Influence of tree species and soil properties on ground beetle (Coleoptera: Carabidae) communities

Acta Oecologica 91 (2018) 120–126

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Influence of tree species and soil properties on ground beetle (Coleoptera: Carabidae) communities

T

Vladimír Viciana, Marek Svitokb,c, Eva Michalkováb, Ivan Lukáčikd, Slavomír Stašiovb,∗ a

Department of Lanscape Planing, Faculty of Ecolgy and Environmental Sciences, Technical University in Zvolen, T. G. Masaryka 24, SK-96053, Zvolen, Slovakia Department of Biology and General Ecology, Faculty of Ecology and Environmental Sciences, Technical University in Zvolen, T. G. Masaryka 24, SK-96053, Zvolen, Slovakia c Department of Ecosystem Biology, Faculty of Science, University of South Bohemia, Branišovská 1760, CZ-370 05, České Budějovice, Czech Republic d Borová Hora Arboretum, Technical University in Zvolen, Borovianská cesta 66, SK-960 53, Zvolen, Slovakia b

A R T I C LE I N FO

A B S T R A C T

Keywords: Arboretum Carabids Forest Soil conditions Bioindication

Although Carabidae is among the best-studied families of beetles in Europe from the faunistic point of view, there is still a lack of available information on the ecological requirements of the particular carabid species. The habitat preferences that determine the distribution of species are largely influenced by habitat structure and microclimate. In addition to other factors, these habitat parameters are influenced by the nature of the vegetation. Therefore, our study investigated the influence of tree species on carabid beetle communities. We conducted the research at 9 stands in the Borová Hora Arboretum (Zvolen, Central Slovakia). Each studied site represents a monoculture of one of nine tree species. At each site, some soil and leaf litter attributes (pH, conductivity, and content of H, C, N and P) were evaluated. Ground beetles were collected by pitfall trapping during the vegetation periods in 2008–2011. In total, 3012 individuals of 29 species were obtained. Significant differences in the total dynamic activity and species richness of the carabid beetle communities among the compared forest stands were revealed. The results of the research confirmed statistically significant relationships among 1) the soil conductivity and both the richness and Shannon diversity of the ground beetle communities, 2) the litter and soil N content and richness, the Shannon diversity and the species composition of the ground beetle communities. The Shannon diversity and richness were negatively related to the soil conductivity and positively related with the N content. Our research showed that dominant tree species indirectly influence diversity and composition of carabid communities via the soil properties.

1. Introduction Carabids are terrestrial beetles. Although carabids live mainly on the soil surface, some species occasionally live on vegetation. They prey on various invertebrates in different growth stages. In this way, carabid beetles participate in the maintenance of the natural equilibrium of a wide range of habitats (Hůrka, 1996). European carabids are useful model organisms and possibly useful environmental indicators because they are diverse and well-known both taxonomically and ecologically; they efficiently reflect biotic and abiotic conditions, are relevant at multiple spatial scales, and are easy to collect in sufficiently large numbers to allow statistical analyses (Koivula, 2011). Vegetation cover-related variables, such as moisture, temperature and shade are considered the main drivers of diversity of ground beetle communities since the distribution of carabid species is markedly

influenced by microclimatic conditions (e.g., Diefenbach and Becker, 1992; Kostova, 2015; Moraes et al., 2013; Niemelä, 1996; Šustek, 2004; Thiele, 1977; Voronin, 1995). In forest habitats, species composition and structure of a tree layer plays an important role since litter and soil quality and quantity greatly affect niche availability for carabids (e.g. Sklodowski, 2014; Yanahan and Taylor, 2014). Carabid beetles are also sensitive to anthropogenic abiotic conditions, such as pesticide use in agro-ecosystems and the contamination of soils with heavy metals (Butovsky, 2011). Carabids might thus reflect ecological sustainability and ‘ecosystem health’. Therefore, carabids may potentially serve as keystone indicators (Koivula, 2011). Several authors have studied the influence of tree species on the composition of carabid beetle communities. For example, Apigian and Wheelwright (2000) found that the mixed forest support higher total dynamic activity than monospecific stands. Also diversity of carabid

∗

Corresponding author. E-mail addresses: [email protected] (V. Vician), [email protected] (M. Svitok), [email protected] (E. Michalková), [email protected] (I. Lukáčik), [email protected] (S. Stašiov). https://doi.org/10.1016/j.actao.2018.07.005 Received 19 March 2018; Received in revised form 3 July 2018; Accepted 14 July 2018 1146-609X/ © 2018 Published by Elsevier Masson SAS.

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PB – stand of downy birch (Betula pubescens Ehrh.), geographic coordinates (GC) – 48°35′45.8″ N and 19°08′09.3″ E, stand canopy (SC) – 50%, altitude (A) – 340 m, exposure (E) – north-northwest, pedogenic substrate (PS) – tuff material slope deposits, sporadically with small additions of silt loams and siliceous gravels, soil (S) –saturated typical Cambisols, PS – stand of Scots pine (Pinus sylvestris L.), GC – 48°35′47.2″ N and 19°08′16.5″ E, SC – 50%, A – 345 m, E − north, PS – silt loam slope deposits and slope deposits of kaolinised andesite tuff, S – Albic Luvisols, LD – stand of European larch (Larix decidua (Mill.)), GC – 48°35′49.1″ N and 19°08′23.0″ E, SC – 60%, A – 350 m, E − north, PS – tuff material slope deposits and slope deposits of kaolinised andesite tuff, S – saturated typical Cambisols, CB – stand of European hornbeam (Carpinus betulus L.), GC – 48°36′03.8″ N and 19°08′42.1″ E, SC – 80%, A – 310 m, E − northnortheast, PS – tuff material slope deposits with larger addition of siliceous gravels, S – saturated typical Cambisols with additions of siliceous gravels, AA – stand of European silver fir (Abies alba Mill.), GC – 48°35′55.1″ N and 19°08′30.1″ E, SC – 100%, A – 330 m, E − north, PS – tuff material slope deposits with larger additions of siliceous gravels, P – two-substratum Albic Luvisols, PA – stand of Norway spruce (Picea abies (L.) Karst.), GC – 48°35′51.1″ N and 19°08′26.7″ E, SC – 80%, A – 335 m, E − north, PS – silt loam slope deposits and slope deposits of kaolinised andesite tuff, S – two-substratum Albic Luvisols, AI – stand of grey alder (Alnus incana (L.) Moench), GC – 48°35′57.8″ N and 19°08′02.8″ E, SC – 80%, A – 290 m, E − none, PS – mainly medium grain size alluvial deposits of the Hron River, S – carbonate Glei patterns, PN – stand of black poplar (Populus nigra L.), GC – 48°35′58.7″ N and 19°08′06.5″ E, SC – 50%, A – 290 m, E − none, PS – mainly medium grain size alluvial deposits of the Hron River, S – carbonate Glei patterns, UL – stand of European white elm (Ulmus laevis Pall.), GC – 48°35′54.0″ N and 19°07′58.0″ E, SC – 70%, A – 315 m, E − northnorthwest, PS – silt slope deposit with additions of travertine in the top layers (20–30 cm), S – calcareous Cambisols.

beetle communities is linked to tree species composition (Zou et al., 2015). Podrázský et al. (2010a,b) summarised the literature on the bioindication potential of ground beetle communities in forest ecosystems and found that ground beetle communities reflect the tree species composition more than the stand structure and that the carabid communities sensitively mirror changes in tree species compositions. In contrast, the effect of soil properties, which are driven by tree species (Binkley and Giardina, 1998), on carabid beetle communities is relatively understudied. Only few studies examined the importance of soil types and soil physico-chemical properties for carabid beetles (e.g., Baker and Dunning, 1975; Spomer et al., 2015). A research focused on the both, soil- and vegetation-effects, is generally missing (but see Sklodowski, 2014). Here, we examine the hypothesis that tree species influence soil and leaf litter attributes (pH, conductivity, and content of H, C, N and P) which, in turn, affect ground beetle communities. The Borová Hora Arboretum is especially suitable for this purpose because it enables the assessment of the different ecological properties of various tree species within homogenous area. 2. Material and methods 2.1. Study stands The Borová Hora Arboretum is an important educational and research facility, of the Technical University in Zvolen. The planting of trees started at the arboretum in 1965 (Lukáčik et al., 2005). The arboretum is located near the middle reach of the Hron River in Central Slovakia, approximately 3 km northwest of the centre of Zvolen, from 48°35′42´´ to 48°36′06´´ N and 19°07′58´´ to 19°10′00´´ E. It lies on the southwestern foot of the Zvolenská Pahorkatina hills. The arboretum has hills ranging in altitudes from 290 m (in the northwestern part) to 377 m in the eastern part (Labanc and Čížová, 1993). The town of Zvolen belongs to a warm region, with a moderately humid climate and cold winters. The mean annual temperature of this region is +8.8 °C, and the mean temperature during the vegetation period is +15.6 °C. The mean annual amount of precipitation is 640 mm, with 399 mm during the vegetation period (Čížová, 2005). The research was carried out on 9 stands. The minimum distance between the stands was 100 m. They differed by tree species, and some soil and leaf litter attributes (Table 1). An overview and brief description of the studied stands are given below according to the data of Pagan et al. (1975):

2.2. Methods The research was carried out between 2008 and 2011. Carabid

Table 1 Measured physico-chemical parameters of soil (s) and leaf litter (l) samples of the studied stands. Stand/layer

Tree species

pH/H2O

κ [μS.cm−1]a

H [%W]b

C [%W]b

N [%W]b

P [mg.kg−1]

BP/s BP/l PS/s PS/l LD/s LD/l CB/s CB/l AA/s AA/l PA/s PA/l AI/s AI/l PN/s PN/l UL/s UL/l

Betula pubescens Betula pubescens Pinus sylvestris Pinus sylvestris Larix decidua Larix decidua Carpinus betulus Carpinus betulus Abies alba Abies alba Picea abies Picea abies Alnus incana Alnus incana Populus nigra Populus nigra Ulmus laevis Ulmus laevis

5.6 5.8 4.7 4.5 5.0 4.2 6.5 5.5 4.8 5.4 4.5 5.6 7.0 5.6 7.2 6.9 7.1 6.0

428 1000 175 350 146 740 500 770 310 970 98 790 380 770 315 1300 473 745

2.04 6.37 1.76 4.84 1.56 4.64 1.74 4.52 1.59 4.06 1.48 4.13 1.48 4.76 1.41 3.55 1.74 4.64

6.0 45.6 2.9 35.3 2.2 33.9 4.2 30.6 4.1 29.0 2.6 29.5 5.0 33.8 3.8 24.8 8.4 29.5

0.38 0.45 0.24 0.56 < 0.01 0.46 0.31 0.66 0.32 0.85 0.21 0.66 0.43 0.73 0.27 0.93 0.63 0.78

19.8 204.0 14.5 104.0 6.6 130.0 24.3 228.0 37.0 199.0 8.1 130.0 15.5 161.0 6.8 177.0 102.0 249.0

a b

Conductivity in H2O extract. % weighted. 121

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we have used diversity values standardized by rarefaction to a common abundance level (n = 75 ind.) to ensure comparability across stands (Chao et al., 2014). In order to investigated sample completeness, we calculated expected total number of species present in the assemblage using Chao1 estimator (Chao, 1984). Generalised linear models (GLM, McCullagh and Nelder, 1989) were used to assess the relationships between the diversity measures and soil conditions (Table 1). As a first step, we screened the soil data for pairwise correlations and removed %C(s) and %C(l) from the dataset due to their strong correlations with other variables, especially with %N (Pearson's r > 0.8). We calculated variance inflation factors (VIFs) to verify that the full GLMs did not show considerable multicollinearity patterns (VIF < 10, Quinn and Keough, 2002). Since rarefied richness and Shannon diversity take only positive values, and their variances increased with the mean, a GLM with inverse link-function and gamma error distribution was chosen to fit these data. We built parsimonious GLMs via the sequential deletion of the non-significant terms (p ≥ 0.05) based on the likelihood ratio F tests. The final models were displayed as effect plots (Fox, 2003). Principal component analysis (PCA) on the correlation matrix of physico-chemical properties was used to summarise differences in the physico-chemical properties of the soil and leaf litter samples taken at stands with different tree species. Canonical correspondence analysis (CCA) was used to relate the Carabidae community composition (species presence/absence) to soil variables. A forward selection procedure accompanied by permutation tests (9999 unrestricted permutations) was used to select the most parsimonious model. Statistical analyses were performed in Spade (Chao and Shen, 2010) and R language (R Core Team, 2016) using the libraries iNEXT (Hsieh et al., 2016) and vegan (Oksanen et al., 2016).

beetles were captured by pitfall trapping, by using glass cups with an opening diameter of 5.5 cm and a volume of 0.3 l. The fixation fluid in the traps (approximately one-third of the trap volume) was 1% formaldehyde (Barber, 1931). A drop of ethylene glycol was use as a detergent. The traps were covered by a small metal roofs to prevent overfilling by a rain water and leaf litter. At each site, we placed 3 traps along a line, with a distance of 5 m between neighbouring cups (a total of 27 traps for all the tested stands). The traps were active from midMarch to mid-December in every year and emptied at three-month intervals. This approach is frequently used in the research of ground beetle communities (Greenslade, 1964; Zou et al., 2012; Siewers et al., 2014). The contents of the three traps at each site and date were merged. In this way, one composite collection was obtained from each site every period. The obtained biological material was sorted in the laboratory. Carabid beetles were determined to the species level according to (Hůrka, 1996). Specimens were fixed in 80% ethyl alcohol and deposited at the Faculty of Ecology and Environmental Sciences of the Technical University in Zvolen, Department of Biology and General Ecology. All soil and leaf litter samples for chemical analyses were taken on 28 December 2009 in order to ensure comparability among stands. Five soil samples (to a depth of 10 cm) and five leaf litter samples, all approximately 100 g each, were taken from five different randomly chosen spots at each site. At each site, the multiple soil samples were combined into a single composite sample (Gregorich and Carter, 2007). The same procedure was applied to the leaf litter samples. From the primary data, the mean species dynamic activity per day and per trap were calculated in order to assess the diversity, equability and similarity of the carabid beetle communities. The species diversity was quantified as species richness and the Shannon diversity (Jost, 2006). Since sample sizes varied considerably among plots (Table 2),

Table 2 Total number of carabid specimens and chosen parameters of the carabid communities recorded at the studied stands. Taxon

BP

PS

LD

CB

Carabus scheidleri Panzer, 1799 Carabus ullrichii Germar, 1824 Carabus granulatus Linnaeus, 1758 Carabus hortensis Linnaeus, 1758 Carabus convexus Fabricius, 1775 Carbus intricatus Linnaeus, 1761 Carabus violaceus Linnaeus, 1758 Leistus ferrugineus (Linnaeus, 1758) Nebria brevicollis (Fabricius,1792) Notiophilus biguttatus (Fabricius, 1799) Aptinus bombarda (Illiger, 1800) Brachinus crepitans (Linnaeus, 1758) Poecilus cupreus (Linnaeus, 1758) Pterostychus oblongopunctatus (Fabricius, 1787) Pterosytchus niger (Schaler, 1783) Pterostychus melanarius (Illiger, 1798) Pterostychus strenuus (Panzer, 1797) Abax ovalis (Duftschmid, 1812) Abax parallelepipedus (Piller et Mitterpacher, 1783) Molops piceus (Panzer, 1793) Calathus fuscipes (Goeze, 1777) Acupalpus elegans Dejean, 1829 Platynus assimilis (Paykull, 1790) Amara sp. Trichotichnus laevicollis(Duftschmid, 1812) Ophonus stictus (Fabricius, 1775) Pseudoophonus rufipes (De Geer, 1774) Harpalus affinis (Schrank, 1781) Licinus depressus (Paykul, 1790) Total abundance Species richness Rarefied species richness (n = 75) Shannon diversity Rarefied Shannon diversity (n = 75)

6 6

3 3

14 19

1

13

4 16

101

10 7

11

60

157

5 4

1 3 2 21 1 1 27 3

2 1 22 72 159 1 19 17 11

74 1 1

31 4

43

169 6

AA

PA

4 1 10 54 14

1

44 21 5 4 18

3 5

446 19 13.7 8.6 7.8

574 18 11.0 7.7 7.0

122

320 12 9.9 5.1 4.8

3 3 7 55 2 17

46 46 41 204 328 3 365 9 225 5 229 8 38 34 453 665 5 48 49 96 17 1 1 3 26 12 28 26 1 3012 16 11.2 4.8 4.4

22

23

2

6 2 14 23

1

14 5 103 189

3 1 35 63

2 3 2 2

2

7 3 35 40 1 1 4 5 2 1

2 13

7 2 5 1

15

13 15

6 1

1

16 12

∑

15

2 4 2 1

1 7 3 1 263 16 11.2 4.8 4.4

UL

10 4 14 1 1

52

4 1

9 14 78 68

1 19

PN 15 4 17 47 53 1 95

1

3 1 135 134 2 10 5 22

AI

206 17 13.0 8.5 7.9

75 15 15.0 9.2 9.2

314 20 13.6 9.3 8.4

8 1 2 4 7 5 608 20 13.1 8.7 7.7

206 15 11.6 6.8 6.3

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Fig. 1. Results of PCA showing relationships between the physico-chemical properties of the soil (black circles) and leaf litter (white circles) of the stands with different tree species. Ordination scores are scaled symmetrically. Variations explained by the ordination axes are displayed in parentheses. The stand name abbreviations are explained in the Study stands section.

3. Results

was observed at the BP with downy birch site (0.45) that was associated with the PS and LD stands. These results suggest that environmentally similar stands also had similar community compositions. C. granulatus and O. stictus preferred the AI with grey alder and PN with black poplar stands that represented fragments of floodplain forests, as stated above. P. rufipes preferred the BP with downy birch and PS with Scots pine stands. Both of these stands were characterised by a relatively low leaf litter N content. A. bombarda preferred the CB with European hornbeam site, which was characterised by the second highest leaf litter P content. The GLMs revealed that soil conductivity and the soil N content and soil conductivity and the litter N content had statistically significant effects on rarefied species richness (F(2,6) = 7.83, p = 0.0213) and Shannon diversity (F(2,6) = 8.54, p = 0.0176), respectively. Species richness was negatively related with soils conductivity (β [95% conf. limits]: −0.014 [-0.021, −0.007]) and positively related with the soil N content (0.010 [0.006, 0.036]) (Fig. 3). Due to a strong correlation between the both diversity measures (Pearson's r = 0.89, t(7) = 5.2, p = 0.0012), similar pattern emerged for the Shannon diversity; negative relationship with soils conductivity (−0.029 [-0.044, −0.014]) and positive relationship with the litter N content (0.021 [0.006, 0.036]).

In total, 3012 ground beetles specimens from 29 species were obtained during the investigation. Chao1 estimator of 32 (95% conf. interval: 29–55) implies that three species remain undetected. The total dynamic activity values of the carabids and selected carabid community parameters of the studied stands are shown in Table 2. PCA showed a clear trend in the physico-chemical properties of the soil and leaf litter samples (Fig. 1). Across all species, the leaf litter samples had a higher relative content of H, C, N and P than the soil samples. The stands of different trees were distributed along a pH gradient. Acidity gradually increased from the stands with deciduous species (elm, poplar and alder) towards conifers (spruce, pine and larch), which suggests a considerable effect of tree species on pH. Moreover, tree species appears to have affected the relative nitrogen content and conductivity. Stands with conifers showed a lower conductivity and %N than stands with deciduous species. The species composition was significantly related to the litter N content only (CCA, pseudo-F = 2.08, p < 0.0001) which explained 22.9% of the variation in the carabid presence/absence data (Fig. 2). The PS with Scots pine and LD with European larch stands were characterised by relatively low soil N contents (0.56 and 0.46% weighted, respectively), in contrast to the AA with European silver fir and UL with European white elm stands, which were characterised by a higher soil N content (0.85 and 0.78% weighted, respectively). The CB with European hornbeam and PA with Norway spruce stands had identical soil N contents (0.66% weighted) (Table 1). A relatively low soil N content

4. Discussion The quite varied species composition of carabid beetle communities recorded in the territory of the Borová Hora Arboretum is probably related to the diversity of the local habitats, which is affected by the Fig. 2. Results of CCA showing relationships between the compositions of ground beetle communities and the litter N content. Scaling of ordinations is focused on sample distances (left) and species correlations (right). Variations explained by the ordination axes are displayed in parentheses. The stand name abbreviations are explained in the Study stands section.

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Fig. 3. GLM results showing the relationships between the rarefied species richness, soil conductivity and N content. Lines represent fitted relationships holding the other variable constant ± 95% confidence intervals (grey areas).

investigations to elucidate which of the abovementioned factors greatly influence the species richness and abundance of carabid beetle communities and how these values are affected. Nevertheless, all the mentioned attributes (except for stand canopy) can potentially affect the species richness because they were identical to the values of other stands with a high recorded species richness (AI with grey alder) that also represented floodplain forest fragments. Moisture could play an especially important role in supporting high species richness at both stands because most carabid species have specific moisture condition requirements. The influence of moisture on carabids was confirmed, for example, by Voronin (1995), who studied distinguishing ecological groups of ground beetles according to the similarity of their biotopic distribution and moisture responses in the Middle Urals forest zone (Russia). This author distinguished three groups of carabid species according to their moisture responses and suggested their original classifications. The effect of humidity on carabid beetle assemblages was also confirmed elsewhere (e.g., Šustek, 2004; Sklodowski, 2014). Several studies have also showed the positive influence of relatively high soil and leaf litter pH and leaf litter N content on the abundance and species richness of ground beetle communities that was observed at the PN with black poplar stand in the present work. According to these studies, soils with a rich reserve of organic material, neutral pH and high content of C and N were suitable for most edaphone groups, including carabids (Weibull et al., 2003; Petřvalský et al., 2005, 2007; Porhajašová et al., 2008, 2010; Stašiov et al., 2012; Vician et al., 2015 and others). The high total dynamic activity of the carabid beetle communities recorded at the PN with black poplar stand could be affected by the low stand canopy because low stand canopy was also recorded the LD with European larch and PS with Scots pine stands that had the second and third highest numbers of captured individuals (Table 2). These two stands (LD and PS) were also characterised by a relatively high species richness (Table 2). Canopy, in combination with the other factors (e.g., relief and habitat structure), affects the microclimatic conditions of habitats that greatly determine the distribution of carabids. Other authors have also referred to the influence of stand canopy on carabids. Šustek (2004) proposed a four-degree scale of species based on their relation to vegetation cover (shadowing), where 1 indicates heliophilous species that prefer habitats with discontinuous vegetation, 2 – habitats without woody vegetation, 3 – habitats with sparse woody vegetation or species indifferent to shadowing and 4 – forests species. At the PN with black poplar stand, relatively high values of total dynamic activity and species richness of the harvestman (Opliones) communities (Stašiov et al., 2017) and millipede (Diplopoda) communities (Stašiov et al., 2012) have also been recorded.

vegetation and soil conditions (modified by vegetation), as well as by the location of the arboretum within the boundaries of a closed forest (the northern side), grassland (the eastern side) and an urbanised environment (the southern and western sides). Our study showed an indirect effect of the dominant tree species on carabid beetle communities via the tree influence on soil properties (see references below). The results revealed significant differences in the total dynamic activity, species structure, Shannon diversity and species richness between the carabid beetle communities of the studied stands. The factor that probably determined the microclimatic conditions and soil properties of the studied stands was tree species. In addition to tree species, the carabid beetle communities are also related to the quality of leaf litter and soil. An important soil feature is the leaf litter N content. The results of our research confirmed statistically significant relationships between the N content and the richness, Shannon diversity and species composition of ground beetle communities. The litter N content may have an indirect impact (through saprophages, prey of carabid beetles) on the food available for ground beetles. Leaf litter rich in nitrogen is an attractive source of food for saprophages. Therefore, such material decomposes by the activity of saprophages more quickly (Wittich, 1942, 1943). The importance of nitrogen as the main element determining the animal production and food resources for invertebrates, including carabids, has been reported by Dunger (1958). Another important soil feature is electrical conductivity. Electrical conductivity has been used as a surrogate measure for soil properties such as salinity, moisture content, topsoil depth, and clay content (Sudduth et al., 2001). According to Atul Kumar (2015), electrical conductivity is a strong soil health indicator and is positively correlated with the content of organic C, P, K, Fe, S and Mn in the soil. A positive correlation between the electrical conductivity and the organic carbon content and available nutrients of soil samples was also confirmed by Chaudhari and Ahire (2013). The scope and focus of our research do not allow us to reliably clarify the negative effect of litter conductivity on carabid beetle communities. Nevertheless, conductivity may have, analogous to the litter N content, an indirect impact the food that is available for ground beetles by influencing the prey of carabid beetles (litter consumers); consequently, the competitive relationships among species are also affected. This may result in changes in species composition and species proportions in a community. The stand that offered the most favourable conditions for carabids based on the total dynamic activity and species richness (PN with black poplar) (Table 2) is a fragment of a floodplain forest characterised by a relatively high soil moisture, leaf litter pH, and leaf litter N and a low stand canopy (50%). Well-designed research could enable future 124

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communities and report novel findings about the effect of soil conductivity and nitrogen content on ground beetles. We specifically showed a link between dominant tree species and carabid beetle communities mediated by soil conductivity and nutrient content litter and soil.

In terms of total dynamic activity, PA with Norway spruce stand offered the most unsuitable conditions for carabids. Relatively few carabid species were recorded at this stand. In addition, Pearce et al. (2003) recorded fewer carabid species and individuals in spruce stands than mixedwood and deciduous mature boreal forest types. Similarly, relatively few carabid individuals were captured at the AA stand with coniferous tree species (European silver fir). Nevertheless, the data recorded at PA and AA stands cannot be generalised for all studied stands with coniferous tree species because high values of total dynamic activity and species richness for carabid beetle communities were recorded at two other stands with coniferous tree species (PS with Scots pine and LD with European larch). However, in contrast with the PA and AA stands, which were as the only studied sites characterised by a high stand canopy and the absence of a herb layer, stands PS and LD had a low canopy and relatively dense herb cover. This suggests that forest stands without the herb layers are less suitable for carabids or their prey because they offer few refuges for both. The influence of the herb layer on some carabid species was confirmed also by Magura et al. (2000). They determined that the herb layer was a significant positive predictor for Carabus coriaceus (Linnaeus, 1758). In the Borová Hora Arboretum, the herb layer positively influenced dynamic activity, especially that of C. violaceus, which dominated three stands with a dense herb layer (PN with black poplar, LD with European larch, and PS with Scots pine) (Table 2). The lowest carabid species richness was recorded on the CB with European hornbeam stand. This stand was part of a large forest that continued beyond the boundary of the arboretum. A similar result was also observed for harvestmen at stand CB (Opiliones) (Stašiov et al., 2017). In contrast, a previous study recorded the second highest millipede species richness on this stand (Stašiov et al., 2012). The interpretation of these discoveries is difficult, although it is a fact that carabids and harvestmen are predators, while millipedes are detritivores. Hristovski et al. (2016) determined a negative relationship between forest stand area and carabid abundance. These authors studied the effects of microhabitats and forest fragmentation on the composition and species abundance of a ground beetle community at three different beech forest patches on Mt. Osogovo (Macedonia). They found the lowest total carabid abundance in the continuous forest, and beetle catches increased as the size of the fragment decreased. The results of this study revealed that an arboretum can provide favourable conditions for carabid beetle communities with high species richness. The distribution of some species on individual stands was also influenced by their relatively large mobility. Due to this mobility, ground beetles can temporarily be present at stands that do not have optimal conditions, since ground beetles may pass through these stands when they are looking for suitable habitats. This is especially true of adjacent forest stands that were not separated by open habitats. Therefore, the species composition of surrounding habitats has a major impact on the structure of the carabid beetle communities of the individual stands, particularly their species richness. Distinguishing between permanent and temporary members of carabid beetle communities at individual stands is difficult, especially for an area as small as an arboretum, where some forest stands are only a few tens of metres apart.

Author contributions S.S. conceived and designed the study. S.S., V.V. and I.L. performed the field survey. V.V. and E.M. processed and analysed biological and soil samples in the laboratory. M.S. conducted statistical analysis of the data. S.S. and M.S. wrote the manuscript. Acknowledgement We are grateful to Ján Beňo, Lenka Hazuchová, Šimon Kertys, Mária Pavlíková, Andrea Uhlíková, Peter Urblík, and Lucia Miňová, for their help in the field-work. The work was supported from European Regional Development Fund-Project "Mechanisms and dynamics of macromolecular complexes: from single molecules to cells" (No. CZ.02.1.01/0.0/0.0/15_003/0000441) and from the Slovak Grant Agency VEGA (No. 2/0052/15). References Apigian, K., Wheelwright, N.T., 2000. Forest ground beetles (Coleoptera, Carabidae) on a boreal island: habitat preferences and the effect of experimental removals. Can. Entomol. 132, 627–634. Atul Kumar, H.P., 2015. Electrical conductivity in relation with macro-micro nutrients of agricultural soil of Amereli district. Int. J. Humanit. Arts Med. Sci. 3, 25–30. Baker, A.N., Dunning, R.A., 1975. Some effects of soil type and crop density on the activity and abundance of the epigeic fauna, particularly Carabidae, in sugar-beet fields. J. Appl. Ecol. 12, 809–818. Barber, H.S., 1931. Traps for cave-inhabiting insects. J. Elisha Mitchell Sci. Soc. 46, 259–266. Binkley, D.A.N., Giardina, C., 1998. Why do tree species affect soils? The warp and woof of tree-soil interactions. Biogeochemistry 42, 89–106. Butovsky, R.O., 2011. Heavy metals in carabids (Coleoptera, Carabidae). ZooKeys 100, 215–222. Chao, A., 1984. Nonparametric estimation of the number of classes in a population. Scand. J. Stat. 11, 265–270. Chao, A., Shen, T.-J., 2010. Program SPADE (species prediction and diversity estimation). Program and User′s Guide published at. http://chao.stat.nthu.edu.tw, Accessed date: 11 December 2015. Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K., Ellison, A.M., Chao, A., Gotelli, N.J., Hsieh, T.C., Sander, E.L., Ma, K.H., Colwell, R.K., Ellison, A.M., 2014. Rarefaction and extrapolation with Hill numbers: a framework for sampling and estimation in species diversity studies. Ecol. Monogr. 84, 45–67. Chaudhari, P.R., Ahire, D.V., 2013. Electrical conductivity and dielectric constant as predictors of chemical properties and available nutrients in the soil. J. Chem. Biol. Phys. Sci. 3, 1382–1388. Čížová, M., 2005. Meteorologické pozorovania v Arboréte Borová hora. In: Lukáčik, I., Škvareninová, J. (Eds.), Proceedings: Autochtónna Dendroflóra a Jej Uplatnenie V Krajine; 2005, June 15–16; Zvolen. Technical University in Zvolen, Zvolen, Slovakia, pp. 82–83 CD-ROM. 8. Diefenbach, L.M.G., Becker, M., 1992. Carabid taxocenes of an urban park in subtropical Brazil: I. specific composition, seasonality and constancy (Insecta: Coleoptera: Carabidae). Stud. Neotrop. Fauna Environ. 27, 169–187. Dunger, W., 1958. Über die der Zersetzung Laubstreu durch die Boden-Makrofauna im Auenwald. Zool. Jahrb. Syst. 86, 139–180. Fox, J., 2003. Effect displays in R for generalised linear models. J. Stat. Software 8, 1–27. Greenslade, P.J.M., 1964. Pitfall trapping as a method for studying populations of Carabidae (Coleoptera). J. Anim. Ecol. 39, 301–310. Gregorich, E.G., Carter, M.R., 2007. Soil Sampling and Methods of Analysis. CRC Press, Boca Raton. Hristovski, S., Cvetkovska-Gjorgievska, A., Mitev, T., 2016. Microhabitats and fragmentation effects on a ground beetle community (Coleoptera: Carabidae) in a mountainous beech forest landscape. Turk. J. Zool. 40, 402–410. Hsieh, T.C., Ma, K.H., Chao, A., 2016. iNEXT: INterpolation and EXTrapolation for Species Diversity. R Package Version 2.0.12. Hůrka, K., 1996. Carabidae of the Czech and Slovak Republics: Illustrated Key. Kabourek, Zlin). Jost, L., 2006. Entropy and diversity. Oikos 113, 363–375. Koivula, M.J., 2011. Useful model organisms, indicators, or both? Ground beetles (Coleoptera, Carabidae) reflecting environmental conditions. ZooKeys 100, 287–317. Kostova, R., 2015. Ground beetles (Coleoptera Carabidae) diversity patterns in forest habitats of high conservation value, Southern Bulgaria. Biodivers. J 6, 341–352. Labanc, J., Čížová, M., 1993. Arborétum Borová Hora Technickej Univerzity Vo Zvolene.

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