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Organic carbon content and temperature as substantial factors affecting diversity and vertical distribution of Collembola on forested scree slopes
European Journal of Soil Biology 75 (2016) 180e187
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European Journal of Soil Biology journal homepage: http://www.elsevier.com/locate/ejsobi
Original article
Organic carbon content and temperature as substantial factors affecting diversity and vertical distribution of Collembola on forested scree slopes lia Raschmanova a, Lubomír b, Michal Rendos a, *, Nata Kova c a, Dana Miklisova a a cik Andrej Mock , Peter Lupta a b
rik University, rova 2, SK-04154, Kosice, Slovakia Institute of Biology and Ecology, Faculty of Science, Pavol Jozef Safa Sroba Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, SK-04001, Kosice, Slovakia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 6 October 2015 Received in revised form 1 June 2016 Accepted 6 June 2016
Vertical distribution of collembolan communities along a depth gradient and the impact of temperature and chemical parameters (pH, organic carbon content) on the structure of communities were studied on three forested scree slopes differing in type of bedrock and topography in the Western Carpathians, Slovakia (Central Europe). Collembola were collected using subterranean traps at depths of 5e95 cm from the soil surface. A total of 70 species were identified at the sites, of which 20 were subterranean forms (17 eutroglophiles, 3 troglobionts). Higher organic carbon content and lower temperature in the screes resulted in distinctly higher activities of the subterranean forms. The north-exposed limestone scree slope with mesophilous linden-maple wood and sediment layers rich in organic carbon had the most pronounced community structure and a distinctly higher number of eutroglophiles and troglobionts. The south-west facing carbon-poor volcanic scree slope with xerophilous oak-hornbeam wood had a slightly higher internal temperature and distinctly lower species richness compared with the other two sites. The north-facing limestone scree slope with mesophilous beech-hornbeam wood characterized by a rather cool microclimate and low carbon content showed lower activity and a relatively uniform pattern of distribution of Collembola across the depth profile. Species richness and activity of sub- and eutroglophiles at the sites correlated significantly with the organic carbon content in the depth layers. The activity of troglobionts increased considerably with depth and negatively correlated with the temperature inside the scree. Thus, organic carbon content and the microclimate were substantial factors that determined the diversity and vertical distribution of Collembola within the forested screes. The present study implies that in forested scree deposits with well-developed upper organic horizons microarthropod communities have an obvious vertical stratification. © 2016 Elsevier Masson SAS. All rights reserved.
Handling editor: Stefan Schrader Keywords: Microarthropods Subterranean fauna Abiotic parameters Depth gradient Shallow subterranean habitat Western Carpathians
1. Introduction Screes represent an accumulation of broken rock fragments that arose in particular due to frost weathering of rock faces. In the temperate zone, such formations constitute island habitats, and are mostly limited to steep slopes associated with hills and river valleys [1,2]. Extensive interior spaces among the stony accumulation form a type of intermediate-sized (1 mme20 cm in diameter) shallow subterranean habitat. These aphotic habitats are distinguished
* Corresponding author. E-mail address: [email protected] (M. Rendos). http://dx.doi.org/10.1016/j.ejsobi.2016.06.001 1164-5563/© 2016 Elsevier Masson SAS. All rights reserved.
from deep caves by their close connection to the surface (less than 10 m) and better accessibility of organic matter [3,4]. Scree slopes are in general dynamic elements of a landscape [5]. The early phase in their evolution is the formation of a stony accumulation along a slope. The result is then a bare scree slope characterized by a sharp contrast between the external and internal microclimates [6]. In the next phase, the bare screes are gradually stabilized with soil and vegetation cover. The network of empty spaces between the base of the soil and bedrock is a typical example of mesovoid shallow substratum [4,7]. The complete clogging of these spaces with soil is the last phase in scree slope evolution. In this case, the only intermediate-sized spaces that remain are those found between stones and roots [8].
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The proximity of soil and the above-growing vegetation is essential for maintaining relatively constant microclimatic conditions throughout a scree slope [9,10], and they ultimately affect the species composition and richness of the invertebrate fauna in the whole profile. Decaying organic material accumulating on the soil surface is one of the main energy sources for scree habitats. Such material can be transported either passively in the form of dissolved substances, or actively by the migration of soil macrofauna [11]. Due to the favourable microclimate and good accessibility of nutrients, forested scree slopes are generally populated by diverse invertebrate fauna, predominantly by species sensitive to the fluctuation of external environmental factors [12,13]. In general, the communities of common soil-dwelling and subterranean species (eutroglophiles and troglobionts) overlap in this habitat [14,15]. Collembola are among the most diversified groups of terrestrial invertebrates that are also abundant in subterranean habitats [16]. Despite intensive research on shallow subterranean habitats in recent decades, this hexapod group has received little attention. Gers and Najt [17] observed that among the Collembola generalists regularly inhabiting caves and cave entrances, two troglobiotic species known also from local caves occurred in the mesovoid shallow substratum in southern France. Similarly, Christian [18] found two troglobiotic species of Collembola when performing a study of underground fauna on scree slopes covered with permafrost soil in the Austrian Alps. Querner and Greben-Krenn [19] observed that the abundance of collembolans decreased with depth at two high-mountain sites in the Austrian Alps. Thereafter, Nitzu et al. [20e22] and Popa [23] described Collembola communities in several mesovoid shallow substratum sites in the Romanian Carpathians. Except for a few eutroglophiles, most Collembola sampled there were common soil-dwelling species. The present study was focused on Collembola communities occupying the depth gradient of three forested scree slopes in the Western Carpathians, Slovakia. Based on current knowledge, we assumed that the communities would vary considerably along the depth gradient, and the differences in their structure would be directly related to changes in temperature, organic carbon content and the pH of the substrate. It was also expected that the activity of common soil-dwelling species would decline, whereas the activity of subterranean species (eutroglophiles and troglobionts) would increase with the depth of the scree deposits. The present study aimed (1) to define differences in the vertical distribution of collembolan communities and the presence of subterranean forms along a depth gradient (5e95 cm from soil surface) and (2) to reveal the response of Collembola communities to environmental parameters (temperature, pH, organic carbon content) at three forested scree slope sites differing in topography and type of bedrock. 2. Material and methods 2.1. Study sites Collembola were collected at three sites situated in different geomorphological units of the Western Carpathians, Central Europe (Table 1): skaly e Cerova vrchovina Highlands, near the (1) Belinske village of Belina (south-eastern Slovakia). The site is characterized by approximately 5-metre high basalt towers jutting out from the hillside and a scree slope stretching along them. There were four distinct layers in the scree slope profile: litter and humus (0e5 cm), organo-mineral layer (5e30 cm), a mixture of basalt rocks and mineralized soil (30e70 cm) and scree with spaces filled with soil
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(70e110 cm). Although the amount of rocks grew proportionally with increasing depth, their size of 2 cm in diameter remained unchanged. (2) Drien canský kras e a small karst area in the Revúcka vrchovina Highlands, near the village of Spanie Pole (southeastern Slovakia). The site is formed by a limestone ridge and a steep scree slope lying a few metres below the entrance of n opolsk a Cave. The scree slope profile conthe Spa a jaskyn sisted of four layers: leaf litter and humus (0e5 cm), organomineral layer (5e25 cm), soil with stones (25e70 cm) and scree partially clogged with soil (70e110 cm). Both the amount and size of the rocks increased with depth. While the penultimate layer consisted of rock fragments reaching the size of a few centimetres, the diameter of the rocks forming the scree below this layer ranged from 15 to 30 cm. (3) Malý Ru zínok e a karst valley in the Cierna hora Mountains, Lodina (eastern Slovakia). A massive near the village of Mala limestone cliff with several short caves and a scree slope at its base are the typical features of this site. The scree profile consisted of the following layers: leaf litter and humus (0e15 cm), organo-mineral layer (15e45 cm) clearly separated from scree (45e110 cm). The scree with spaces slightly filled up with soil was composed of rocks varying from 10 to 15 cm in diameter.
2.2. Sampling and species identification At each site, a few metres under the top of the scree slope, a pit approximately 200 40 cm in size and over 100 cm deep was excavated, and the soil of the particular layers was carefully separated. Two subterranean traps, after Schlick-Steiner and Steiner [24], were vertically placed into the pit, 50 cm from one another. The pit was subsequently backfilled with the dug-out soil in the original order of the layers. The subterranean trap consisted of a plastic cylinder (length 110 cm, diameter 10.5 cm) with openings
Table 1 Topographic, microclimatic and soil-chemical characteristics of the study sites (soil type classification after the FAO system). Site
Coordinates Altitude (m a.s.l) Slope ( ) Exposition Bedrock Soil type Forest composition T ( C) 5 cm 35 cm 65 cm 95 cm pHðH2 OÞ 5 cm 35 cm 65 cm 95 cm Corg (%) 5 cm 35 cm 65 cm 95 cm
skaly Belinske
Drien canský kras
Malý Ru zínok
48 13.30 N 19 51.80 E 460 20 SW Basalt Calcaric cambisol Oakehornbeam
48 31.70 N 20 07.10 E 315 35 N Limestone Rendzina Beechehornbeam
48 50.50 N 21 06.60 E 530 15 NE Limestone Rendzina Lindenemaple
17.1 16.9 15.7 15.0
± ± ± ±
3.3 2.1 1.7 0.9
13.9 14.0 13.7 13.2
± ± ± ±
2.2 1.7 1.0 0.7
13.7 13.5 14.0 12.8
5.0 5.6 6.3 6.4
6.6 8.1 8.2 8.3
7.7 8.2 8.2 8.3
3.2 0.8 0.8 0.5
7.3 3.6 2.4 1.7
15.5 9.2 9.6 8.8
± ± ± ±
2.6 2.3 2.3 2.4
T e average temperature and standard deviation (monthly measures), pHðH2 OÞ e soil acidity, Corg e organic carbon content.
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(diameter 0.8 cm) drilled around at 10 horizontal levels (5, 15, 25, 35, 45, 55, 65, 75, 85 and 95 cm), and a demountable system of 10 plastic cups (volume 500 ml) connected to each other by a central iron rod and nuts. The buried cylinder served as a casing, allowing the insertion of cups filled with a 4% formaldehyde solution. The position of each of the ten cups inside the cylinder corresponded to the openings on the cylinder perimeter. The top of the cylinder was tightly closed with a plastic cap (Fig. 1). At the Malý Ru zínok site, the subterranean traps were exposed from May to October 2009 (163 days) and were emptied monthly. This design for fauna collecting was used for a detailed study on Collembola community dynamics at this site, the data from which will be presented in a skaly and Drien separate paper. At both the Belinske canský kras sites, the traps were exposed from May to October 2012 (150 days). To remove the captured specimens, the system of plastic cups was pulled out of the buried cylinder and the individual cups were dismounted from one another. The contents of the cups were then poured into plastic bottles and brought to the laboratory. Collembola were separated from the rest of the captured fauna, mounted on permanent slides after Rusek [25] and identified using a Leica DM1000 phase-contrast microscope and identification keys [26e29]. Based on the classification proposed by Sket [30], the species were assigned to four trogloforms regarding their affinity to the subterranean environment: (1) trogloxenes e species occurring in subterranean habitats exceptionally and unable to establish subterranean populations there, (2) subtroglophiles e species commonly found in subterranean habitats but intimately associated with epigean habitats for some biological functions, (3) eutroglophiles e essentially epigean species able to maintain permanent subterranean populations, and (4) troglobionts e species restricted exclusively to subterranean habitats, with well developed morphological adaptations to a life in darkness, such as the absence of eyes, pigmentation and the elongation of appendages (antennae, limbs, claws). At each sampled site, microclimatic and chemical parameters were collected from depths of 5, 35, 65 and 95 cm. The temperature was measured continually over the sampling period at 4-hour intervals using iButton DS1921G data-loggers mounted on the wall of the plastic cups. To determine the soil chemical parameters (pH and organic carbon content), soil samples were taken once during the pits excavation, with a total of 12 samples analysed (3 sites 4 depths). Samples were hand-mixed and coarse particles, such as stones and vegetation remnants, were removed. In the laboratory, the samples were air-dried for several weeks and subsequently sieved (mesh size 2 mm). Soil pH was measured potentiometrically in a 1:5 soil:deionised water suspension, and organic carbon content was analysed using the dynamic combustion method [31]. 2.3. Statistical analysis The average number of individuals from the pair of traps was standardized for 100 days (¼cumulative activity densities). Nonparametric Spearman correlation coefficient was used to evaluate the impact of environmental parameters on the activity of dominant species and particular trogloforms of Collembola (trogloxenes, subtroglophiles, eutroglophiles and troglobionts). Correlation analyses were performed using Statistica for Windows version 12 [32]. To point out the community similarities along the depth profile, the Sørensen incidence-based (qualitative) similarity index [33] and the Bray-Curtis (¼Sørensen quantitative) similarity index [34] were calculated for each site using the EstimateS package [35]. Collembolan activities throughout the depth profile were depicted graphically separately for each trogloform. We performed canonical correspondence analysis (CCA) to investigate associations of collembolan communities with environmental parameters
Fig. 1. Subterranean trap design (a e plastic cylinder with openings above each cup, b e plastic cup filled with a 4% formaldehyde solution, c e central iron rod, d e plastic cap).
measured at four depths, with a total of 12 samples/plots (3 sites 4 depths) analysed. Response variables were represented by the activity of selected collembolan species. Species with a total activity of < 4 were arbitrarily excluded from the analysis due to the uncertain relationship with environmental factors. Temperature, organic carbon content and depth were used as explanatory variables. Soil pH, which significantly correlated with temperature (Spearman correlation coefficient), was excluded from the analysis. The data on Collembola activity had a gradient 3.2 SD units along, thus the unimodal CCA method with log transformed data was used (recommended by the Canoco 5 software [36]). 3. Results 3.1. Temperature and chemical characteristics All sites were characterized by similar patterns of temperature regime. The largest temperature fluctuations were observed near the surface (5 cm). Deeper, the amplitudes were lower but synchronized with the climate dynamics on the surface (Fig. 2). The skaly site presented slightly higher temperatures along Belinske the depth gradient compared with Drien canský kras and Malý Ru zínok. With the exception of Malý Ru zínok, we found the average temperature to decline gradually along the depth gradient. Belinske
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skaly had acidic soil, whereas the other two sites had alkaline soil pH, except for the depth of 5 cm at Drien canský kras. The carbon skaly, especially between depths content was very low at Belinske 35 and 95 cm (0.8e0.5%). In contrast to this, Malý Ru zínok was characterized by high organic carbon content even at deeper levels (9.2e8.8%). For the soil at the Drien canský kras site, carbon content decreased in proportion to increasing depth (Table 1). 3.2. Collembola diversity A total of 5271 individuals of Collembola comprising 70 species were sampled across all the investigated sites. The total number of individuals captured at Malý Ru zínok was distinctly higher than at the other sites. The total number of individuals found at Belinske skaly was about twice as high as at Drien canský kras. Distinctly higher species richness was found at Malý Ru zínok, followed by skaly (Appendix). All three sampled Driencanský kras and Belinske sites harboured both eutroglophiles and troglobionts. The highest number of these subterranean forms was observed at Malý Ru zínok (12 eutroglophiles, 2 troglobionts), followed by Drien canský kras (8 skaly (8 eutroglophiles, eutroglophiles, 1 troglobiont) and Belinske 1 troglobiont), (Appendix).
Fig. 2. Monthly fluctuations of temperature along the depth profile of the investigated skaly, DK e Driencanský kras, MR e Malý Ruzínok). scree slopes (BS e Belinske
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3.3. Vertical distribution of Collembola Vertical distribution of Collembola differed considerably among skaly site was characterized by a the sites studied. The Belinske gradual decrease in activity and species number between the depths of 5 and 35 cm. From 35 cm downwards, both parameters were similar. At Malý Ru zínok, the highest proportions of individuals (59.6%) and species (83.7%) were captured at a depth of 5 cm. The decline in both characteristics was very sharp between 5 and 15 cm. Deeper, the distribution of Collembola showed a similar skaly. In contrast, Drien pattern as at Belinske canský kras was characterized by relatively uniform patterns of total activities and species richness of Collembola within the scree slope (Fig. 3, Appendix). Malý Ru zínok had the most pronounced stratification of collembolan communities across the depth profile. At this site, the
Fig. 3. Distribution of Collembola along the depth gradient of the scree slopes skaly, DK e expressed as a total number of individuals trapped (BS e Belinske Driencanský kras, MR e Malý Ruzínok; * Number of individuals ¼ 2788, ** Species richness ¼ 410, *** Number of individuals ¼ 507, **** Number of individuals ¼ 307).
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Table 2 Similarity of collembolan communities along the depth gradient at three scree slope sites. Above the diagonal: the Bray-Curtis index, below the diagonal: the Sørensen incidence-based index. Index values > 0.50 are indicated in bold. Value 1.00 indicates identical communities. Depth
5 cm
skaly Belinske 5 cm e 15 cm 0.48 25 cm 0.33 35 cm 0.21 45 cm 0.40 55 cm 0.40 65 cm 0.32 75 cm 0.21 85 cm 0.21 95 cm 0.20 Drien canský kras 5 cm e 15 cm 0.38 25 cm 0.43 35 cm 0.32 45 cm 0.40 55 cm 0.24 65 cm 0.17 75 cm 0.21 85 cm 0.25 95 cm 0.24 Malý Ru zínok 5 cm e 15 cm 0.48 25 cm 0.49 35 cm 0.34 45 cm 0.43 55 cm 0.37 65 cm 0.41 75 cm 0.46 85 cm 0.36 95 cm 0.41
15 cm
25 cm
35 cm
45 cm
55 cm
65 cm
75 cm
85 cm
95 cm
0.57 e 0.47 0.33 0.62 0.62 0.50 0.33 0.50 0.46
0.25 0.41 e 0.36 0.50 0.50 0.55 0.36 0.36 0.17
0.07 0.12 0.34 e 0.29 0.29 0.33 0.33 0.33 0.29
0.09 0.16 0.39 0.44 e 1.00 0.86 0.57 0.57 0.25
0.16 0.26 0.57 0.31 0.69 e 0.86 0.57 0.57 0.25
0.17 0.29 0.72 0.44 0.59 0.51 e 0.67 0.67 0.29
0.19 0.32 0.72 0.40 0.47 0.47 0.87 e 0.67 0.29
0.06 0.13 0.31 0.63 0.63 0.42 0.48 0.43 e 0.57
0.04 0.09 0.15 0.35 0.35 0.24 0.23 0.21 0.53 e
0.60 e 0.50 0.47 0.15 0.27 0.00 0.35 0.29 0.40
0.25 0.30 e 0.40 0.36 0.31 0.25 0.27 0.17 0.15
0.28 0.42 0.21 e 0.50 0.56 0.31 0.40 0.35 0.44
0.18 0.07 0.29 0.25 e 0.43 0.67 0.38 0.31 0.43
0.09 0.10 0.15 0.34 0.28 e 0.36 0.44 0.27 0.13
0.07 0.00 0.22 0.11 0.55 0.17 e 0.15 0.20 0.18
0.07 0.19 0.11 0.25 0.15 0.19 0.06 e 0.35 0.44
0.10 0.22 0.09 0.33 0.17 0.22 0.11 0.38 e 0.27
0.07 0.19 0.05 0.19 0.21 0.04 0.06 0.67 0.30 e
0.30 e 0.61 0.48 0.75 0.67 0.65 0.55 0.56 0.53
0.10 0.41 e 0.57 0.71 0.55 0.73 0.69 0.71 0.67
0.06 0.25 0.67 e 0.67 0.48 0.55 0.64 0.59 0.55
0.09 0.39 0.72 0.71 e 0.79 0.81 0.77 0.80 0.69
0.09 0.36 0.66 0.62 0.80 e 0.67 0.69 0.64 0.67
0.13 0.29 0.46 0.32 0.45 0.57 e 0.67 0.81 0.71
0.09 0.25 0.44 0.36 0.52 0.68 0.74 e 0.77 0.73
0.05 0.19 0.30 0.18 0.41 0.61 0.53 0.67 e 0.75
0.05 0.16 0.30 0.27 0.45 0.55 0.45 0.56 0.73 e
high degree of quantitative (Bray-Curtis) similarity was recorded in the range of depths 25e55 cm ( 0.62) and depths 55e95 cm ( 0.45). The lowest quantitative similarity was observed between the depths of 5 cm and 85e95 cm (0.05 for both pairs). Furthermore, the Sørensen qualitative similarity index showed that the depth of 5 cm is comparatively different in species composition from the rest of the depth profile. The most similar species skaly was in the range of depth 45e85 cm composition at Belinske (Sørensen index 0.57). No remarkable similarity pattern of the community among the particular depths was observed at Drien canský kras (Table 2). The activity of collembolan trogloforms along the depth profile had comparable patterns at the studied scree slopes (Fig. 4). Trogloxenes were active predominantly in the uppermost level (5 cm), deeper their occurrence was only accidental. On the contrary, troglobionts showed inverted distributional pattern, with predominance at the deepest horizon (95 cm). An exception to this was the Malý Ru zínok site, where troglobiotic collembolans were distributed across the depth profile and had maximum activity between the depths of 55 and 95 cm. The activity of subtroglophiles was characterized by a gradual decrease between 5 and 25 cm and remained constant in the lower depths. Eutroglophiles occurred at all monitored depths and dominated notably in the lower half of skaly. the depth profile, with the exception of Belinske
content. On the other hand, troglobionts showed a negative correlation with temperature. The activity of nine species correlated positively with organic carbon content and one species with pH, whereas five species correlated negatively with temperature. The community data from the 12 plots (3 sites 4 depth) were further processed by CCA ordination analysis (Fig. 5). The total activity assigned to these plots consisted of 60 Collembola species. After exclusion of species with lower activity, the remaining 26 species (97.5% of total activity) were used as response variables and three environmental parameters (depth, temperature and organic carbon content) as explanatory variables, which accounted for 54.2% of total variation. The first two axes, with eigenvalues of 0.44 and 0.36, respectively, explained 48% of the cumulative variance. The permutation test on all axes confirmed their statistical significance (pseudo F ¼ 3.2, p ¼ 0.002). The direction of both temperature and depth arrows indicates a positive correlation between these environmental variables and ordination axes. The species Orchesella multifasciata, Orchesella bifasciata and Pseudosinella horaki were skaly scree slope, characterized by a associated with the Belinske higher temperature at particular depth layers compared with the other sites. Ceratophysella denticulata, Caprainea marginata, Morulina verrucosa, Pseudachorutes dubius, Pogonognathellus flavescens and some other species were grouped with the organic carbon-rich scree layers at Malý Ru zínok, while Pygmarrhopalites pygmaeus and Neelus koseli were species characteristic for the deeper scree layers.
3.4. Impact of environmental variables 4. Discussion Collembola species richness showed a strong positive correlation with organic carbon content (Table 3). Assessing the dependence of trogloforms on environmental variables, we found suband eutroglophiles to be positively correlated with organic carbon
Culver and Pipan [37] stressed that shallow subterranean habitats are highly variable in terms of environmental factors. In the present study, the greatest variability was observed in organic
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Fig. 4. Cumulative activity densities of collembolan forms along the depth profile of the scree slopes (Tgx e trogloxenes, Stp e subtroglophiles, Etp e eutroglophiles, Tgb e skaly, DK e Driencanský kras, MR e Malý Ruzínok; trend line: dotted e Belinske skaly, dashed e Driencanský kras, solid e Malý Ruzínok). troglobionts; BS e Belinske
carbon content and its distribution across the depth gradient. Indeed, this parameter is only a proxy for nutrient resources, as Collembola feed on microorganisms dependent on organic material. The scree slope at Malý Ru zínok, overgrown with linden-maple wood, had the highest soil organic carbon content, which was relatively high even at deeper levels. In contrast, the scree at skaly, covered predominantly with oak wood, had a very Belinske low carbon content, especially at depths below 5 cm. The availability of organic carbon to the deeper layers of shallow subterranean habitats depends on several factors, mainly on the
composition of the vegetation cover [4]. The rate of decomposition is determined by the chemical quality of the decaying leaf litter. It is known that leaves of European oak species decompose slowly (over 2e3 years) due to the high concentration of polyphenol-protein complexes in tissues compared with other deciduous leaves [38,39]. The flow of organic carbon from the surface to lower levels of the depth profile is likely to be closely related to the rate of decomposition of vegetation residues. Scree slopes which are partially filled with soil in deeper horizons are thus richer in organic carbon compared with bare screes and mesovoid shallow
Table 3 Spearman correlation coefficients between dominant Collembola species/trogloforms and soil-chemical parameters at the three scree sites and four depth levels. Environmental parameter
Species
Tf
Spearman correlation
T
Troglobionts Desoria tigrina Folsomia fimetaria Megalothorax hipmani Neelus koseli Pygmarrhopalites pygmaeus Pygmarrhopalites pygmaeus
stp stp tgb tgb etp etp
0.717 0.595 0.613 0.668 0.643 0.608 0.582
etp stp stp stp tgb tgb stp etp etp
0.861 0.674 0.797 0.591 0.650 0.832 0.809 0.815 0.587 0.609 0.707 0.648
pHðH2 OÞ Corg
Species richness Subtroglophiles Eutroglophiles Ceratophysella denticulata Ceratophysella silvatica Desoria tigrina Folsomia fimetaria Megalothorax hipmani Neelus koseli Parisotoma notabilis Plutomurus carpaticus Protaphorura armata
T e temperature, pH(H2O) e soil acidity, Corg e organic carbon content; Tf e trogloform, stp e subtroglophile, etp e eutroglophile, tgb e troglobionte.
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Fig. 5. CCA ordination triplot indicating associations of collembolan communities and sites with environmental parameters. Eigenvalues of the first two axes were 0.44 and 0.36, skaly :DK e Driencanský kras, -MR e Malý Ruzínok, with a number specifying the depth; respectively (T e temperature, Corg e organic carbon content; sites BBS e Belinske AREL e Pygmarrhopalites elegans, ARPR e P. principalis, ARPY e P. pygmaeus, CAMA e Caprainea marginata, CEDE e Ceratophysella denticulata, CEGR e C. granulata, CESL e C. silvatica, DIOR e Dicyrtomina ornata, DRTI e Desoria tigrina, FOFI e Folsomia fimetaria, FOMA e F. manolachei, ISNO e Parisotoma notabilis, LELI e Lepidocyrtus lignorum, MGHI e Megalothorax hipmani, MOVE e Morulina verrucosa, NLKO e Neelus koseli, OPCR e Oncopodura crassicornis, ORBI e Orchesella bifasciata, ORFL e O. flavescens, ORMU e O. multifasciata, PCDU e Pseudachorutes dubius, PGFL e Pogonognathellus flavescens, PLCA e Plutomurus carpaticus, PRAR e Protaphorura armata, PSHO e Pseudosinella horaki, PSTH e P. thibaudi).
substratum covered with a layer of moss or soil. On the other hand, bare screes are poor in carbon, as their only source of nutrients are fallen leaves brought by wind from adjacent forest, thus the concentration of carbon decreases rapidly at lower levels [11,40]. Dissimilarities among the studied scree slopes were also observed in their internal temperatures. It is apparent that the exposure of a scree slope affects the character of the internal microclimate. This was particularly evident on the southwest skaly which, unlike both northfacing scree slope at Belinske exposed slopes at Driencanský kras and Malý Ru zínok, presented higher values of temperature across the depth profile. Thus, organic carbon content along with the microclimate determined the diversity and distribution of Collembola within the studied forested screes. High organic content and cooler microclimate in the scree slope at Malý Ru zínok was reflected in distinctly higher activities of Collembola, including eutroglophiles and troglobionts. Furthermore, this site was characterized by a much more pronounced vertical stratification of communities along the scree slope profile. In contrast, the carbon-poor and warm scree slope at skaly was occupied mostly by eurytopic species of Belinske Collembola. As have been reported by several authors e.g. Refs. [11,19,41], species richness and abundance of arthropod fauna decrease rapidly with depth in shallow subterranean habitats. Such a distribution pattern was, however, observed in Collembola only at Malý Ru zínok; at the superficial layer both activity and species richness were extremely high compared with deeper layers. The sharp decline of both characteristics is most likely associated with the amount of leaf litter and humus accumulations in the first centimetres of the vertical profile. It is important to note that the vertical stratification of invertebrate communities inhabiting the scree slope may be negatively affected by the excavation of the sampling pit. The dislocation of particular scree slope layers may result in the absence of species sensitive to such disturbance at the beginning of trapping [42].
Although the Collembola sampling in this study was initiated instantly after burying the traps, we assume the disruption of collembolan communities was only slight and lasted only for a short period after burying. Most of the previously published studies e.g. Refs. [14,17,18,43] agreed that shallow subterranean habitats, including scree slopes, are inhabited by a mixture of troglobiotic and non-troglobiotic species. One of the principal objectives of our study was to define a pattern of depth distribution of Collembola according to their affinity to the subterranean realm. The study showed that most of the trogloxenes were exclusively bound to the uppermost level of the depth gradient and that they occurred deeper very rarely. With few exceptions, the majority of subtroglophiles and eutroglophiles had tendency to be distributed across the entire depth gradient. Troglobionts showed a reversed pattern of distribution, with significant predominance in the lower half of the depth gradient. Moreover, they occasionally occurred closer to the surface, at the levels completely filled with the soil. This contradicts the argument of Giachino and Vailati [9], who upon studying beetles stated that screes filled up with soil sediment cannot be colonized by subterranean fauna. It seems that the body size is an important factor limiting the vertical distribution of organisms in shallow subterranean habitats. The body size of most troglobiotic collembolans in this study did not exceed a length of 1.0 mm, which allowed them to colonize even tight spaces in the soil that filled the scree. Among the soil parameters monitored, organic carbon content and temperature were those that ruled the diversity and distribution of Collembola inside the scree slopes. Furthermore, our study showed that activity of subterranean species, both eutroglophiles and troglobionts, correlated with organic carbon. This supports the assumption of Pipan and Culver [44] that the content of organic carbon is an important limiting factor for the occurrence of or skaly ganisms in shallow subterranean habitats. Unlike Belinske and Drien canský kras, the carbon-rich Malý Ru zínok site was inhabited by distinctly higher number of eutroglophiles and
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troglobionts. Moreover, the present study implies that in forested scree deposits with well-developed upper organic horizons microarthropod communities have obvious vertical stratification. However, more data are necessary to make generalizations regarding this issue. Acknowledgement This study was supported by grant 1/0199/14 from the Slovak Scientific Grant Agency VEGA, by grant VVGS-2014-228 of P.J. Saf arik University in Kosice and by Operational Programme “Research & Development” funded from ERDF (Code ITMS: 26220120022, rate 0.4). We express our gratitude to P. Fend’a, R. Zamec (Comenius University, Bratislava), L. Papa cov a and V. Papa c Sobota) for their kind (Slovak Caves Administration, Rimavska assistance during the installation of the subterranean traps. M. skova for Dzurinka is acknowledged for help in the field work, T. Sa (P.J. help in the sorting of captured specimens and A. Parimuchova Saf arik University, Kosice) for sketching the subterranean trap design. We are also thankful to D. McLean for linguistic corrections of the manuscript and anonymous reviewers for their very constructive comments to earlier manuscript version. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.ejsobi.2016.06.001. References [1] V. R u zi cka, Stony debris ecosystems-sources of landscape diversity, Ekologia 12 (1993) 291e298. [2] V. R u zi cka, The first steps in subterranean evolution of spiders (Araneae) in Central Europe, J. Nat. Hist. 33 (1999) 255e256. [3] D.C. Culver, T. Pipan, Superficial subterranean habitatsegateway to the subterranean realm? Cave Karst Sci. 35 (2008) 5e12. [4] D.C. Culver, T. Pipan, Shallow Subterranean Habitats. Ecology, Evolution and Conservation, first ed., Oxford University Press, Oxford, 2014. [5] C. Gers, Ecologie et biologie des arthropodes terrestres du milieu souterrain cologie e volutive, Dissertation, Universite superficiel, functionnement et e Toulouse III, 1992 (in French). [6] V. R u zi cka, Structure and ecology of invertebrates communities of stony debris in Czech Republic, Bull. Soc. Neuchat. Sci. Nat. 116 (1991) 209e214. [7] C. Juberthie, B. Delay, M. Bouillon, Extension du milieu souterrain en zone non calcaire: description d’un nouveau milieu et de son peuplement par les opte res troglobies, Me m. Biospe ol. 7 (1980) 19e52 (in French). cole [8] T. Novak, P. Matja z, S. Lipovsek, F. Jan zekovi c, Duality of terrestrial subterranean fauna, Int. J. Speleol. 41 (2012) 181e188. [9] P.M. Giachino, D. Vailati, The Subterranean Environment. Hypogean Life, Concepts and Collecting Techniques, first ed., WBA Handbooks, Verona, 2010. pez, P. Oromí, S. Polak, D.C. Culver, Temperature variation and [10] T. Pipan, H. Lo the presence of troglobionts in terrestrial shallow subterranean habitats, J. Nat. Hist. 45 (2011) 253e273. [11] C. Gers, Diversity of energy fluxes and interactions between arthropod communities: from soil to cave, Acta Oecol. 19 (1998) 205e213. mcova , P. Smilauer, [12] V. R u zi cka, M. Zacharda, L. Ne J.C. Nekola, Periglacial microclimate in low-altitude scree slopes supports relict biodiversity, J. Nat. Hist. 46 (2012) 2145e2157. ncil ias¸u, Scree habitats: [13] E. Nitzu, A. Nae, R. Ba a, I. Popa, A. Giurginca, R. Pla ecological function, species conservation and vertical-temporal variation in the arthropod community, Syst. Biodivers. 12 (2014) 65e75. [14] C. Juberthie, The diversity of the karstic and pseudokarstic hypogean habitats in the world, in: H. Wilkens, D.C. Culver, W.F. Humphreys (Eds.), Subterranean Ecosystems, Elsevier, Amsterdam, 2000, pp. 17e39. [15] C. Juberthie, V. Decu, Interstitial habitats (terrestrial), in: J. Gunn (Ed.), Encyclopedia of Caves and Karst Science, Taylor and Francis, New York, 2004, pp.
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European Journal of Soil Biology journal homepage: http://www.elsevier.com/locate/ejsobi
Original article
Organic carbon content and temperature as substantial factors affecting diversity and vertical distribution of Collembola on forested scree slopes lia Raschmanova a, Lubomír b, Michal Rendos a, *, Nata Kova c a, Dana Miklisova a a cik Andrej Mock , Peter Lupta a b
rik University, rova 2, SK-04154, Kosice, Slovakia Institute of Biology and Ecology, Faculty of Science, Pavol Jozef Safa Sroba Institute of Parasitology, Slovak Academy of Sciences, Hlinkova 3, SK-04001, Kosice, Slovakia
a r t i c l e i n f o
a b s t r a c t
Article history: Received 6 October 2015 Received in revised form 1 June 2016 Accepted 6 June 2016
Vertical distribution of collembolan communities along a depth gradient and the impact of temperature and chemical parameters (pH, organic carbon content) on the structure of communities were studied on three forested scree slopes differing in type of bedrock and topography in the Western Carpathians, Slovakia (Central Europe). Collembola were collected using subterranean traps at depths of 5e95 cm from the soil surface. A total of 70 species were identified at the sites, of which 20 were subterranean forms (17 eutroglophiles, 3 troglobionts). Higher organic carbon content and lower temperature in the screes resulted in distinctly higher activities of the subterranean forms. The north-exposed limestone scree slope with mesophilous linden-maple wood and sediment layers rich in organic carbon had the most pronounced community structure and a distinctly higher number of eutroglophiles and troglobionts. The south-west facing carbon-poor volcanic scree slope with xerophilous oak-hornbeam wood had a slightly higher internal temperature and distinctly lower species richness compared with the other two sites. The north-facing limestone scree slope with mesophilous beech-hornbeam wood characterized by a rather cool microclimate and low carbon content showed lower activity and a relatively uniform pattern of distribution of Collembola across the depth profile. Species richness and activity of sub- and eutroglophiles at the sites correlated significantly with the organic carbon content in the depth layers. The activity of troglobionts increased considerably with depth and negatively correlated with the temperature inside the scree. Thus, organic carbon content and the microclimate were substantial factors that determined the diversity and vertical distribution of Collembola within the forested screes. The present study implies that in forested scree deposits with well-developed upper organic horizons microarthropod communities have an obvious vertical stratification. © 2016 Elsevier Masson SAS. All rights reserved.
Handling editor: Stefan Schrader Keywords: Microarthropods Subterranean fauna Abiotic parameters Depth gradient Shallow subterranean habitat Western Carpathians
1. Introduction Screes represent an accumulation of broken rock fragments that arose in particular due to frost weathering of rock faces. In the temperate zone, such formations constitute island habitats, and are mostly limited to steep slopes associated with hills and river valleys [1,2]. Extensive interior spaces among the stony accumulation form a type of intermediate-sized (1 mme20 cm in diameter) shallow subterranean habitat. These aphotic habitats are distinguished
* Corresponding author. E-mail address: [email protected] (M. Rendos). http://dx.doi.org/10.1016/j.ejsobi.2016.06.001 1164-5563/© 2016 Elsevier Masson SAS. All rights reserved.
from deep caves by their close connection to the surface (less than 10 m) and better accessibility of organic matter [3,4]. Scree slopes are in general dynamic elements of a landscape [5]. The early phase in their evolution is the formation of a stony accumulation along a slope. The result is then a bare scree slope characterized by a sharp contrast between the external and internal microclimates [6]. In the next phase, the bare screes are gradually stabilized with soil and vegetation cover. The network of empty spaces between the base of the soil and bedrock is a typical example of mesovoid shallow substratum [4,7]. The complete clogging of these spaces with soil is the last phase in scree slope evolution. In this case, the only intermediate-sized spaces that remain are those found between stones and roots [8].
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The proximity of soil and the above-growing vegetation is essential for maintaining relatively constant microclimatic conditions throughout a scree slope [9,10], and they ultimately affect the species composition and richness of the invertebrate fauna in the whole profile. Decaying organic material accumulating on the soil surface is one of the main energy sources for scree habitats. Such material can be transported either passively in the form of dissolved substances, or actively by the migration of soil macrofauna [11]. Due to the favourable microclimate and good accessibility of nutrients, forested scree slopes are generally populated by diverse invertebrate fauna, predominantly by species sensitive to the fluctuation of external environmental factors [12,13]. In general, the communities of common soil-dwelling and subterranean species (eutroglophiles and troglobionts) overlap in this habitat [14,15]. Collembola are among the most diversified groups of terrestrial invertebrates that are also abundant in subterranean habitats [16]. Despite intensive research on shallow subterranean habitats in recent decades, this hexapod group has received little attention. Gers and Najt [17] observed that among the Collembola generalists regularly inhabiting caves and cave entrances, two troglobiotic species known also from local caves occurred in the mesovoid shallow substratum in southern France. Similarly, Christian [18] found two troglobiotic species of Collembola when performing a study of underground fauna on scree slopes covered with permafrost soil in the Austrian Alps. Querner and Greben-Krenn [19] observed that the abundance of collembolans decreased with depth at two high-mountain sites in the Austrian Alps. Thereafter, Nitzu et al. [20e22] and Popa [23] described Collembola communities in several mesovoid shallow substratum sites in the Romanian Carpathians. Except for a few eutroglophiles, most Collembola sampled there were common soil-dwelling species. The present study was focused on Collembola communities occupying the depth gradient of three forested scree slopes in the Western Carpathians, Slovakia. Based on current knowledge, we assumed that the communities would vary considerably along the depth gradient, and the differences in their structure would be directly related to changes in temperature, organic carbon content and the pH of the substrate. It was also expected that the activity of common soil-dwelling species would decline, whereas the activity of subterranean species (eutroglophiles and troglobionts) would increase with the depth of the scree deposits. The present study aimed (1) to define differences in the vertical distribution of collembolan communities and the presence of subterranean forms along a depth gradient (5e95 cm from soil surface) and (2) to reveal the response of Collembola communities to environmental parameters (temperature, pH, organic carbon content) at three forested scree slope sites differing in topography and type of bedrock. 2. Material and methods 2.1. Study sites Collembola were collected at three sites situated in different geomorphological units of the Western Carpathians, Central Europe (Table 1): skaly e Cerova vrchovina Highlands, near the (1) Belinske village of Belina (south-eastern Slovakia). The site is characterized by approximately 5-metre high basalt towers jutting out from the hillside and a scree slope stretching along them. There were four distinct layers in the scree slope profile: litter and humus (0e5 cm), organo-mineral layer (5e30 cm), a mixture of basalt rocks and mineralized soil (30e70 cm) and scree with spaces filled with soil
181
(70e110 cm). Although the amount of rocks grew proportionally with increasing depth, their size of 2 cm in diameter remained unchanged. (2) Drien canský kras e a small karst area in the Revúcka vrchovina Highlands, near the village of Spanie Pole (southeastern Slovakia). The site is formed by a limestone ridge and a steep scree slope lying a few metres below the entrance of n opolsk a Cave. The scree slope profile conthe Spa a jaskyn sisted of four layers: leaf litter and humus (0e5 cm), organomineral layer (5e25 cm), soil with stones (25e70 cm) and scree partially clogged with soil (70e110 cm). Both the amount and size of the rocks increased with depth. While the penultimate layer consisted of rock fragments reaching the size of a few centimetres, the diameter of the rocks forming the scree below this layer ranged from 15 to 30 cm. (3) Malý Ru zínok e a karst valley in the Cierna hora Mountains, Lodina (eastern Slovakia). A massive near the village of Mala limestone cliff with several short caves and a scree slope at its base are the typical features of this site. The scree profile consisted of the following layers: leaf litter and humus (0e15 cm), organo-mineral layer (15e45 cm) clearly separated from scree (45e110 cm). The scree with spaces slightly filled up with soil was composed of rocks varying from 10 to 15 cm in diameter.
2.2. Sampling and species identification At each site, a few metres under the top of the scree slope, a pit approximately 200 40 cm in size and over 100 cm deep was excavated, and the soil of the particular layers was carefully separated. Two subterranean traps, after Schlick-Steiner and Steiner [24], were vertically placed into the pit, 50 cm from one another. The pit was subsequently backfilled with the dug-out soil in the original order of the layers. The subterranean trap consisted of a plastic cylinder (length 110 cm, diameter 10.5 cm) with openings
Table 1 Topographic, microclimatic and soil-chemical characteristics of the study sites (soil type classification after the FAO system). Site
Coordinates Altitude (m a.s.l) Slope ( ) Exposition Bedrock Soil type Forest composition T ( C) 5 cm 35 cm 65 cm 95 cm pHðH2 OÞ 5 cm 35 cm 65 cm 95 cm Corg (%) 5 cm 35 cm 65 cm 95 cm
skaly Belinske
Drien canský kras
Malý Ru zínok
48 13.30 N 19 51.80 E 460 20 SW Basalt Calcaric cambisol Oakehornbeam
48 31.70 N 20 07.10 E 315 35 N Limestone Rendzina Beechehornbeam
48 50.50 N 21 06.60 E 530 15 NE Limestone Rendzina Lindenemaple
17.1 16.9 15.7 15.0
± ± ± ±
3.3 2.1 1.7 0.9
13.9 14.0 13.7 13.2
± ± ± ±
2.2 1.7 1.0 0.7
13.7 13.5 14.0 12.8
5.0 5.6 6.3 6.4
6.6 8.1 8.2 8.3
7.7 8.2 8.2 8.3
3.2 0.8 0.8 0.5
7.3 3.6 2.4 1.7
15.5 9.2 9.6 8.8
± ± ± ±
2.6 2.3 2.3 2.4
T e average temperature and standard deviation (monthly measures), pHðH2 OÞ e soil acidity, Corg e organic carbon content.
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(diameter 0.8 cm) drilled around at 10 horizontal levels (5, 15, 25, 35, 45, 55, 65, 75, 85 and 95 cm), and a demountable system of 10 plastic cups (volume 500 ml) connected to each other by a central iron rod and nuts. The buried cylinder served as a casing, allowing the insertion of cups filled with a 4% formaldehyde solution. The position of each of the ten cups inside the cylinder corresponded to the openings on the cylinder perimeter. The top of the cylinder was tightly closed with a plastic cap (Fig. 1). At the Malý Ru zínok site, the subterranean traps were exposed from May to October 2009 (163 days) and were emptied monthly. This design for fauna collecting was used for a detailed study on Collembola community dynamics at this site, the data from which will be presented in a skaly and Drien separate paper. At both the Belinske canský kras sites, the traps were exposed from May to October 2012 (150 days). To remove the captured specimens, the system of plastic cups was pulled out of the buried cylinder and the individual cups were dismounted from one another. The contents of the cups were then poured into plastic bottles and brought to the laboratory. Collembola were separated from the rest of the captured fauna, mounted on permanent slides after Rusek [25] and identified using a Leica DM1000 phase-contrast microscope and identification keys [26e29]. Based on the classification proposed by Sket [30], the species were assigned to four trogloforms regarding their affinity to the subterranean environment: (1) trogloxenes e species occurring in subterranean habitats exceptionally and unable to establish subterranean populations there, (2) subtroglophiles e species commonly found in subterranean habitats but intimately associated with epigean habitats for some biological functions, (3) eutroglophiles e essentially epigean species able to maintain permanent subterranean populations, and (4) troglobionts e species restricted exclusively to subterranean habitats, with well developed morphological adaptations to a life in darkness, such as the absence of eyes, pigmentation and the elongation of appendages (antennae, limbs, claws). At each sampled site, microclimatic and chemical parameters were collected from depths of 5, 35, 65 and 95 cm. The temperature was measured continually over the sampling period at 4-hour intervals using iButton DS1921G data-loggers mounted on the wall of the plastic cups. To determine the soil chemical parameters (pH and organic carbon content), soil samples were taken once during the pits excavation, with a total of 12 samples analysed (3 sites 4 depths). Samples were hand-mixed and coarse particles, such as stones and vegetation remnants, were removed. In the laboratory, the samples were air-dried for several weeks and subsequently sieved (mesh size 2 mm). Soil pH was measured potentiometrically in a 1:5 soil:deionised water suspension, and organic carbon content was analysed using the dynamic combustion method [31]. 2.3. Statistical analysis The average number of individuals from the pair of traps was standardized for 100 days (¼cumulative activity densities). Nonparametric Spearman correlation coefficient was used to evaluate the impact of environmental parameters on the activity of dominant species and particular trogloforms of Collembola (trogloxenes, subtroglophiles, eutroglophiles and troglobionts). Correlation analyses were performed using Statistica for Windows version 12 [32]. To point out the community similarities along the depth profile, the Sørensen incidence-based (qualitative) similarity index [33] and the Bray-Curtis (¼Sørensen quantitative) similarity index [34] were calculated for each site using the EstimateS package [35]. Collembolan activities throughout the depth profile were depicted graphically separately for each trogloform. We performed canonical correspondence analysis (CCA) to investigate associations of collembolan communities with environmental parameters
Fig. 1. Subterranean trap design (a e plastic cylinder with openings above each cup, b e plastic cup filled with a 4% formaldehyde solution, c e central iron rod, d e plastic cap).
measured at four depths, with a total of 12 samples/plots (3 sites 4 depths) analysed. Response variables were represented by the activity of selected collembolan species. Species with a total activity of < 4 were arbitrarily excluded from the analysis due to the uncertain relationship with environmental factors. Temperature, organic carbon content and depth were used as explanatory variables. Soil pH, which significantly correlated with temperature (Spearman correlation coefficient), was excluded from the analysis. The data on Collembola activity had a gradient 3.2 SD units along, thus the unimodal CCA method with log transformed data was used (recommended by the Canoco 5 software [36]). 3. Results 3.1. Temperature and chemical characteristics All sites were characterized by similar patterns of temperature regime. The largest temperature fluctuations were observed near the surface (5 cm). Deeper, the amplitudes were lower but synchronized with the climate dynamics on the surface (Fig. 2). The skaly site presented slightly higher temperatures along Belinske the depth gradient compared with Drien canský kras and Malý Ru zínok. With the exception of Malý Ru zínok, we found the average temperature to decline gradually along the depth gradient. Belinske
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skaly had acidic soil, whereas the other two sites had alkaline soil pH, except for the depth of 5 cm at Drien canský kras. The carbon skaly, especially between depths content was very low at Belinske 35 and 95 cm (0.8e0.5%). In contrast to this, Malý Ru zínok was characterized by high organic carbon content even at deeper levels (9.2e8.8%). For the soil at the Drien canský kras site, carbon content decreased in proportion to increasing depth (Table 1). 3.2. Collembola diversity A total of 5271 individuals of Collembola comprising 70 species were sampled across all the investigated sites. The total number of individuals captured at Malý Ru zínok was distinctly higher than at the other sites. The total number of individuals found at Belinske skaly was about twice as high as at Drien canský kras. Distinctly higher species richness was found at Malý Ru zínok, followed by skaly (Appendix). All three sampled Driencanský kras and Belinske sites harboured both eutroglophiles and troglobionts. The highest number of these subterranean forms was observed at Malý Ru zínok (12 eutroglophiles, 2 troglobionts), followed by Drien canský kras (8 skaly (8 eutroglophiles, eutroglophiles, 1 troglobiont) and Belinske 1 troglobiont), (Appendix).
Fig. 2. Monthly fluctuations of temperature along the depth profile of the investigated skaly, DK e Driencanský kras, MR e Malý Ruzínok). scree slopes (BS e Belinske
183
3.3. Vertical distribution of Collembola Vertical distribution of Collembola differed considerably among skaly site was characterized by a the sites studied. The Belinske gradual decrease in activity and species number between the depths of 5 and 35 cm. From 35 cm downwards, both parameters were similar. At Malý Ru zínok, the highest proportions of individuals (59.6%) and species (83.7%) were captured at a depth of 5 cm. The decline in both characteristics was very sharp between 5 and 15 cm. Deeper, the distribution of Collembola showed a similar skaly. In contrast, Drien pattern as at Belinske canský kras was characterized by relatively uniform patterns of total activities and species richness of Collembola within the scree slope (Fig. 3, Appendix). Malý Ru zínok had the most pronounced stratification of collembolan communities across the depth profile. At this site, the
Fig. 3. Distribution of Collembola along the depth gradient of the scree slopes skaly, DK e expressed as a total number of individuals trapped (BS e Belinske Driencanský kras, MR e Malý Ruzínok; * Number of individuals ¼ 2788, ** Species richness ¼ 410, *** Number of individuals ¼ 507, **** Number of individuals ¼ 307).
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184
Table 2 Similarity of collembolan communities along the depth gradient at three scree slope sites. Above the diagonal: the Bray-Curtis index, below the diagonal: the Sørensen incidence-based index. Index values > 0.50 are indicated in bold. Value 1.00 indicates identical communities. Depth
5 cm
skaly Belinske 5 cm e 15 cm 0.48 25 cm 0.33 35 cm 0.21 45 cm 0.40 55 cm 0.40 65 cm 0.32 75 cm 0.21 85 cm 0.21 95 cm 0.20 Drien canský kras 5 cm e 15 cm 0.38 25 cm 0.43 35 cm 0.32 45 cm 0.40 55 cm 0.24 65 cm 0.17 75 cm 0.21 85 cm 0.25 95 cm 0.24 Malý Ru zínok 5 cm e 15 cm 0.48 25 cm 0.49 35 cm 0.34 45 cm 0.43 55 cm 0.37 65 cm 0.41 75 cm 0.46 85 cm 0.36 95 cm 0.41
15 cm
25 cm
35 cm
45 cm
55 cm
65 cm
75 cm
85 cm
95 cm
0.57 e 0.47 0.33 0.62 0.62 0.50 0.33 0.50 0.46
0.25 0.41 e 0.36 0.50 0.50 0.55 0.36 0.36 0.17
0.07 0.12 0.34 e 0.29 0.29 0.33 0.33 0.33 0.29
0.09 0.16 0.39 0.44 e 1.00 0.86 0.57 0.57 0.25
0.16 0.26 0.57 0.31 0.69 e 0.86 0.57 0.57 0.25
0.17 0.29 0.72 0.44 0.59 0.51 e 0.67 0.67 0.29
0.19 0.32 0.72 0.40 0.47 0.47 0.87 e 0.67 0.29
0.06 0.13 0.31 0.63 0.63 0.42 0.48 0.43 e 0.57
0.04 0.09 0.15 0.35 0.35 0.24 0.23 0.21 0.53 e
0.60 e 0.50 0.47 0.15 0.27 0.00 0.35 0.29 0.40
0.25 0.30 e 0.40 0.36 0.31 0.25 0.27 0.17 0.15
0.28 0.42 0.21 e 0.50 0.56 0.31 0.40 0.35 0.44
0.18 0.07 0.29 0.25 e 0.43 0.67 0.38 0.31 0.43
0.09 0.10 0.15 0.34 0.28 e 0.36 0.44 0.27 0.13
0.07 0.00 0.22 0.11 0.55 0.17 e 0.15 0.20 0.18
0.07 0.19 0.11 0.25 0.15 0.19 0.06 e 0.35 0.44
0.10 0.22 0.09 0.33 0.17 0.22 0.11 0.38 e 0.27
0.07 0.19 0.05 0.19 0.21 0.04 0.06 0.67 0.30 e
0.30 e 0.61 0.48 0.75 0.67 0.65 0.55 0.56 0.53
0.10 0.41 e 0.57 0.71 0.55 0.73 0.69 0.71 0.67
0.06 0.25 0.67 e 0.67 0.48 0.55 0.64 0.59 0.55
0.09 0.39 0.72 0.71 e 0.79 0.81 0.77 0.80 0.69
0.09 0.36 0.66 0.62 0.80 e 0.67 0.69 0.64 0.67
0.13 0.29 0.46 0.32 0.45 0.57 e 0.67 0.81 0.71
0.09 0.25 0.44 0.36 0.52 0.68 0.74 e 0.77 0.73
0.05 0.19 0.30 0.18 0.41 0.61 0.53 0.67 e 0.75
0.05 0.16 0.30 0.27 0.45 0.55 0.45 0.56 0.73 e
high degree of quantitative (Bray-Curtis) similarity was recorded in the range of depths 25e55 cm ( 0.62) and depths 55e95 cm ( 0.45). The lowest quantitative similarity was observed between the depths of 5 cm and 85e95 cm (0.05 for both pairs). Furthermore, the Sørensen qualitative similarity index showed that the depth of 5 cm is comparatively different in species composition from the rest of the depth profile. The most similar species skaly was in the range of depth 45e85 cm composition at Belinske (Sørensen index 0.57). No remarkable similarity pattern of the community among the particular depths was observed at Drien canský kras (Table 2). The activity of collembolan trogloforms along the depth profile had comparable patterns at the studied scree slopes (Fig. 4). Trogloxenes were active predominantly in the uppermost level (5 cm), deeper their occurrence was only accidental. On the contrary, troglobionts showed inverted distributional pattern, with predominance at the deepest horizon (95 cm). An exception to this was the Malý Ru zínok site, where troglobiotic collembolans were distributed across the depth profile and had maximum activity between the depths of 55 and 95 cm. The activity of subtroglophiles was characterized by a gradual decrease between 5 and 25 cm and remained constant in the lower depths. Eutroglophiles occurred at all monitored depths and dominated notably in the lower half of skaly. the depth profile, with the exception of Belinske
content. On the other hand, troglobionts showed a negative correlation with temperature. The activity of nine species correlated positively with organic carbon content and one species with pH, whereas five species correlated negatively with temperature. The community data from the 12 plots (3 sites 4 depth) were further processed by CCA ordination analysis (Fig. 5). The total activity assigned to these plots consisted of 60 Collembola species. After exclusion of species with lower activity, the remaining 26 species (97.5% of total activity) were used as response variables and three environmental parameters (depth, temperature and organic carbon content) as explanatory variables, which accounted for 54.2% of total variation. The first two axes, with eigenvalues of 0.44 and 0.36, respectively, explained 48% of the cumulative variance. The permutation test on all axes confirmed their statistical significance (pseudo F ¼ 3.2, p ¼ 0.002). The direction of both temperature and depth arrows indicates a positive correlation between these environmental variables and ordination axes. The species Orchesella multifasciata, Orchesella bifasciata and Pseudosinella horaki were skaly scree slope, characterized by a associated with the Belinske higher temperature at particular depth layers compared with the other sites. Ceratophysella denticulata, Caprainea marginata, Morulina verrucosa, Pseudachorutes dubius, Pogonognathellus flavescens and some other species were grouped with the organic carbon-rich scree layers at Malý Ru zínok, while Pygmarrhopalites pygmaeus and Neelus koseli were species characteristic for the deeper scree layers.
3.4. Impact of environmental variables 4. Discussion Collembola species richness showed a strong positive correlation with organic carbon content (Table 3). Assessing the dependence of trogloforms on environmental variables, we found suband eutroglophiles to be positively correlated with organic carbon
Culver and Pipan [37] stressed that shallow subterranean habitats are highly variable in terms of environmental factors. In the present study, the greatest variability was observed in organic
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185
Fig. 4. Cumulative activity densities of collembolan forms along the depth profile of the scree slopes (Tgx e trogloxenes, Stp e subtroglophiles, Etp e eutroglophiles, Tgb e skaly, DK e Driencanský kras, MR e Malý Ruzínok; trend line: dotted e Belinske skaly, dashed e Driencanský kras, solid e Malý Ruzínok). troglobionts; BS e Belinske
carbon content and its distribution across the depth gradient. Indeed, this parameter is only a proxy for nutrient resources, as Collembola feed on microorganisms dependent on organic material. The scree slope at Malý Ru zínok, overgrown with linden-maple wood, had the highest soil organic carbon content, which was relatively high even at deeper levels. In contrast, the scree at skaly, covered predominantly with oak wood, had a very Belinske low carbon content, especially at depths below 5 cm. The availability of organic carbon to the deeper layers of shallow subterranean habitats depends on several factors, mainly on the
composition of the vegetation cover [4]. The rate of decomposition is determined by the chemical quality of the decaying leaf litter. It is known that leaves of European oak species decompose slowly (over 2e3 years) due to the high concentration of polyphenol-protein complexes in tissues compared with other deciduous leaves [38,39]. The flow of organic carbon from the surface to lower levels of the depth profile is likely to be closely related to the rate of decomposition of vegetation residues. Scree slopes which are partially filled with soil in deeper horizons are thus richer in organic carbon compared with bare screes and mesovoid shallow
Table 3 Spearman correlation coefficients between dominant Collembola species/trogloforms and soil-chemical parameters at the three scree sites and four depth levels. Environmental parameter
Species
Tf
Spearman correlation
T
Troglobionts Desoria tigrina Folsomia fimetaria Megalothorax hipmani Neelus koseli Pygmarrhopalites pygmaeus Pygmarrhopalites pygmaeus
stp stp tgb tgb etp etp
0.717 0.595 0.613 0.668 0.643 0.608 0.582
etp stp stp stp tgb tgb stp etp etp
0.861 0.674 0.797 0.591 0.650 0.832 0.809 0.815 0.587 0.609 0.707 0.648
pHðH2 OÞ Corg
Species richness Subtroglophiles Eutroglophiles Ceratophysella denticulata Ceratophysella silvatica Desoria tigrina Folsomia fimetaria Megalothorax hipmani Neelus koseli Parisotoma notabilis Plutomurus carpaticus Protaphorura armata
T e temperature, pH(H2O) e soil acidity, Corg e organic carbon content; Tf e trogloform, stp e subtroglophile, etp e eutroglophile, tgb e troglobionte.
186
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Fig. 5. CCA ordination triplot indicating associations of collembolan communities and sites with environmental parameters. Eigenvalues of the first two axes were 0.44 and 0.36, skaly :DK e Driencanský kras, -MR e Malý Ruzínok, with a number specifying the depth; respectively (T e temperature, Corg e organic carbon content; sites BBS e Belinske AREL e Pygmarrhopalites elegans, ARPR e P. principalis, ARPY e P. pygmaeus, CAMA e Caprainea marginata, CEDE e Ceratophysella denticulata, CEGR e C. granulata, CESL e C. silvatica, DIOR e Dicyrtomina ornata, DRTI e Desoria tigrina, FOFI e Folsomia fimetaria, FOMA e F. manolachei, ISNO e Parisotoma notabilis, LELI e Lepidocyrtus lignorum, MGHI e Megalothorax hipmani, MOVE e Morulina verrucosa, NLKO e Neelus koseli, OPCR e Oncopodura crassicornis, ORBI e Orchesella bifasciata, ORFL e O. flavescens, ORMU e O. multifasciata, PCDU e Pseudachorutes dubius, PGFL e Pogonognathellus flavescens, PLCA e Plutomurus carpaticus, PRAR e Protaphorura armata, PSHO e Pseudosinella horaki, PSTH e P. thibaudi).
substratum covered with a layer of moss or soil. On the other hand, bare screes are poor in carbon, as their only source of nutrients are fallen leaves brought by wind from adjacent forest, thus the concentration of carbon decreases rapidly at lower levels [11,40]. Dissimilarities among the studied scree slopes were also observed in their internal temperatures. It is apparent that the exposure of a scree slope affects the character of the internal microclimate. This was particularly evident on the southwest skaly which, unlike both northfacing scree slope at Belinske exposed slopes at Driencanský kras and Malý Ru zínok, presented higher values of temperature across the depth profile. Thus, organic carbon content along with the microclimate determined the diversity and distribution of Collembola within the studied forested screes. High organic content and cooler microclimate in the scree slope at Malý Ru zínok was reflected in distinctly higher activities of Collembola, including eutroglophiles and troglobionts. Furthermore, this site was characterized by a much more pronounced vertical stratification of communities along the scree slope profile. In contrast, the carbon-poor and warm scree slope at skaly was occupied mostly by eurytopic species of Belinske Collembola. As have been reported by several authors e.g. Refs. [11,19,41], species richness and abundance of arthropod fauna decrease rapidly with depth in shallow subterranean habitats. Such a distribution pattern was, however, observed in Collembola only at Malý Ru zínok; at the superficial layer both activity and species richness were extremely high compared with deeper layers. The sharp decline of both characteristics is most likely associated with the amount of leaf litter and humus accumulations in the first centimetres of the vertical profile. It is important to note that the vertical stratification of invertebrate communities inhabiting the scree slope may be negatively affected by the excavation of the sampling pit. The dislocation of particular scree slope layers may result in the absence of species sensitive to such disturbance at the beginning of trapping [42].
Although the Collembola sampling in this study was initiated instantly after burying the traps, we assume the disruption of collembolan communities was only slight and lasted only for a short period after burying. Most of the previously published studies e.g. Refs. [14,17,18,43] agreed that shallow subterranean habitats, including scree slopes, are inhabited by a mixture of troglobiotic and non-troglobiotic species. One of the principal objectives of our study was to define a pattern of depth distribution of Collembola according to their affinity to the subterranean realm. The study showed that most of the trogloxenes were exclusively bound to the uppermost level of the depth gradient and that they occurred deeper very rarely. With few exceptions, the majority of subtroglophiles and eutroglophiles had tendency to be distributed across the entire depth gradient. Troglobionts showed a reversed pattern of distribution, with significant predominance in the lower half of the depth gradient. Moreover, they occasionally occurred closer to the surface, at the levels completely filled with the soil. This contradicts the argument of Giachino and Vailati [9], who upon studying beetles stated that screes filled up with soil sediment cannot be colonized by subterranean fauna. It seems that the body size is an important factor limiting the vertical distribution of organisms in shallow subterranean habitats. The body size of most troglobiotic collembolans in this study did not exceed a length of 1.0 mm, which allowed them to colonize even tight spaces in the soil that filled the scree. Among the soil parameters monitored, organic carbon content and temperature were those that ruled the diversity and distribution of Collembola inside the scree slopes. Furthermore, our study showed that activity of subterranean species, both eutroglophiles and troglobionts, correlated with organic carbon. This supports the assumption of Pipan and Culver [44] that the content of organic carbon is an important limiting factor for the occurrence of or skaly ganisms in shallow subterranean habitats. Unlike Belinske and Drien canský kras, the carbon-rich Malý Ru zínok site was inhabited by distinctly higher number of eutroglophiles and
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troglobionts. Moreover, the present study implies that in forested scree deposits with well-developed upper organic horizons microarthropod communities have obvious vertical stratification. However, more data are necessary to make generalizations regarding this issue. Acknowledgement This study was supported by grant 1/0199/14 from the Slovak Scientific Grant Agency VEGA, by grant VVGS-2014-228 of P.J. Saf arik University in Kosice and by Operational Programme “Research & Development” funded from ERDF (Code ITMS: 26220120022, rate 0.4). We express our gratitude to P. Fend’a, R. Zamec (Comenius University, Bratislava), L. Papa cov a and V. Papa c Sobota) for their kind (Slovak Caves Administration, Rimavska assistance during the installation of the subterranean traps. M. skova for Dzurinka is acknowledged for help in the field work, T. Sa (P.J. help in the sorting of captured specimens and A. Parimuchova Saf arik University, Kosice) for sketching the subterranean trap design. We are also thankful to D. McLean for linguistic corrections of the manuscript and anonymous reviewers for their very constructive comments to earlier manuscript version. Appendix A. Supplementary data Supplementary data related to this article can be found at http:// dx.doi.org/10.1016/j.ejsobi.2016.06.001. References [1] V. R u zi cka, Stony debris ecosystems-sources of landscape diversity, Ekologia 12 (1993) 291e298. [2] V. R u zi cka, The first steps in subterranean evolution of spiders (Araneae) in Central Europe, J. Nat. Hist. 33 (1999) 255e256. [3] D.C. Culver, T. Pipan, Superficial subterranean habitatsegateway to the subterranean realm? Cave Karst Sci. 35 (2008) 5e12. [4] D.C. Culver, T. Pipan, Shallow Subterranean Habitats. Ecology, Evolution and Conservation, first ed., Oxford University Press, Oxford, 2014. [5] C. Gers, Ecologie et biologie des arthropodes terrestres du milieu souterrain cologie e volutive, Dissertation, Universite superficiel, functionnement et e Toulouse III, 1992 (in French). [6] V. R u zi cka, Structure and ecology of invertebrates communities of stony debris in Czech Republic, Bull. Soc. Neuchat. Sci. Nat. 116 (1991) 209e214. [7] C. Juberthie, B. Delay, M. Bouillon, Extension du milieu souterrain en zone non calcaire: description d’un nouveau milieu et de son peuplement par les opte res troglobies, Me m. Biospe ol. 7 (1980) 19e52 (in French). cole [8] T. Novak, P. Matja z, S. Lipovsek, F. Jan zekovi c, Duality of terrestrial subterranean fauna, Int. J. Speleol. 41 (2012) 181e188. [9] P.M. Giachino, D. Vailati, The Subterranean Environment. Hypogean Life, Concepts and Collecting Techniques, first ed., WBA Handbooks, Verona, 2010. pez, P. Oromí, S. Polak, D.C. Culver, Temperature variation and [10] T. Pipan, H. Lo the presence of troglobionts in terrestrial shallow subterranean habitats, J. Nat. Hist. 45 (2011) 253e273. [11] C. Gers, Diversity of energy fluxes and interactions between arthropod communities: from soil to cave, Acta Oecol. 19 (1998) 205e213. mcova , P. Smilauer, [12] V. R u zi cka, M. Zacharda, L. Ne J.C. Nekola, Periglacial microclimate in low-altitude scree slopes supports relict biodiversity, J. Nat. Hist. 46 (2012) 2145e2157. ncil ias¸u, Scree habitats: [13] E. Nitzu, A. Nae, R. Ba a, I. Popa, A. Giurginca, R. Pla ecological function, species conservation and vertical-temporal variation in the arthropod community, Syst. Biodivers. 12 (2014) 65e75. [14] C. Juberthie, The diversity of the karstic and pseudokarstic hypogean habitats in the world, in: H. Wilkens, D.C. Culver, W.F. Humphreys (Eds.), Subterranean Ecosystems, Elsevier, Amsterdam, 2000, pp. 17e39. [15] C. Juberthie, V. Decu, Interstitial habitats (terrestrial), in: J. Gunn (Ed.), Encyclopedia of Caves and Karst Science, Taylor and Francis, New York, 2004, pp.
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