**6. The predator first- hypothesis**

According to conventional ecological textbooks, a primary succession should start with the establishment of plants. These would offer life conditions for herbivore animals, which finally allow the presence of predators. Hodkinson et al. (2002) showed that in practice, newly exposed substrates, as a fresh glacial moraine or a cooled volcanic lava flow, are to a large degree inhabited by various predator invertebrates. In other words, the autotrophs are preceded by a largely unrecognized heterotrophic phase. Summing up literature documenting aerial transport and deposition of invertebrates, they assumed that pioneer predators were fed by a fallout of invertebrates onto land and water surfaces (Figs. 6-7). In adition, a fallout of detritus would favour scavenging detritivores. It was suggested that these heterotrophic communities conserve nutrients, particularly nitrogen, and facilitate the establishment of green plants. In a glacier foreland on Svalbard, Hodkinson et al. (2001) showed that spider densities were highly correlated with allochthonous inputs of potential prey items, predominantly chironomid midges. Coulson et al. (2003) further documented aerial transport of invertebrates in the same foreland.

Pioneer species with a short life cycle might have an advantage compared to species with a long life cycle in establishing a high and permanent population. Most of the typical pioneer springtail species in alpine south Norway have a one-year life cycle, which is relatively "fast" under these conditions (Fjellberg, 1974; Hågvar, 2010). However, the pioneer oribatid mite *Tectocepheus velatus*, is assumed to use two or more years to fulfil the life cycle in the same area (Solhøy, 1975). This species was represented mainly with juveniles in the pioneer site at Hardangervidda, indicating local reproduction (Hågvar, 2010). For this species, a

slow development does not seem to be a handicap in colonisation and establishment.

High densities of pioneer microarthropods could be due to continuous transport by air. Theoretically, the pioneer ground might be an ecological sink, receiving animals which continuously die. However, filled guts in sampled microarthropods indicate feeding activity on the pioneer ground. Whether pioneer ground may to a large degree be a sink for

In a glacier foreland in the Austrian Alps, Bardgett et al., (2007) found that pioneer, heterotrophic microbial communities to a large degree used ancient carbon released by the glacier as an energy source. Only after more than 50 years of organic matter accumulation did the soil microbial community change to one supported primarily by modern carbon, most likely from recent plant production. This means that also pioneer microarthropods feeding on fungi and bacteria could use ancient carbon, allowing microarthropods to establish resident populations immediately after the ground is laid free of ice. Inblown organic material will also gradually add substrate for saprophagous food chains. Microbialfeeding animals like microarthropods, rotatoria, tardigrada, nematoda and enchytraeidae may be the first animals which establish viable and resident populations independently of

According to conventional ecological textbooks, a primary succession should start with the establishment of plants. These would offer life conditions for herbivore animals, which finally allow the presence of predators. Hodkinson et al. (2002) showed that in practice, newly exposed substrates, as a fresh glacial moraine or a cooled volcanic lava flow, are to a large degree inhabited by various predator invertebrates. In other words, the autotrophs are preceded by a largely unrecognized heterotrophic phase. Summing up literature documenting aerial transport and deposition of invertebrates, they assumed that pioneer predators were fed by a fallout of invertebrates onto land and water surfaces (Figs. 6-7). In adition, a fallout of detritus would favour scavenging detritivores. It was suggested that these heterotrophic communities conserve nutrients, particularly nitrogen, and facilitate the establishment of green plants. In a glacier foreland on Svalbard, Hodkinson et al. (2001) showed that spider densities were highly correlated with allochthonous inputs of potential prey items, predominantly chironomid midges. Coulson et al. (2003) further documented

resources from outside. If so, they are the super-pioneers among animals.

**5.4 Resident survivors or continuously colonising?** 

ballooning spiders, is an open question.

**5.5 Saprophagous super-pioneers?** 

**6. The predator first- hypothesis** 

aerial transport of invertebrates in the same foreland.

**5.3 Short or long life cycle?** 

Pioneer foreland communities containing macroarthropod predators have been documented both on Svalbard, in Norway, and in the Alps (Bråten & Flø, 2009; Gobbi et al., 2006a,b, 2007; Hodkinson et al., 2004; Kaufmann, 2001; Kaufmann & Raffl, 2002; Vater, 2006). While spiders represent the pioneer predators on Svalbard, a mixture of carabid beetles, various spiders and one or two harvestman species are typical on the European mainland.

Fig. 7. Air-borne insects sampled on the surface of the Hardangerjøkulen glacier, south Norway. These specimens have been a part of the air plankton, but low temperatures above the glacier have made them fall down. Photo: Marte Lilleeng.

### **6.1 The predator first-hypothesis challenged**

The predator first-hypothesis is at first sight an ecological paradox, but can be explained if the predators are fed by airborne food as for instance chironomid midges. But how stable is the airborn input of suitable and sufficient food to the pioneer ground? As already pointed at by Hodkinson et al. (2002), detritivores such as Collembola can also be eaten by predators such as spiders and carabid beetles. But to what degree is this occurring, and how important are resident Collembola or mite species as a stable food source? Gut content analyses are needed to answer these questions, preferably by recognizing prey items via their specific DNA. Perhaps the input of predators is very high, for instance of ballooning spiders, and that predators to a large degree eat other predators? Are pioneer sites in practice large sinks, where the majority of even predators do not survive? And which of the pioneer beetles, spiders and harvestmen do really reproduce on the barren ground?

Recent studies in the foreland of Midtalsbreen glacier snout, south Norway, indicate that chlorophyll-based food chains may start very early. Interestingly, the key organisms in this respect are mosses. On a large moraine which was freed from ice in 2005, twenty pitfall

Primary Succession in Glacier Forelands:

How Small Animals Conquer New Land Around Melting Glaciers 163

Fig. 9. Three specimens of the moss-eating springtail *Bourletiella hortensis.* An inblown moss

Fig. 10. Gut content of the springtail *Bourletiella hortensis* showing brown moss fragments.

Photo: Marte Lilleeng.

fragment of 1 mm length is in the middle. Photo: Marte Lilleeng.

traps were operated during the snow-free season 2008. Besides a pioneer fauna of beetles, spiders and harvestmen (Bråten and Flø, 2009), mites and springtails, the traps contained inblown fragments of various mosses. These fragments, among them so-called bulbils (Fig. 8) are able to develop into moss colonies. However, because these diaspores are tiny and end up between stones and gravel, they are not visible by eye in the field. By studying the gut content of springtails in the traps, it was revealed that most individuals of the large, sphere-formed species *Bourletiella hortensis* had eaten leaves and/or rhizoids of mosses (Figs. 9-10). This species can be very active and was observed to make jumps up to 10 cm length on the moraine, so it can obviously locate the inblown moss fragments. If the predatory beetles, spiders and harvestmen can eat this species, chlorophyll-based food chains may start very early.

Fig. 8. Certain mosses can easily be wind-dispersed by so-called bulbils. This picture shows how individual moss plants, including rhizoids, develop from bulbils placed on moist plaster of Paris. Photo: Sigmund Hågvar.

The first moss patches may also serve as a habitat for certain moss-living macroinvertebrates. After four years, in 2009, dry extraction of a small moss patch on the moraine revealed two larvae of terrestrial Chironomidae, as well as larvae and a pupa of the beetle *Simplocaria metallica* (Byrrhidae). The pupa soon hatched in the laboratory. Few insects are moss-eaters, but the family Byrrhidae is an exeption (Figs. 11-12). The importance of mosses for early faunal succession in glacier forelands should be closer studied. Maybe pioneer mosses represent a "driver" which facilitates the colonisation of certain invertebrates.

It should also be noted that some pioneer carabid beetles in the genus *Amara* are considered to be omnivorous, for instance *Amara quenseli* and *Amara alpina* (e.g. Lindroth, 1986) and these might for instance feed on inblown seeds.

traps were operated during the snow-free season 2008. Besides a pioneer fauna of beetles, spiders and harvestmen (Bråten and Flø, 2009), mites and springtails, the traps contained inblown fragments of various mosses. These fragments, among them so-called bulbils (Fig. 8) are able to develop into moss colonies. However, because these diaspores are tiny and end up between stones and gravel, they are not visible by eye in the field. By studying the gut content of springtails in the traps, it was revealed that most individuals of the large, sphere-formed species *Bourletiella hortensis* had eaten leaves and/or rhizoids of mosses (Figs. 9-10). This species can be very active and was observed to make jumps up to 10 cm length on the moraine, so it can obviously locate the inblown moss fragments. If the predatory beetles, spiders and harvestmen can eat this species, chlorophyll-based food chains may

Fig. 8. Certain mosses can easily be wind-dispersed by so-called bulbils. This picture shows how individual moss plants, including rhizoids, develop from bulbils placed on moist

The first moss patches may also serve as a habitat for certain moss-living macroinvertebrates. After four years, in 2009, dry extraction of a small moss patch on the moraine revealed two larvae of terrestrial Chironomidae, as well as larvae and a pupa of the beetle *Simplocaria metallica* (Byrrhidae). The pupa soon hatched in the laboratory. Few insects are moss-eaters, but the family Byrrhidae is an exeption (Figs. 11-12). The importance of mosses for early faunal succession in glacier forelands should be closer studied. Maybe pioneer mosses represent a "driver" which facilitates the colonisation of certain

It should also be noted that some pioneer carabid beetles in the genus *Amara* are considered to be omnivorous, for instance *Amara quenseli* and *Amara alpina* (e.g. Lindroth, 1986) and

start very early.

plaster of Paris. Photo: Sigmund Hågvar.

these might for instance feed on inblown seeds.

invertebrates.

Fig. 9. Three specimens of the moss-eating springtail *Bourletiella hortensis.* An inblown moss fragment of 1 mm length is in the middle. Photo: Marte Lilleeng.

Fig. 10. Gut content of the springtail *Bourletiella hortensis* showing brown moss fragments. Photo: Marte Lilleeng.

Primary Succession in Glacier Forelands:

Norway. Photo: Sigmund Hågvar.

**8. Succession patterns after the pioneer stage** 

How Small Animals Conquer New Land Around Melting Glaciers 165

Maybe also cyanobacteria with chlorophyll are present very early. Some of the typical pioneer beetles are omnivorous and may eat inblown seeds. Finally, who eats who is still an open question, as well as whether pioneer ground is a sink or a reproduction ground. The

Fig. 13. This rim of pioneer mosses along a large stone after four years is due to inblown moss fragments which have aggregated along the stone. Midtdalsbreen glacier snout, south

The succession from a pioneer stage to a mature, stable community goes through various phases which are more or less predictable. Not surprisingly, both the botanical and the zoological succession can be related to three more or less interrelated factors: Time since glaciation, distance to glacier and vegetation cover (e.g. Bråten & Flø, 2009; Gobbi, 2007; Hågvar, 2010; Hågvar et al., 2009; Hodkinsen et al., 2004; Kaufmann, 2001; Matthews, 1992; Vater, 2006). In the zoological succession, an obvious element is that herbivores like Chrysomelidae and Curculionidae have to wait for their host plant to be established. Furthermore, certain microarthropods and saprophagous beetles depend on a certain thickness of the soil organic layer (Bråten & Flø, 2009; Hågvar, 2010; Hågvar et al., 2009). Different taxonomic groups may show different succession patterns in the same foreland. For instance, at the Midtdalsbreen glacier foreland in south Norway, springtails colonised faster than oribatid mites. After 70 years, 84 % of the springtail species in the chronosequence were present, but only 57 % of the oribatid mites (Hågvar, 2010; Hågvar et al., 2009). Beetles followed a pattern similar to springtails, while spiders colonised more gradually, similar to oribatid mites (Bråten & Flø, 2009). The general rate of succession can also differ between geographical sites. In the foreland of the Rotmoos glacier in Austria, most beetle and spider species were present after only 40-50 years (Kaufmann, 2001). This is

ecology of pioneer communities may be more complicated than earlier thought
