Colonization of subterranean habitats by spiders in Central Europe

Headnote

Abstract: Using data from the Czech Republic, we studied the distribution of spiders in soils, crevice systems, scree and caves, i.e. subterranean habitats at depths spanning from 10 cm to 100 m. In total, we found 161 species. The number of species declines with increasing habitat depth, with a major drop in species richness at the depth of 10 meters. Thirteen species exhibit morphological adaptations to life in subterranean habitats. At depths greater than 10 meters, spider assemblages are almost exclusively composed of troglomorphic species. We propose a hypothesis of evolution of troglomorphisms at spiders during Quaternary climatic cycles.

Keywords: superficial and deep subterranean habitats; caves; spiders; troglomorphisms; Quaternary climatic cycle

Received 27 November 2012 ; Revised 9 April 2013; Accepted 12 April 2013

Citation: Ruzicka V., Smilauer P. and Mlejnek R., 2013. Colonization of subterranean habitats by spiders in Central Europe. International Journal of Speleology, 42 (2), 133-140. Tampa, FL (USA) ISSN 0392-6672 http://dx.doi.org/10.5038/1827-806X.42.2.5

INTRODUCTION

A variety of subterranean habitats exists and have been colonized by arthropods (Ruzicka, 1999; Culver & Pipan, 2009; Giachino & Vailati, 2010). According to the space dimensions, we can distinguish on one hand the soil, with interstices of dimensions comparable with body size of arthropods inhabiting the soil, and, on the other hand, all other terrestrial subterranean habitats fashioned by spaces distinctly larger than arthropod body dimensions. According to their depth, we can very roughly distinguish superficial subterranean habitats (usually up to several meters deep, with considerable annual temperature fluctuations) and deep subterranean habitats (usually with very limited or no annual temperature fluctuations). Superficial subterranean habitats are formed in soils, cracks and fissures in rock mantle, in bare and forest scree, in slope sediments, in river terraces, and in crevice systems and cave entrances formed in solid rock. Deep subterranean habitats are represented by fissure network in rock massifs, human-sized caves included.

Many subterranean invertebrates display similar morphologies that have evolved convergent under the similar selective pressures imposed by subterranean environment. Such spiders show the typical morphological changes - reduced pigment and eyes and lengthening of appendages (Culver & Pipan, 2010). Hotspots of subterranean biodiversity in the Europe, characterized by rich occurrence of highly specialized species, are concentrated in the Dinaric Karst (Culver & Sket, 2000). In Central Europe, the oscillation of climate during the Quaternary brought about repeated shifting and reconstruction of floras and faunas, cave fauna included. During the first Pleistocene glaciation, the eradication of any preglacial highly specialized terrestrial animals inhabiting caves is likely in the periglacial zone (Holdhaus, 1932). All subsequent glaciations represented the same threat for cave animals. In spite of that, we found spiders adapted to life in caves and other subterranean habitats in Central Europe (Ruzicka,1999).

In this paper we concentrate on spiders occupying subterranean habitats in the Czech Republic. The basic aims of our study were (1) to find in which habitats troglomorphic spiders occur, (2) to find how deep to subterranean spaces they penetrate, and (3) to provide a working hypothesis explaining the evolution of troglomorphic spiders in Central Europe.

MATERIALS AND METHODS

Study area

The Czech Republic lies in the temperate zone of Europe. The country has diverse geological and geomorphological structures and is rich in both superficial and deep subterranean habitats (Hromas, 2009). During Pleistocene glaciations, the Czech Republic formed a narrow ice-free passage between the Northern European and Alpine areas of glaciation (Ehlers & Gibbard, 2004). Zák et al. (2004, 2009) reported the finding of cryogenic cave carbonates in Czech, Polish, and Slovak caves, formed in slowly freezing water pools, probably on the surface of cave ice. It documents that caves were frozen in areas where discontinuous permafrost intermittently existed during glaciations.

Subterranean habitats and sampling

We evaluated material of spiders collected in four subterranean habitats (Fig. 1). We use the depth as a surrogate for the degree of isolation from the surface. "Depth" is characterised as the shortest distance, either horizontal or vertical, from the surface habitats. In subsurface habitats, this means the depth below the surface in which the spiders were collected. In caves, it represents the depth below the surface, or horizontal distance to the cave entrance, whichever is smaller (Novak et al., 2012). We collected spiders in pitfall traps (cans with fixation fluid), usually modified board traps (Ruzicka, 1982, 1988b). Each such sample represents an assemblage of spiders from one trap leftin concrete place usually for one year.

Soils (Fig. 1A)

We collected spiders in soils in three regions in Eastern Bohemia and Northern Moravia (Laska et al., 2011). Spiders were collected using pitfall traps. In total, we obtained 119 samples from the vertical span of 0.15-1.35 m.

Crevice systems (Fig. 1B)

We collected spiders in crevice systems formed in sandy marl, limestone, and phonolite in three regions in Central, Eastern, and Northern Bohemia. We were unable to dig under the layer of soil at a depth of 2-3 meters to reach crevice system, so using a hammer, a chisel, and a crowbar we penetrated into crevice systems through the side of a quarry wall. Spiders were trapped in pitfall traps. In total, we obtained 10 samples, with sampling depth of 0.35 m (horizontal distance from the quarry wall).

Scree (Fig. 1C)

We collected spiders in bare stony accumulations (sloping mass of coarse rock fragments without soil admixture) collected from the whole territory of the Czech Republic. The size of stones ranged from 10 cm up to 80 cm (exclusively several meters). The investigated scree are formed by limestone, sandstone, volcanic rocks (basalt, phonolite, andesite), gneiss, conglomerate, quartzite, granite and other kinds of rock (Ruzicka & Klimes, 2005). Spiders were trapped in pitfall traps. In total, we obtained 225 samples from the vertical span of 0.1-6.5 m.

Caves (Fig. 1D)

We evaluated data from the whole territory of the Czech Republic, from caves formed in limestone (dolomite), sandstone, volcanic rocks (basalt, phonolite), gneiss, sandy marl, and loess. Caves deeper than 20 m are formed exclusively in limestone. Spiders completing the whole living cycle on concrete place were collected using pitfall traps and hand picking. We do not take into consideration samples from open abysses or caves with open water flow, where spiders living on surface could be transported. In total, we obtained 95 samples varying in depth from 2-100 m.

Spiders and their morphology

Zacharda (1979), studying the morphological adaptations of mites, distinguished two different classes of adaptations to life in subterranean environment: edaphomorphisms are adaptations to life in soil environment, and troglomorphisms are adaptations to life in all other subsurface habitats. Depigmentation, desclerotization, and the atrophy (even loss) of the eyes are characteristic for both types of adaptations. Legs shorter than in epigean congeners are typical for edaphomorphic species, whereas legs longer than in epigean congeners are typical for troglomorphic species. In harvestmen, depigmentation and changes in leg length are among initial changes, eye size may be the last character affected (Derkarabetian et al., 2010). In spider genus Troglohyphantes, pigmentation is the first to get lost, the next stage is loss of pigment around the eyes, which runs parallel to reduction of eye size (Deeleman-Reinhold, 1978).

We searched for species with published data documenting troglomorphisms/edaphomorphisms among spiders caught. All such populations/taxa are described in relation to conspecific surface population or to closely related surface species. We consider slight changes in leg length and barely noticeable eye diminishing to be initial changes. We designated marked eye reduction, characterized by posterior median eyes interdistance greater than two eye diameters (measured by us), as advanced eye reduction.

Nomenclature of species is according to Platnick (2012). Dysdera lantosquensis Simon, 1882 sensu Øezáè et al. (2008). We suppose that Porrhomma cambridgei Merrett, 1994 and P. oblitum (Cambridge, 1871) can be conspecific, and for the purpose of this study we designate all specimens as Porrhomma oblitum. We suppose that Porrhomma myops Simon, 1884 and Porrhomma rosenhaueri (Koch, 1872) can be conspecific, and for the purpose of this study we designate all specimens as Porrhomma rosenhaueri.

The spiders were examined and determined under Olympus SZX12 stereomicroscope in 80% ethanol. The posterior median eyes interdistance were measured with an Olympus BX40 compound microscope fitted with an ocular micrometer. The material for photographing was transferred into a mixture of this ethanol and glycerol 4 : 1. Photographs were taken with an Olympus C-5060 wide zoom digital camera mounted on an Olympus BX40 microscope. The images were montaged using CombineZP image stacking software.

Data analysis

Counts of individuals for each spider species in each sample, as well as the species richness (measured as the number of spider species occurring in each sample) were log-transformed (using ln(x+1) formula) before their use in statistical models, to achieve homogeneity of variances in statistical models.

We have summarized the relative changes in composition of spider assemblages across individual sites using the detrended correspondence analysis (DCA) method, with down-weighting of rare spider species (ter Braak & Smilauer, 2002, p. 203). The differences in spider assemblages among the four distinguished habitat types was tested and visualized using canonical correspondence analysis (CCA) with a Monte Carlo permutation test of significance (Leps & Smilauer, 2003). Habitat preference of selected spider species (17 species with abundance best predicted by habitat type) was displayed with a pie attribute plot. All multivariate analyses were performed and graph created using Canoco for Windows package version 4.5 (ter Braak & Smilauer, 2002).

Change of species richness (number of occurring taxa) with depth was described with a linear model using log-transformed richness as well as log-transformed depth, using F-static based test of model significance. The proportion of troglomorphic taxa in the spider assemblages was predicted using a generalized linear model with an assumed binomial distribution, and this model was tested using likelihood-ratio test based on a test statistic with assumed χ2 distribution under H0. Linear and generalized linear models were fitted using R package version 2.8 (R Development Core Team, 2008).

RESULTS

In total, we found 161 spider species across all investigated habitats. Thirteen species exhibit troglomorphisms in all or in some populations. We register them in karst areas, as well as far from karst areas on bedrock of all investigated types. This set of species (Table 1) forms a focal group for our study.

In soils we captured 362 spiders belonging to 35 species. Cicurina cicur, Palliduphantes alutacius, and Harpactea lepida were the most frequent. Porrhomma microps and Porrhomma rosenhaueri are troglomorphic.

In crevices we caught 247 spiders belonging to 32 species. Cicurina cicur, Histopona torpida, and Harpactea lepida were the most frequent ones. Porrhomma microps and Improphantes improbulus are troglomorphic species.

In scree habitats 1362 spiders were collected, belonging to 117 species. Lepthyphantes notabilis, Bathyphantes eumenis buchari, and Rugathodes bellicosus were the most frequent ones. B. e. buchari, Comaroma simoni, Rugathodes bellicosus, Theonoe minutissima, Wubanoides uralensis lithodytes, Improphantes improbulus, Porrhomma egeria, and Porrhomma rosenhaueri are troglomorphic species. The first five were collected exclusively in this habitat.

In caves we captured 917 spiders belonging to 75 species. Porrhomma egeria, Nesticus cellulanus, Meta menardi, and Metellina merianae were the most frequent ones. Porrhomma convexum, Porrhomma oblitum, Porrhomma profundum, Pseudomaro aenigmaticus, Improphantes improbulus, Porrhomma egeria, Porrhomma microps, and Porrhomma rosenhaueri are troglomorphic species. The first four species were collected exclusively in this habitat.

We found a great overlap in spider assemblages across the four habitat types (Fig. 2). Seven species were recorded in all four habitats: Centromerus cavernarum, Cicurina cicur, Coelotes terrestris, Harpactea lepida, Histopona torpida, Malthonica silvestris, and Palliduphantes alutacius. Nevertheless, there was a significant difference in spider assemblages among the compared habitats (pseudo-F = 5.3, p=0.001), with habitat type predictor explaining 6% of the total variation. We have found multiple spider species limited only to one of the recognized habitat types (Fig. 3, the species with symbols overlapping a habitat symbol). Also, the species occurring more frequently in two habitat types preferred either a combination of scree and caves, or a combination of soil and crevices (see Fig. 4).

The number of species in a sample declined with increasing depth, with a major drop in species richness at the depth below 10 meters (Fig 5A). Fitted linear model (with log-transformed species richness as well as the habitat depth) explained 23% of the richness variation (F1.265=76.9, p<0.0001).

All four types of habitats studied were occupied by some troglomorphic species. The highest number of these species (eight) was recorded in scree and cave habitats. Proportion of troglomorphic taxa in a sample increased with increasing distance from surface habitats (Fig. 5B, fitted generalized linear model explained 25% of the total variation, χ2=98.9, p<0.0001). At depths greater than 10 meters, spider assemblage was almost exclusively composed of troglomorphic spider species. However, no studied species was exclusively specialised to deep subterranean habitats.

We arranged troglomorphic species in a sequence based on the maximal depth of occurrence (Fig. 6; Table 2). The species exhibiting initial morphological changes tend to occupy only superficial subterranean habitats (especially scree slopes), and tend to have isolated troglomorphic sub-populations and main sub-population inhabiting surface habitats. The species exhibiting advanced eye reduction (Fig. 7) tend to occupy deep subterranean habitats. However, they often occur abundantly also in surface habitats.

DISCUSSION

We discovered that both superficial and deep subterranean habitats are richly colonized by spiders and numerous species occur in several types of subterranean habitats. This supports the idea of Giachino & Vailati (2010: 28) that "different subterranean habitats are in fact closely interrelated and form an inseparable continuum."

The high number of troglomorphic spider species found in superficial subterranean habitats documents the importance of these habitats for subterranean evolution of spiders (Ruzicka, 1999), as the colonizers of subterranean realm must invade first superficial subterranean spaces. It was documented independently also for beetles (Ruzicka, 1998; Giachino & Vailati, 2010) and aquatic crustaceans (Culver & Pipan, 2008; Pipan & Culver, 2012).

Giachino & Vailati (2010; see pages 41, 68), studying beetles, found bare scree accumulations as "unsuited for the life of subterranean organisms". But we found bare scree accumulations to be very important for the life and evolution of subterranean spiders, maybe because the spiders, as good climbers, are better adapted for colonization of bare stone and rock surfaces (Ruzicka et al., 2010).

Generally, the degree of eye regression increases with phylogenetic age (Culver et al., 1995; Langecker, 2000). If we suppose that the evolution of initial troglomorphisms took place during Holocene (Paquin et al., 2009; Rùzièka, 2011), the origin of species exhibiting advanced troglomorphisms must have probably occurred earlier.

Blick & Kreuels (2002) documented numerous records of microphthalmous Pseudomaro aenigmaticus: in caves, in open terrain, and also in aeroplankton in 12 m height. That documents that some troglomorphic spiders may preserve the ability to balloon, and to disperse. Especially members of the family Linyphiidae are known as good ballooners. This family is particularly well represented in the temperate and cooler regions of the Northern Hemisphere (Jocqué & Dippenaar-Schoeman, 2006) and contains numerous troglomorphic taxa (e.g. in genera Porrhomma, Lepthyphantes, and Troglohyphantes). Porrhomma cavernicola, occurring in Appalachian caves, is an example of "exceptionally widespread troglobite" (Miller 2005).

In Central Europe, Quaternary climatic cycles influenced all natural processes (Lozek, 1976). Interglacial periods are characterized by average annual temperature of 8-12 °C, by precipitation of 700-1000 mm, by development of closed forests, by intensive karst processes, and by flowstone formation in caves. Caves are accessible and could be colonized by spiders, with consequent evolution of troglomorphic characters. Glacial periods, in their maxima, are characterized by average annual temperature between -5 and -3 °C, by precipitation of 100-200 mm, by development of cold steppe or (at higher altitudes) tundra vegetation, and by ice formation in caves. Terrestrial animals cannot survive in caves filled with ice (Culver & Pipan, 2010). We assume, that the troglomorphic populations migrated to subsurface and surface habitats. Vertical migrations of cave beetles are well known (Polak, 2012). Following that phenomenon troglomorphisms could have been introduced into populations inhabiting subsurface and surface habitats. Troglomorphic spiders could survived there as they do in present time: such as P. microps in leaf litter (Miller & Obrtel, 1975), such as P. oblitum in detritus and under tree bark (Thaler et al., 2003), such as P. rosenhaueri in scree habitats (Ruzicka et al., 2012), such as P. convexum or P. egeria in various cold and humid habitats, e.g. in mountains. Especially the scree habitats offer a broad scale of microhabitats (Ruzicka, 1990; Ruzicka et al., 1995; Zacharda et al., 2007).

Holdhaus (1932) delimited the northern distribution of blind animals occurring exclusively in caves and documented it on very extensive material. The line goes roughly on northern margin of Pyrenees, southern margin of the Alps, and northern margin of Dinarides. In the region of long-term stable climate (below Holdhaus' line), animals might have continuously penetrated in deeper and more isolated spaces and troglomorphisms might have evolved. The contact between troglomorphic and surface populations could have been eliminated (surface ancestor can become extinct or migrate elsewhere) and troglomorphs could have evolved in a new species (principally different from surface ancestor) (Fig. 8A). But what about above Holdhaus' line, in Central Europe?

We hypothesize that troglomorphic populations of spiders in Central Europe repeatedly migrated from caves to subsurface and surface habitats during glaciations. Troglomorphisms were introduced into populations living in these habitats. Therefore, in the present time, advanced troglomorphic characters occur in deep caves as well as in surface habitats far from karst regions (Fig. 8B), and the broad variability of morphological characters complicates their taxonomic evaluation. The research of evolution of troglomorphic spiders in Pleistocene periglacial zone should take into account multiple glaciations.

ACKNOWLEDGEMENTS

We would like to thank David Culver and Tanja Pipan for their interest and stimulating discussions during their visit of the Czech Republic in July 2011, and Tone Novak and David Culver for substantial improvement of the manuscript. Petr Svácha and Adam Ruzicka assisted with spiders photographing and figures preparation. This research was conducted with institutional support RVO:60077344. P.S. contribution was supported by a grant from University of South Bohemia, GAJU 04-142/2010/P.

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