmole et al. 1992; Miles & Walton 1993; Crawford, Sugg & Edwards 1995; Hodkinson et al. 2002).
Our primary objectives were to describe, measure and model patterns and rates of invertebrate community assembly following glacial retreat, using selected proglacial areas of known chronology. In particular, we tested three linked hypotheses, namely that (1) invertebrate community assembly is deterministic and directional and therefore predictable; (2) invertebrate succession is linked inextricably to plant community and soil development and (3) dispersal, linked to ecophysiological adaptability, is a rate-limiting factor for invertebrate community assembly.
Community assembly for a 1900-year chronosequence along the proglacial area of a land-terminating glacier, the Midtre Lovénbre, was compared with that (over c. 1000 years) on the nearby Lovén Islands (see Hodkinson et al. 2003). These small islands in Kongsfjord were released successively from beneath the ice during the regression of the main valley glacier, the Kongsbre. They lie 3 km from the mainland shore and are separated by c. 1 km of open water. Midtre Lovénbre communities developed on bare nutrient-poor moraines in proximity to the cooling effect of a large glacier but with unrestricted access to colonizing organisms from adjacent areas. The ‘isolated’ Lovén Island communities, by contrast, developed on glacial diamicton, receiving significant nutrient enrichment from surrounding marine ecosystems (Alsos, Elvebakk & Gabrielsen 1998; Hodkinson et al. 2003).
Sites (Table 1) were adjacent to Ny-Ålesund, Kongsfjord, West Spitsbergen, Svalbard. On Midtre Lovénbre foreland, seven sampling plots (approx. 20 × 30 m), were established at roughly equal distances along a transect of 1·7 km across the proglacial area. Starting at the glacier snout, sites 1–5 lay on the moraine, site 6 on the sandur below the terminal moraine and site 7 a little to one side on a raised rock ridge beyond the sandur. Plot 7 was relatively undisturbed by recent glaciation (Hodkinson et al. 2003). The Lovén islands chronosequence comprised sites on three islands, Storholmen, Midtholmen and Leirholmen. Each island plot (approximately 30 m diameter) was situated on the shallow down slope below the crest of the island. For both chronosequences plant cover, plant species richness, depth of soil organic horizon, percentage soil organic matter, soil nitrogen and soil moisture increased over time, whereas soil pH and average soil particle size decreased (Hodkinson et al. 2003). By contrast with the oldest Midtre Lovénbre site, the oldest Lovén Islands sites had a slightly lower vascular plant species richness and higher Bryophyte cover: the dominant species, nevertheless, tended to remain the same. Organic soil depth, however, was greater on the Lovén Islands, resulting presumably from nutrient enrichment and impeded drainage. Table 1 gives locations, altitudes and ages of sites and plots. Plot ages were estimated from land-based and aerial photography, coupled with radiocarbon dating of soil organic matter (Hodkinson et al. 2003).
Table 1. Study sites on Kongsfjord, Spitsbergen, Svalbard. Sites were aged in 2000 by either aerial/ground photography (P) or radiocarbon dating (RC); see Hodkinson et al. (2003) for full details
| Midtre Lovénbre 7||N 78°54·534′||bp 1926–1820|
|E 12°04·537′|| |
| Midtre Lovénbre 6||N 78°54·200′||150|
|E 12°06·763′|| |
| Midtre Lovénbre 5||N 78°54·082′||100|
|E 12°06·339′|| |
| Midtre Lovénbre 4||N 78°53·984′||60|
|E 12°06·085|| |
| Midtre Lovénbre 3||N 78°53·816′||37|
|E 12°05·590′|| |
| Midtre Lovénbre 2||N 78°53·704′||16|
|E 12°05·262′|| |
| Midtre Lovénbre 1||N 78°53·653′||2|
|E 12°04·797′|| |
| Storholmen (S)||N 78°55·860′||bp 968–926|
|E 12°13·617′|| |
| Midtholmen (M)||N 78°55·914′||bp 1174–1058|
|E 12°18·156′|| |
| Leirholmen (L)||N 78°55·215′||100|
| ||E 12°20·285′|| |
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Several techniques were used to sample invertebrates. Four-centimetre-diameter cores were taken randomly in late July 2000 from within each plot (n = 40 or 20 per plot for Midtre Lovénbre and Lovén Islands, respectively) and extracted for soil microarthropods using modified Macfadyen high gradient heat extractors (Leinaas 1978). Parallel sets of identical soil cores (n = 20 per plot) were extracted for Enchytraeidae and larval Chironomidae using wet funnel extraction (O’Connor 1962). On the shallow soils (< 4 cm depth) of Midtre Lovénbre and Leirholmen each core, comprising the top 4 cm of substrate containing a complete soil profile, was inverted before extraction. On the deeper organic soils of Midtholmen and Storholmen (> 4 cm) cores were divided horizontally before extraction. Midtre Lovénbre and Lovén Island sites were sampled in mid July to early August 2000 and 2001, respectively.
Pitfall and yellow sticky traps provided additional data on species present. Water-filled pitfall traps (5 cm diameter, 3 × 5 per site, 1 m spacing) were operated continuously from 16 July to 3 August 2000 on Midtre Lovénbre plots and from 17 July to 6 August 2001 on the Lovén Islands plots. Yellow sticky traps (double-sided, each area 400 cm2, 4 per plot) were operated continuously from 17 July to 6 August on 2001 on Midtre Lovénbre (Coulson et al. 2003a).
Species richness of soil testate amoebae was obtained from six soil cores per plot on Midtre Lovénbre. Soils were homogenized and subsamples examined on glass slides under a compound microscope. Numbers of species found during a 2-h search of six slides per plot were recorded. Lower than expected species richness at sites 6 and 7 was confirmed by examining four extra slides for 1 h.
Canonical correspondence analysis (CCA) was used to examine relationships between invertebrate community composition and site variables. Models based on linear regression were not significantly different from those using polynomial relationships (Makerenkov & Legendre 2002) and results presented use the linear model. CCA graphs were plotted using the Multivariate Statistical Package (mvsp) 3·1. (Kovach Computing Services). Species present at one site only were excluded from the analysis. CCA models, along orthogonal axes, the distribution of animal species (response variables) across sites with respect to environmental data for each site (explanatory variables). Results are displayed as diagrams plotting the correspondence (proximity) of species and sites to vector lines representing the explanatory variables. The closer the proximity, the greater the effect of that vector in determining the species distribution. Analyses are based on six explanatory variables, chronological age of site, soil surface pH, percentage vegetation cover, percentage cover by blue-green bacteria, plant species richness and percentage organic matter (OM) in the top 4 cm of soil. Variables are described fully in Hodkinson et al. (2003). The list was optimized from a larger set in which several variables, such as soil depth, soil moisture, soil clast size and soil nitrogen were serially correlated with those used. Adding these extra variables had minimal effect on the variation explained.
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One problem in chronosequence studies that substitute space for time (Pickett 1989) is that prevailing conditions at any location have probably varied over the long time scales involved. For example, Kaufmann (2002) demonstrated faster community development on Rotmoos Glacier foreland over the last 30 y compared with the previous 30–50 years, linked to marginally warmer temperatures. Another confounding factor is rapid colonization of glacier forelands from lateral vegetated areas, as occurs on Rotmoos. Lack of such areas around Midtre Lovénbre, however, reduces this possibility significantly for soil animals, at least at sites 1–5, where the direction of colonization most probably corresponded with the long time axis of the chronosequence. Furthermore, because of low community diversity, there was little evidence of strong topographical variation in community composition at sites of equivalent age, as evident on Rotmoos (Kaufmann & Raffl 2002). Despite such potential limitations chronosequences provide unique insights into community assembly that cannot be replicated by short-term experimentation.
Time scales for community assembly were slow, reflecting harsh environmental conditions extending over hundreds to thousands of years, longer by an order of magnitude than most studies elsewhere (Matthews 1992). Nevertheless, the composition of animal communities developing on Midtre Lovénbre and Lovén Island chronosequences were broadly similar, despite their contrasting histories and situations. Thus the fauna of Leirholmen after 100 years corresponded closely with that of Midtre Lovénbre site 5, paralleling the established similarities in the soil and vegetation (Hodkinson et al. 2003). Thus I. anglicana, F. quadrioculata, Hypogastrura spp., C. anomia and T. velatus were the dominant soil microarthropods, H. spetsbergensis and E. psychrophila the dominant spiders, S. groenlandicus and A. pusillus the dominant parasitoids and Enchytraeidae and terrestrial chironomids were present. Differences included the substitution of H. tullbergi by H. viatica on Leirholmen and the absence of some of the common Midtre Lovénbre species, such as S. inaequalis and E. arctica. These latter species, nevertheless, were present on the older islands. Similarly, the faunas of Midtholmen and Storholmen largely mirrored that of site 7, but lacked some minor species. Common additional elements included the herbivores P. amentorum and A. svalbardicum, together with the parasitoids I. hyperboreus, D. bifoveatus, D. rapae and Alloxysta sp., the spider H. glacialis, the syrphid P. tarsatus and the microarthropods H. reticulata and O. neerlandica. Lovén Island communities contained many flightless species that have dispersed effectively across the marine water barrier to and between islands over the last 100–1000 years (Coulson et al. 2002). Some apparently more sedentary soil-dwelling microarthropod species, however, such as F. bisetosa, O. groenlandicus, M. sarekensis, C. hoeli and a Brachythonius sp., together with parasitoids such as A. borealis, G. glacialis and S. lineiger, were absent from island samples. Enchytraeidae and F. quadrioculata, were significantly more abundant on the older islands than on Midtre Lovénbre, probably reflecting their better exploitation of deeper, moister organic soils.
Colonization rates by testate amoebae on Midtre Lovénbre contrasted strongly with those for volcanic tephra on Deception Island, South Shetland (Smith 1985). Difflugia sp. occurred within 1 year and three species were present after 60 years compared with the elapse of 150 years before first colonization of unfavourable sites on Deception. The apparent decline in species richness between sites 5–7 is, however, difficult to explain.
In addition to variations between chronosequences, more subtle differences may occur within species populations across the chronosequence. Varying population age structure of H. tullbergi across Midtre Lovénbre may thus result from poor recruitment related to low food availability and high desiccation stress, to which hatching Collembola are particularly susceptible (Birkemoe & Leinaas 1999). Alternatively, it may reflect differential dispersal of mature animals from favourable adjoining sites (Johnson & Wellington 1983; Hertzberg 1997; Hertzberg & Leinaas 1998). Mature Collembola often have a greater tendency to disperse than juveniles.
The chronosequences chosen showed strong directional trends for several factors and it is unsurprising that these often emerged as good predictors of species distributions. Factors linked positively to site age, or distance from the glacier, included soil OM, moisture, depth, clast size and total nitrogen as well as vegetation cover and vascular plant species richness. Other factors, such as cyanobacteria cover, were less dependent on site age. Together these factors provide the environmental template for invertebrate colonization. Community assembly is, however, complex depending on the interplay between the ecology, ecophysiology and dispersal characteristics of individual species. Eight categories of colonizers, each with their characteristic demands can be recognized, namely:
Species independent of vascular plant establishment.
Includes surface-active species subsisting on allochthonous inputs of prey items or organic detritus. These are the first colonizers, including spiders such as H. spetsbergensis
, M. nigripes
and E. psycrophila
and darker pigmented Collembola with protective pigmentation such as I. anglicana
, S. inaequalis
and H. tullbergi
. Species are often highly dispersive and show some drought resistance (Hodkinson et al. 1996a
; Coulson et al. 2002
). The mite C. anomia
is an exception that is slow-moving but it is, nevertheless, highly robust and drought-resistant and may be dispersed passively by other agencies (Hodkinson et al. 1996a
; Coulson et al. 2002
). These Collembola and mite species may feed on cyanobacteria or lichens as they become available.
Species dependent on soil formation linked to plant growth
. Includes Enchytraeidae and some soil-dwelling Collembola, such as O. groenlandicus
and F. bisetosa
. These are desiccation-susceptible species requiring deeper moist soils with a high organic content that tended to occur at older sites (Byzova, Uvarova & Petrova 1995
; Hodkinson et al. 1996a
; Birkemoe, Coulson & Sømme 2000
Species dependent on cyanobacteria or lichen cover
. Embraces mites such as T. velatus
and D. notatus
whose population peaks corresponded with the maximum cover by blue-green bacteria or lichen. These are again desiccation=resistant surface-dwelling species (Hodkinson et al. 1996a
Species dependent on colonization by the host plant.
Obligate herbivores whose appearance corresponded with the first colonization by their plant host. Included P. amentorum
on S. polaris
and A. svalbardicum
on D. octopetala
(Strathdee & Bale 1995
Specialized predators/parasitoids/hyperparasitoids dependent on resident host species
. Includes species such as I. hyperboreus
, S. lineiger
, D. bifoveatus
, D. rapae
sp.and P. tarsatus
associated with obligatory prey. Other species such as A. borealis
and G. glacialis
are associated more closely with spider species and were distributed more broadly (Coulson et al. 2003a
Less specific general predators dependent on general availability of prey. Includes predatory mites that reflect the abundance of potential prey species such as F. quadrioculata. This may give the misleading impression in CCA that prey and predator are responding similarly to the same environmental variables.
Poor dispersers. Species occurring only in the oldest soils and having poor dispersal powers, being apparently absent from sites, where on the basis of similar soil characteristics they might be expected to occur. Includes the mites H. reticulata, C. hoeli and O. neerlandica.
Vagrants. Species of unknown biology that are not permanently resident, e.g. allochthonous Chironomidae that may be present at any site at any time.
Thus, the concept of facilitation, used widely in plant succession (McCook 1994; Callaway & Walker 1997), is equally applicable to animal community assembly. Some species are facilitated by the presence of specific plants, others by the presence of suitable animal hosts. Some require no facilitation, yet others require long-term general facilitation through soil development associated with plant growth.
Patterns of invertebrate community assembly observed parallel those elsewhere, on diverse substrates from mine spoil, polder, mud, scree, glacial moraine, landfill to volcanic lava and ash. Despite the apparent lack of a deep species pool, the same functional groups of species were the first to colonize, namely spiders, surface-active Collembola and desiccation-resistant mites (cf. Meijer 1980; Hutson 1980; Moore & Luxton 1986; Crawford et al. 1995; Judd & Mason 1995; Thornton 1996; Mrzljak & Wiegleb 2000; Kaufmann 2001; Hodkinson et al. 2002; Kaufmann et al. 2002). The main elements missing were surface-active predatory beetles, such as Carabidae, and larger scavenging orthopteroid insect orders sometimes found in the tropics and elsewhere.
High Arctic terrestrial ecosystems have low net primary productivity (< 140 g C m−2 year−1) and low vascular plant species richness, with an essentially two-dimensional vegetation structure (Bliss & Matveyeva 1992). Ecological theory predicts low diversity communities with relatively simple food chains and low connectivity (Bazely & Jefferies 1997; Morin 1999). Is this realized? The food web is dominated by detritivore and omnivores throughout community assembly, with herbivores of vascular plants relatively late entrants, such that they are unlikely to impact significantly on the early direction of plant succession as observed elsewhere (Brown & Gange 1992). However, the food web, particularly at the older sites, is surprisingly complex (cf. Summerhayes & Elton 1923). It comprises relatively high proportions of hymenoperous parasitoids, some hyperparasitoids and a complex of predators, including several spider species, some gamasid and prostigmatic mites and an aphidophagous syrphid. Several larger Hymenoptera were captured at densities that appear to exceed those of their potential prey (Coulson et al. 2003a). This raises the question of how the system sustains such extended food chains with an apparently high parasite/predator loading. The answer appears to lie in the spatial structure of the community and the vagility of parasitoids. The low diversity of plant species produces an extensive vegetation mosaic of relatively uniform species composition. Some prey species exist at low densities across this mosaic and their location requires widespread searching, particularly by the larger parasitoids. Trap catches reflect aggregate numbers of vagile parasitoids searching through the area rather than the absolute numbers present at one time. Furthermore, allochthonous inputs of both insects and detritus provide significant further continuing subsidies to the terrestrial food web in areas of low productivity (Polis et al. 1997; Hodkinson et al. 2002).
Returning to our initial hypotheses, the evidence suggests that community assembly was both deterministic and directional (Ward & Thornton 2000), with similar common predictable patterns, involving common suites of species, across both chronosequences. This relates to species requirements as listed previously, which determine their point of entry into the community. However, as for the plant community (Hodkinson et al. 2003) it is difficult to distinguish between chance and determinism by default, when the community progressively recruits from a limited pool of effectively dispersed species. Kaufmann (2002) reached similar conclusions for his more complex community on Rotmoos Glacier foreland − that community assembly was an ordered and predictable process linked to the varying biologies and tolerances of the colonizing species. Nevertheless, several earlier colonizers exist independently of vascular plants and soil development. Later colonizers depend more directly on characteristics of the developing soil or the presence of particular plant types or species, which facilitate their establishment.
Another conclusion common with the Rotmoos study is that for the more abundant invertebrates rates of dispersal do not appear seriously to limit colonization (Kaufmann 2001; Kaufmann et al. 2002). This is evidenced by the fact that the colonization is almost instantaneous. For many other species requiring facilitation, colonization of three separate islands 3 km from the mainland did not present an insurmountable barrier given the time scales involved, and there was high commonality of species at comparable successional stages. Several species survive extended passage on or in seawater (Coulson et al. 2002) and only in the case of the less common soil-dwelling microarthropods restricted to Midtre Lovénbre site 7 does weak dispersal ability appear to limit their realized distribution.
Invertebrate community assembly on proglacial chronoseqences in the High Arctic thus shares many common features with successions elsewhere, but with a greatly extended time scale. This raises concern over the long-term vulnerability of these isolated island communities when subjected to rapidly accelerating climate change. Future change will almost certainly occur more rapidly than in the past (IPCC 2001).