The effect of mesoclimate on Collembola diversity in the Zádiel Valley, Slovak Karst (Slovakia)

european journal of soil biology 44 (2008) 463–472

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Original article

The effect of mesoclimate on Collembola diversity in the Za´diel Valley, Slovak Karst (Slovakia) Nata´lia Raschmanova´a,*, L’ubomı´r Kova´cˇ a,b, Dana Miklisova´b a

Institute of Biology and Ecology, Faculty of Science, P.J. Sˇafa´rik University, Moyzesova 11, SK-04654 Kosˇice, Slovakia Institute of Zoology, Slovak Academy of Sciences, Lo¨fflerova 10, SK-04001 Kosˇice, Slovakia

b

article info

abstract

Article history:

In 2002–2004 an investigation of Collembola communities in the Za´diel Valley (Slovak

Published online 24 August 2008

Karst, Slovakia) was carried out. The karst valley is characterised by climatic and vegetation inversion. To assess the effect of mesoclimate inversion upon soil Collembola five sites

Keywords:

were selected in hypsometric sequence from the karst plateau down the valley: (1) sub-

Collembola

xerophilous pasture – ass. Glechomo–Festucetum, (2) lime wood – ass. Mercuriali–Tilietum, (3)

Diversity

beech wood – ass. Dentario bulbiferae-Fagetum, (4) maple–hornbeam wood – ass. Aceri–Car-

Mesoclimate

pinetum, and (5) secondary oak wood. In total 152 soil Collembola species were collected,

Climatic inversion

the numbers for particular sites ranging between 70 and 108. Evidently higher species

Slovakia

richness was observed in soil of the beech wood compared to other selected forest plots. Thirteen species revealed affinity to inversed (wet and cold) stands of beech (3) and maple– hornbeam wood (4), four of them represented montane species, whereas five species clearly preferred thermophilous sites (1, 2, 5). The presence of 11 montane species at the bottom of the gorge (4) documented the inverse character of the site: Ceratophysella sigillata, C. silvatica, Friesea albida, Deutonura albella, D. stachi, Superodontella lamellifera, Tetrodontophora bielanensis, Heteraphorura variotuberculata, Kalaphorura carpenteri, Orthonychiurus rectopapillatus and Plutomurus carpaticus. Abundance of Folsomia quadrioculata significantly correlated with the soil microclimate – moisture ( p < 0.01, r ¼ 0.92). Distribution data on Collembola were performed by cluster (PC-ORD) and CCA ordination techniques. Collembolan communities of two neighbouring forest stands with identical soil type (rendzina) – lime (2) and beech wood (3) – were the most similar in species composition. Meso-/microclimatic gradients within a karst landscape play an important role in determining diversity and community structure of the soil Collembola. ª 2008 Elsevier Masson SAS. All rights reserved.

1.

Introduction

The Za´diel Valley is situated in the eastern part of the Slovak Karst National Park – Biosphere Reserve (Western

Carpathians) which is among the most remarkable karst areas in Central Europe. The geomorphology of the diverse karst landscape creates strong meso- and microclimate gradients within relatively small areas serving as the basis for a broad

* Corresponding author. E-mail addresses: [email protected] (N. Raschmanova´), [email protected] (L’. Kova´cˇ), [email protected] (D. Miklisova´). 1164-5563/$ – see front matter ª 2008 Elsevier Masson SAS. All rights reserved. doi:10.1016/j.ejsobi.2008.07.005

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european journal of soil biology 44 (2008) 463–472

variety of habitats and microhabitats. The Za´diel Valley is a good example of a mesoclimate inversion, the local climate of the gorge valley bottom being strongly dissimilar to that of the karstic plateau situated above the valley. Studies on the effect of a meso-/microclimate gradient upon soil invertebrate diversity in natural conditions are rather rare (e.g. [18]). Several papers [27,36] deal with periglacial relict Arthropoda of cold highland screes in Central Europe. Investigation of the soil Acari and Collembola has been carried out at the entrance to the Silicka´ l’adnica Ice Cave (Slovak Karst) with a strong gradient of the inversed mesoclimate [7,10]. Several studies on soil Collembola diversity within the Za´diel Valley have been published during recent years [12–14,16]. The aims of this paper were: (1) to analyze the diversity of soil Collembola of the selected vegetation stands along the mesoclimatic inversion in the Za´diel Valley, and (2) to assess the effects of this phenomenon upon Collembola community structure.

2.

Materials and methods

The Slovak Karst is situated in southeast Slovakia and consists of plateaux whose maximum altitude ranges between 400 and 900 m. The basic structural unit of the region is the Silicka´ Nappe comprising Lower Triassic frustulent sediments, and Middle and Upper Triassic dolomite and limestone, including the coarse Wetterstein limestone. The originally compact

plateau surface has been eroded by streams into subunits. The outer slopes of the plateaux descend deeply down to gorges and adjacent basins over a height of 200–550 m. The region is located at the junction between oceanic and continental climatic zones. The warmest month is July (19–16  C), and the coldest is January (4 to 6  C). Mean annual temperature ranges from 5.7 to 8.5  C, the annual average precipitation ranges from 630 to 990 mm [26]. Five stands were selected for a detailed study of the soil Collembola communities in the Za´diel Valley, from the plateau down through the mouth of the valley. The five sites were: (1) pasture (vegetation association Glechomo–Festucetum) – subxerophilous herbaceous community located on the edge of the Za´dielska Plateau, 48 380 1700 N, 20 490 4300 E, very modest W exposition (1–2 ), 667 m a.s.l., luvisol, soil stony, about 20 cm deep, profile down to 10 cm depth: 2–3 mm layer of herb litter, 4 cm layer of dense rhizosphere, 6 cm layer of weak rhizosphere, mull humus; (2) lime wood (vegetation association Mercuriali–Tilietum) – 48 380 0900 N, 20 490 3400 E, steep, rocky W slope (34 ), 620 m a.s.l., rendzina, soil profile very stony, 6–8 cm thick: 0–4 cm litter layer, 4–8 cm organo-mineral horizon, mull humus; (3) beech wood (vegetation association Dentario bulbiferae–Fagetum) – 48 380 1400 N, 20 490 2700 E, moderate W slope (18 ), 573 m a.s.l., rendzina, soil profile stony, 6–7 cm thick: 1–1.5 cm litter layer, followed by organomineral layer, moder humus; (4) maple–hornbeam wood (vegetation association Aceri–Carpinetum) – fragment of the wood at the bottom of the gorge near the bank of the Blatnicky´ Creek, 48 370 5300 N, 20 490 5000 E, S exposition (5 ), 340 m a.s.l.,

Table 1 – Microclimatic factors, soil-chemical characteristics and ecological parameters of Collembola at sites in the Za´diel Valley Sites

Site characteristics Temperature ( C) Soil moisture content (% initial weight) pHH2O pHKCl Soil Corg (% of initial weight) Soil Nt (% of initial weight) C/N ratio Soil Pt content (mg P kg1 soil) Soil Ca content (g Ca kg1 soil) Community characteristics Abundance (individuals m2) Species richness (no.) Diversity (H0 ) Evenness (J )

1

2

3

4

5

8.88 30  5.81

8.27 51  8.52

7.28 31  4.75

5.16 35  10.16

7.69 27  9.52

6.4 5.63 9.04

7.4 6.8 33.29

6.9 6.4 9.83

7.7 7.2 5.96

7.6 7.2 10.7

0.73

2.37

0.60

0.42

0.88

12.4 1271

14.1 1674

16.3 726

14.1 806

12.2 1961

3.2

4.2

3.0

2.6

3.0

13.981  6150 70 2.80 0.66

16.181  6196 86 2.57 0.58

11.652  5020 108 3.42 0.73

12.522  7825 83 2.78 0.63

20.252  9786 79 2.60 0.59

Soil temperature measured between August 2004 and August 2005; gravimetric soil moisture content with standard deviation (measured between September 2002 and November 2004. Corg, organic carbon content; Nt, total nitrogen content; C/N ratio of organic matter; Pt, total phosphorus content; Ca, calcium content (May 2004). H0 , Shannon diversity index; J, Pielou index of evenness;. Collembola abundance is given with standard deviation. See Section 2 for site names.

X

*

X 0.00 X 0.19 0.87

*

X 0.24 0.04 0.40 X 0.34 0.17 0.89 0.42

**

*

*

**

X 0.09 0.19 0.23 0.83 0.05 0.57 0.38 0.25 0.54 0.94 0.01 0.32 0.28

X 0.58 0.21 0.51 0.60 0.44 0.11 0.34 0.59

X

*

*

**

X 0.38 0.51 0.29 0.50 0.03

*

X 0.97 0.96 0.66 0.79 0.32 0.27 0.06 0.84 0.57 0.02 0.20 0.91 0.24 0.60

** X 0.99 0.47 0.86 0.37 0.46 0.14 0.75 0.71 0.19 0.15 0.80 0.39 0.41

** ** X 0.43 0.89 0.29 0.42 0.11 0.71 0.73 0.24 0.20 0.81 0.47 0.45

X 0.10 0.36 0.20 0.11 0.90 0.21 0.56 0.08 0.79 0.37 0.74

* *

X 0.06 0.31 0.24 0.35 0.92 0.27 0.54 0.63 0.53 0.34

X 0.75 0.76 0.61 0.02 0.15 0.74 0.09 0.11 0.30

* **

X 0.55 0.57 0.49 0.54 0.13 0.96 0.68 0.62 0.77 0.11 0.01 0.55 0.33 0.14 0.08 X 0.22 0.12 0.13 0.12 0.67 0.19 0.37 0.85 0.45 0.28 0.47 0.83 0.34 0.45 0.55 0.78 pHH2O Soil Ptot content Soil Ca content Soil N content Soil C content Temperature Soil moisture content Total abundance FOMA ILMI ISNO FOQU MPAF CELU MGMI CESI HPVA

Pasture on the plateau (1) had higher average soil temperature (microclimatically extreme habitat, with obvious temperature peaks in summer) compared to all other forest sites. Stand at the bottom of the gorge maple – hornbeam wood (4) had the lowest average soil temperature (presence of Blatnicky´ Creek, low light intensity, Table 1). Temperature data document clearly mesoclimatic gradient within valley. The highest soil moisture was found in lime wood (2) and the lowest in cornel oak wood (5). Abundance means of collembolan assemblages during the study period at the individual sites ranged between 11,652 and 20,252 individuals m2 (Table 1). The highest mean was observed in the secondary cornel-oak wood (5) at the mouth of the valley. Relationships between abiotic factors measured and Collembola abundance

Ca N C Temperature Soil moisture Total FOMA ILMI ISNO FOQU MPAF CELU MGMI CESI HPVA Ptot content content content content content abundance

Results

pHH2O

3.

Table 2 – Correlation coefficients and significance levels for the relationship between edaphic parameters and Collembola abundance

fluvisol, soil profile very stony, 6–8 cm thick: 0.5–1 cm litter layer, 1–2 cm organo-mineral layer with dense herbal rhizosphere, followed by mineral layer with high proportion of silt or sand, mull humus; (5) forest stand resembling cornel-oak wood, young secondary wood (former pasture) near the mouth of the gorge, 48 370 1000 N, 20 490 5500 E, modest E slope (12 ), 286 m a.s.l., cambisol, soil profile stony, 5–6 cm thick: 1 cm litter layer, 0.5 cm humus layer, 3–4 cm organo-mineral horizon with dense herbal rhizosphere, followed by dark mineral horizon with a large proportion of sand, mull humus. Soil samples were taken monthly from September 2002 to November 2004. During each sampling 10 replicate soil samples were taken randomly from each plot (1350 samples altogether). The samples represented soil cores 3.6 cm in diameter (10 cm2 in area) to a maximum depth of 10 cm (depending on the soil thickness). The material was extracted in a modified high-gradient extraction apparatus [6] for 7 days. Collembola were identified using a phase-contrast microscope and identification keys (e.g. [3,23,25,31,37]). Soil moisture was calculated monthly using a gravimetric method. During August 2004–August 2005 the soil temperature was measured by data-loggers at a soil depth of 3 cm, every 4 h; the temperature ratio was counted for each site and used as its microclimatic characteristic (Table 1). Species abundance (A), species dominance (D), species frequency (F), Shannon diversity index (H0 ) and Pielou evenness (J) were calculated to be able to compare the collembolan communities between plots. Soil-chemical parameters of the sites are given in Table 1. Relationships between edaphic factors and community parameters were estimated using Pearson’s correlation coefficient, the statistical significance was tested by the t-test. Non-transformed quantitative data matrix was evaluated by CCA ordination analysis [30], where soil-chemical (pH, total phosphorus content) and soilmicroclimatic parameters (temperature, humidity) were used as environmental variables. The species present in less than 10 samples of the total number were excluded from the procedure (80 from total 152 species) because of their low explanatory value. For cluster analysis the PC-ORD system package [21] was used, using the group average method and the So¨rensen diversity index to test qualitative similarity between communities of particular sites.

*p < 0.05; **p < 0.01 (for dimensions see Table 1). Abbreviations of the species: FOMA, Folsomia manolachei; ILMI, Isotomiella minor; ISNO, Parisotoma notabilis; FOQU, Folsomia quadrioculata; MPAF, Metaphorura affinis; CELU, Ceratophysella luteospina; MGMI, Megalothorax minimus; CESI, Ceratophysella sigillata; HPVA, Heteraphorura variotuberculata.

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european journal of soil biology 44 (2008) 463–472

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european journal of soil biology 44 (2008) 463–472

means were tested and coefficients calculated. In this study soil Collembola abundance means were positively correlated with content of total phosphorus (p < 0.01, r ¼ 0.96; Table 2). Abundance of Folsomia quadrioculata was positively correlated with soil moisture (p < 0.01, r ¼ 0.92). Several species revealed significant relationships with soil-chemical parameters: Folsomia manolachei with pHH2O (p < 0.05, r ¼ 0.85), Parisotoma notabilis with average soil temperature (p < 0.05, r ¼ 0.90) and with Ca content (p < 0.05, r ¼ 0.84), Megalothorax minimus with Ca content (p < 0.01, r ¼  0.91). In total 20, 139 specimens belonging to 152 species of Collembola were detected at five study sites in the Za´diel Valley. Species numbers for particular sites ranged between 70 and 108 being higher in forest soils compared to the open habitat (subxerophilous pasture). Higher species richness and diversity indices were observed in the beech wood compared to other forest plots (Table 1). In contrast, thermophilous lime wood (2) hosted the community with the lowest diversity indices due to remarkably high dominance of Folsomia manolachei, Folsomia quadrioculata and Isotomiella minor. Low diversity (species richness, diversity indices) was observed also in the secondary cornel-oak wood (5) due to high dominance of two eurytopic species - F. manolachei and I. minor. The lowest species richness (70) was recorded in the pasture (site 1) situated on the karst plateau. The community of this stand with herbaceous cover was determined by strong fluctuations of soil temperature (Mock, unpublished data), lower soil moisture content and different chemical composition of the soil compared to forest stands (Table 1). For this site a considerable proportion of thermophilous (xerothermophilous) species in the community was characteristic. In the cluster analysis diagram of qualitative community data (Fig. 1) thermophilous stands – pasture and secondary cornel-oak wood (sites 1,5) – were allocated to the same branch in contrast to the natural forest stands (sites 2,3,4) that were grouped together. Soil Collembola communities in lime and beech wood stands (sites 2,3) were the most similar as a consequence of their close location and rendzina soil type. It is apparent from the Table 3 that thirteen species of Collembola preferred wet and cold forest stands (3,4), the most of them representing forest species. Xenylla brevisimilis, Pseudachorutella asigillata and Tomocerus minutus belong to corticophilous fauna [31,34], Friesea albida, Deutonura stachi, Orthonychiurus rectopapillatus and Plutomurus carpaticus often being classified as montane species. Micranurida pygmaea and Pseudachorutes dubius are species with plastic hygro-preferences [18]. Friesea truncata, Micranurida spirillifera, Superodontella lamellifera, Tetrodontophora bielanensis, Neonaphorura

Log distance -3.12

-2.73

-2.36

-1.98

-1.60

|-------+-------+-------+-------+-------+-------+-------+-------+

Site 1 Site 5 Site 2 Site 3 Site 4

Fig. 1 – Cluster analysis of species composition of Collembola at the five sites in the Za´diel Valley.

dungeri, Entomobrya corticalis, Pogonognathellus flavescens and Arrhopalites ulehlovae occurred exclusively at the humid site (4) and are known to prefer such conditions [3,4,8]. On the other hand, five species were associated with thermophilous stands (1,2,5): Mesaphorura cf. rudolphi, Doutnacia xerophila, Karlstejnia annae, Mesaphorura hylophila and Sphaeridia pumilis. The highest number (11) and dominance (D ¼ 18.05 %) of montane species were recorded in maple-hornbeam wood situated at the bottom of the gorge (4) with the lowest mean soil temperature (Table 1): Ceratophysella sigillata, C. silvatica, Friesea albida, Superodontella lamellifera, Deutonura albella, D. stachi, Tetrodontophora bielanensis, Kalaphorura carpenteri, Heteraphorura variotuberculata, Orthonychiurus rectopapillatus and Plutomurus carpaticus. Data set of species with frequency higher or equal to 0.8% and their related abundance were performed by CCA ordination technique. The combination of chemical (pH, Pt) and microclimatic factors (mean soil temperature and moisture) was used (Fig. 2). The ordination technique separated the 72 most frequent species into three distinct clusters. One of them refers to the plateau pasture (1) with thermophilous and open habitat species: Lepidocyrtus cyaneus, Pseudachorutes pratensis, Axenyllodes bayeri, Isotoma anglicana, Protaphorura serbica, Isotomodes productus, Metaphorura affinis and Desoria germanica, and eurytopic O. flavescens and S. pumilis. The second cluster involved species inhabiting forest plot of beech wood (3), comprising Entomobrya nivalis, Ceratophysella denticulata, Pseudanurophorus binoculatus, Ceratophysella engadinensis, Superodontella sp. 2, Oncopodura crassicornis, Folsomia penicula, Pseudosinella zygophora, P. horaki and Kalaphorura carpenteri as characteristic species. The third cluster consisted of species inhabiting other forest plots (2,4,5) with very similar community structure. Characteristic species such as F. manolachei, F. quadrioculata, Heteraphorura variotuberculata, Pseudachorutes parvulus, Ceratophysella silvatica, Karlstejnia annae, Deutonura conjucta, Deutonura albella and Neanura pseudoparva were associated with edaphic factors: higher pH level, higher content of total phosphorus, calcium and soil moisture.

4.

Discussion

The highest Collembola abundance mean (20,252 individuals m2) was observed in the secondary cornel-oak wood (5) at the mouth of the valley. Soil type as an important factor determining soil Collembola community abundance in the karst region has been documented [15,17]. Our results are not fully consistent with the literature, since thermophilous forest stands, i.e. lime (2) and cornel-oak wood (5), with rendzina and cambisol respectively, showed the highest mean community abundance. On the other hand, the lowest mean abundances were found in the rendzina of the beech wood (3) and the fluvisol plot (4). Site 4 had a shallow soil profile washed during periodic spring floods and thus characterised by the lowest content of the soil carbon (Table 1). Soil Collembola at stands with rendzina (2,3) showed rather different abundance means. At the lime wood stand (2) relatively high average monthly values of soil moisture were recorded compared to other forest stands due to a thicker humus/organo-mineral

Table 3 – Abundance (individuals mL2), dominance (%) and frequency (%) of Collembola species at five sites in the Za´diel Valley (see Section 2 for site names) Species code

Ceratophysella armata Ceratophysella denticulata Ceratophysella engadinensis Ceratophysella luteospina Ceratophysella sigillata Ceratophysella silvatica Hypogastrura socialis Microgastrura duodecimoculata Mesogastrura ojcoviensis Willemia anophthalma Willemia bedosae Willemia denisi Willemia intermedia Willemia scandinavica Xenylla brevicauda Xenylla brevisimilis Brachystomella parvula Friesea albida Friesea mirabilis Friesea truncata Anurida lvivska Anurida uniformis Micranurida bescidica Micranurida cf. balta Micranurida granulata Micranurida pygmaea Micranurida spirillifera Micranurida vontoernei Pseudachorutella asigillata Pseudachorutes corticicolus Pseudachorutes dubius Pseudachorutes palmiensis Pseudachorutes parvulus Pseudachorutes pratensis Pseudachorutes subcrassus Endonura sp. 1 Endonura sp. 2 Deutonura albella Deutonura conjuncta Deutonura phlegraea Deutonura stachi Neanura minuta Neanura pseudoparva

Author and date

(Nicolet, 1841) (Bagnall, 1941) (Gisin, 1949) (Stach, 1920) (Uzel, 1891) (Rusek, 1964) (Uzel, 1891) Stach, 1922 (Stach, 1919) Bo¨rner, 1901 ´ Haese, 1998 D Mills, 1932 Mills, 1934 Stach, 1949 Tullberg, 1869 Stach, 1949 (Scha¨ffer, 1896) Stach, 1949 (Tullberg, 1871) Cassagnau, 1958 Babenko, 1998 Gisin,1953 yn´ski, 2004 Smolis et Skarz Fjellberg, 1998 (Agrell, 1943) Bo¨rner, 1901 Hammer, 1953 Nosek, 1962 (Bo¨rner, 1901) (Scha¨ffer, 1896) Krausbauer, 1898 (Bo¨rner, 1903) Bo¨rner, 1901 Rusek, 1973 Tullberg, 1871

(Stach, 1920) (Stach, 1926) (Caroli, 1912) (Gisin, 1952) Gisin, 1963 Rusek, 1963

Site 1

2

3

4

5

15 – – 11 1241 4 – – – – – – – 22 – – – – – – – – – – – 11 – – – – 26 – 89 159 4 – – – 15 – – 7 –

11 – – 63 7 281 30

37 200 181 600 33 7 – 19 7 52 4 41 4 337 159 4 4 74 – – – – 7 – 11 63 – 15 11 4 52 4 30 4 4 11 4 – 7 – 11 22 19

37 – 7 19 370 56 – – – – – – 7 – 4 11 – 344 44 85 – – 11 – – 63 7 – 11 4 85 15 126 – 7 11 – 30 48 7 37 11 22

59 4 15 1922 541 33 – – – 4 4 – 7 470 4 – – – – – – – 11 – – 56 – – – – 37 4 326 15 – 4 – 19 15 – – 204 59

– 15 – – 4 152 – – – – 4 – 4 4 15 4 – 11 – – – 19 26 – 119 – 30 15 – 22 59 4 4 78 19

Abundance

Dominance

Frequency

32 41 41 523 439 76 6 4 1 14 1 8 4 196 33 3 1 84 10 17 1 1 9 1 2 41 1 3 4 5 45 4 138 36 9 8 1 14 29 2 10 64 24

0.21 0.27 0.27 3.51 2.94 0.51 0.04 0.02 0.01 0.09 0.01 0.05 0.03 1.32 0.22 0.02 0.00 0.56 0.06 0.11 0.00 0.00 0.06 0.00 0.01 0.27 0.01 0.02 0.03 0.03 0.30 0.03 0.92 0.24 0.06 0.05 0.00 0.09 0.19 0.01 0.07 0.43 0.16

2.00 2.59 1.70 16.52 5.41 4.52 0.30 0.37 0.07 1.04 0.15 0.52 0.44 9.70 0.59 0.30 0.07 3.48 0.81 1.26 0.07 0.07 0.81 0.07 0.07 3.48 0.15 0.22 0.30 0.44 2.96 0.44 9.26 1.78 0.81 0.67 0.07 1.33 2.37 0.22 0.89 4.59 2.30

467

(continued on next page)

european journal of soil biology 44 (2008) 463–472

CEA CED CEE CEU CES CEL HYS MID MEO WLA WIB WID WII WLS XBC XBS BRP FRA FRM FRT ANL ANU MIC MIB MIG MIP MIS MIV PCA PCC PCD PCP PCP PCR PCS EN1 EN2 DEA DEC DEP DES NEM NEP

Species

468

Table 3 (continued) Species code

Pumilinura dudichi Pumilinura loksai Axenyllodes bayeri Superodontella lamellifera Superodontella sp. 1 Superodontella sp. 2 Xenyllodes armatus Tetrodontophora bielanensis Hymenaphorura polonica Hymenaphorura pseudosibirica Heteraphorura variotuberculata Kalaphorura carpenteri Micraphorura absoloni ‘‘Onychiurus’’ sp. juv. Onychiuroides pseudogranulosus Orthonychiurus rectopapillatus Deuteraphorura silesiaca Deuteraphorura silvaria Protaphorura armata Protaphorura aurantiaca Protaphorura campata Protaphorura cancellata Protaphorura gisini Protaphorura pannonica Protaphorura serbica Protaphorura subarmata Protaphorura subuliginata Protaphorura tricampata Doutnacia xerophila Fissuraphorura sp. juv. Jevania weinerae Karlstejnia annae Metaphorura affinis Metaphorura orestia Mesaphorura cf. rudolfi Mesaphorura cf. simoni Mesaphorura critica Mesaphorura florae Mesaphorura hylophila Mesaphorura italica Mesaphorura macrochaeta Mesaphorura sylvatica Mesaphorura tenuisensillata Neonaphorura dungeri Stenaphorurella lubbocki

Author and date

(Loksa, 1967) (Dunger, 1973) (Kseneman, 1935) (Axelson, 1903)

Axelson, 1903 (Waga, 1842) Pomorski, 1990 (Stach, 1954) (Stach, 1934) (Stach, 1919) (Bo¨rner, 1901) (Gisin, 1951) (Stach, 1933) (Dunger, 1977) (Gisin, 1952) (Tullberg, 1869) (Ridley, 1880) (Gisin, 1952) (Gisin, 1956) (Haybach, 1960) (Haybach, 1960) (Loksa et Bogojevicˇ, 1967) (Gisin, 1957) (Gisin, 1956) (Gisin, 1956) Rusek, 1974 Rusek,1991 Rusek, 1978 Rusek, 1974 (Bo¨rner, 1902) Pomorski, Skarzyn´ski et Kaprus, 1998 Rusek, 1987 Jordana et Arbea, 1994 Ellis, 1976 Simo´n, Ruiz, Martin et Lucia´nˇez, 1994 Rusek, 1982 (Rusek, 1971) Rusek, 1976 (Rusek, 1971) Rusek, 1974 Schulz, 1994 (Bagnall, 1935)

Site 1

2

– – 193 – – – – – – – – – – – 15 4 – – 44 41 7 52 – – 1211 4 4 – 115 – – 19 3544 15 19 4 159 26 174 15 4 7 74 – –

–

3 7

– – – 11 – – 15 15 33 48 11 – 1000 4 – – 311 41 89 330 4 89 70 15 52 11 159 – – 263 11 – 4 – 70 7 148 115 – 15 – – 7

4

5

4

– –

4

7 144 – – – 119 – – 1074 70 – – 319 7 – – 244 15 19 48 15 – 37 48 – 7 4 4 11 19 – – – – 67 – 100 7 – 67 7 4 44

– – – – – 30 – – – – 896 44 – – 19 – 96 22 367 11 59 107 – 204 15 7 81 – 330 – 15 22 30 – 4 – 52 148 159 15 – 78 – – –

– – 4 226 11 – 7 15 15 356 7 7 607 19 – – 385 81 200 163 7 41 26 26 19 11 4 7 15 7 19 – – – 44 85 70 85 11 41 37 – –

Abundance

Dominance

Frequency

1 1 41 29 1 53 2 24 4 6 404 104 4 1 392 7 19 4 270 38 75 140 5 67 272 20 31 6 122 2 8 66 721 3 5 1 79 53 130 47 3 41 24 1 10

0.00 0.01 0.27 0.19 0.00 0.36 0.01 0.16 0.03 0.04 2.71 0.70 0.02 0.01 2.63 0.04 0.13 0.03 1.81 0.25 0.50 0.94 0.03 0.45 1.82 0.13 0.21 0.04 0.82 0.01 0.05 0.44 4.83 0.02 0.03 0.00 0.53 0.36 0.87 0.32 0.02 0.28 0.16 0.00 0.07

0.07 0.15 2.59 1.04 0.07 1.26 0.15 0.44 0.30 0.44 15.33 6.15 0.30 0.15 16.37 0.30 0.15 0.37 17.41 2.89 5.04 9.11 0.44 4.81 10.59 1.70 2.07 0.52 7.48 0.22 0.52 3.70 13.04 0.22 0.37 0.07 5.70 3.33 7.85 3.04 0.22 2.59 1.26 0.07 0.96

european journal of soil biology 44 (2008) 463–472

PUD PUL AXB ODL OD1 OD0 XEA TEB HPP HPS HPV KAC MIA ONS ONP ORR DES DEV PRA PRU PRM PRC PRG PRP PRR PRS PRG PRT DOX FIJ JEW KSA MPA MPO MPR MPS MSC MSF MSH MSI MSM MSS MST NED SFL

Species

Appendisotoma abiskoensis Desoria divergens Desoria germanica Folsomides parvulus Folsomia manolachei Folsomia penicula Folsomia quadrioculata Isotomodes productus Isotomodes sexsetosus Isotomiella minor Isotoma anglicana Parisotoma notabilis Isotoma viridis Jesenikia filiformis Pseudanurophorus binoculatus Proisotoma minima Subisotoma pusilla Tetracanthella montana Entomobryidae juv. Entomobrya corticalis Entomobrya nivalis Heteromurus nitidus Lepidocyrtus sp. Lepidocyrtus cyaneus Lepidocyrtus lignorum Lepidocyrtus violaceus Orchesella bifasciata Orchesella flavescens Orchesella multifasciata Pseudosinella sp. 1 Pseudosinella sp. 2 Pseudosinella sp. 3 Pseudosinella horaki Pseudosinella huetheri Pseudosinella thibaudi Pseudosinella zygophora Willowsia buski Willowsia nigromaculata Pogonognathelus sp. juv. Pogonognathellus flavescens Plutomurus carpaticus Tomocerus sp. juv. Tomocerus minutus Cyphoderus sp. juv. Oncopodura crassicornis Megalothorax incertus Megalothorax minimus

(Agrell, 1939) (Axelson, 1900) (Hu¨ther et Winter, 1961) Stach, 1922 Bagnall, 1939 Bagnall, 1939 (Tullberg, 1871) (Axelson, 1906) Da Gama, 1963 (Scha¨ffer, 1896) Lubbock, 1862 (Scha¨ffer, 1896) Bourlet, 1839 Rusek, 1997 Kseneman, 1934 (Absolon, 1901) (Scha¨ffer, 1900) Stach, 1947 (Nicolet, 1842) (Linne´, 1758) (Templeton, 1835) Tullberg, 1871 (Fabricius, 1775) (Fourcroy, 1785) Nicolet, 1842 (Bourlet, 1839) Stscherbakow, 1898

Rusek, 1985 Stamp, 1971 Stomp, 1977 (Schille, 1908) (Lubbock, 1869) (Lubbock, 1873) (Tullberg, 1871) Rusek et Weiner, 1978 Tullberg, 1876 Shoebotham, 1911 Bo¨rner, 1903 Willem, 1900

– 141 1126 – 74 22 107 189 – 430 304 1226 19 – 4 – – – 326 – – – 4 1285 41 – – 41 – 19 – 4 44 – – 7 – 26 4 – – 7 – 4 7 4 344

– 44 – – 5270 78 2478 4 – 1833 – 1474 – – 4 4 67 – 133 – – – – 37 85 – 22 – 11 19 11 – 281 – – 33 – 4 – – – 4 – – 22 4 22

– 4 – 7 215 533 56 – – 2067 7 1000 – 7 122 – – 4 22 – 89 4 – 111 259 – – – 7 93 11 – 841 44 63 163 – 11 – – 4 52 – 548 4 374

– 70 – – 3941 19 1507 4 – 770 – 593 – – – – – – 130 100 – – – 30 104 – 15 – – – – 56 – – 4 – 15 – 4 7 – 48 4 44 4 859

4 259 – – 6111 26 81 11 7 4059 4 1270 11 – – – – – 181 – – – – 93 222 11 – 15 30 11 – 7 270 – 4 – 15 – – – – – – – 19 11 596

1 104 225 1 3122 136 846 41 1 1832 63 1113 6 1 26 1 13 1 159 20 18 1 1 311 142 2 7 11 10 28 4 2 299 9 13 41 3 11 1 1 2 2 20 1 128 5 439

0.00 0.70 1.51 0.01 20.93 0.91 5.67 0.28 0.01 12.28 0.42 7.46 0.04 0.01 0.17 0.00 0.09 0.00 1.06 0.13 0.12 0.00 0.00 2.09 0.95 0.01 0.05 0.07 0.06 0.19 0.03 0.01 2.00 0.06 0.09 0.28 0.02 0.07 0.00 0.00 0.01 0.01 0.13 0.01 0.86 0.03 2.94

0.07 6.22 7.70 0.07 48.44 6.00 21.11 2.74 0.07 43.56 2.81 37.04 0.52 0.15 1.41 0.07 0.22 0.07 9.48 0.52 1.41 0.07 0.07 13.48 10.07 0.22 0.67 0.89 0.81 1.70 0.37 0.22 16.96 0.44 0.67 2.67 0.30 1.11 0.07 0.07 0.22 0.22 1.56 0.15 8.00 0.52 12.15

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european journal of soil biology 44 (2008) 463–472

APA DRD DRG FOP FOM FOP FOQ IDP ISS ILM ISA ISN ISV JEF PAB PRM SUP TEM EN ENC ENN HEN LES LEC LEL LEV ORB ORF ORM PS1 PS2 PS3 PSH PSU PST PSZ WIB WIN POJ POF PLC TOJ TOM CYJ OPC MGI MGM

470

– 41 4 – – – – 181 52 4 7 7 – – – 4 – – 11 7 4 – – 19 33 115 11 – 7 – – – – – (Stach,1920) (Linne´, 1758) Stebaeva, 1966 (Tullberg, 1872)

(Tullberg, 1871) (Wankel, 1860) Rusek, 1967 Rusek,1970 (Lubbock, 1862) (Fitch, 1863) Gisin, 1957 Gama, 1965

3

7 4 19 7 – 4 – 126 15 – – – 4 30 – 7 – – 19 – – 26 – – 67 11 – – – – 7 15 126 15 63 544 – 15 – – – 81 30 – – 52 11 – – – 26 Dunger et Bretfeld, 1989 (Krausbauer, 1898)

Sphaeridia furcata Sphaeridia pumilis Arrhopalites sp. juv. Arrhopalites caecus Arrhopalites pygmaeus Arrhopalites spinosus Arhopalites ulehlovae Sminthurinus aureus Sminthurinus elegans Gisinianus flammeolus Sminthurinus gisini Sminthurus sp. juv. Spathulosminthurus guthriei Allacma fusca Sminthurus cf. ghilarovi Lipothrix lubbocki Deuterosminthurus sp. juv. SPF SPP ARJ ARC ARP ARS ARU SNA SNE GIF SMG SMJ SPG ALF SMR LIL DEJ

Species code

Table 3 (continued)

Species

Author and date

1

2

Site

4

5

14 124 6 5 5 1 4 98 44 3 1 13 3 7 3 27 8

Abundance

0.09 0.83 0.04 0.03 0.03 0.00 0.02 0.66 0.30 0.02 0.01 0.09 0.02 0.05 0.02 0.18 0.05

Dominance

0.74 4.30 0.59 0.44 0.37 0.07 0.15 2.89 1.93 0.22 0.07 0.44 0.22 0.52 0.15 0.52 0.67

Frequency

european journal of soil biology 44 (2008) 463–472

layer in the soil profile. Structure and abundance of collembolan communities are positively correlated with better developed organic profiles of soils and soil moisture content [1,9]. In this study several species revealed significant relationships to soil-chemical parameters of the soil (pH, Ca) and soil Collembola abundance means were positively correlated with content of total phosphorus (Pt). Soil moisture is often reported as the most important environmental factor acting upon soil Collembola [32]. F. quadrioculata is known to prefer soils that tend to be moist [16,25]. It seems that meso-/microclimatic gradient plays a key role in the soil collembolan diversity. Five xeroresistant and xerothermophilous species were found in the pasture located on the plateau (1), in lime wood at the edge of the plain (2) and in xerothermophilous cornel-oak wood near entrance of the valley (5). From the CCA analysis it is evident that D. germanica was characteristic for pasture community, its abundance negatively correlating with pHH2O. Desoria divergens, which occurred at all studied sites (Table 3), is more ecologically plastic compared to D. germanica. Autecology of both species has been poorly documented [25]. The inverse character of the Za´diel Valley was documented by preference of thirteen forest species to the cold and wet beech and maple-hornbeam stands (3,4). Moreover, the highest number of montane species was recorded in maple-hornbeam wood at the bottom of the gorge (4) characterised by the lowest mean soil temperature. We suspect that meso-/microclimatic gradient is the driving factor in distribution of collembolan communities within a karst landscape, though also other parameters related to soil microclimate may play a role such as a precipitation interception, humus form, rootlet density, etc. [24,33]. From the qualitative cluster analysis the species composition of collembolan communities between lime and beech wood stands (2,3) was very similar (adjacent locations with rendzina soil type), although they differ in humus form, soil chemical parameters, soil temperature, all known as factors which may considerably affect the structure of soil collembolan communities. Differences in abundance and diversity indices of Collembola at both studied sites are probably related to the humus composition. The humus form is considered a decisive factor in the establishment of soil Collembola communities and the way in which the litter is decomposed is more important than the nature of the litter [5,24]. ˇ arnogursky´ [7] identified 53 and Kova´cˇ In the Slovak Karst, C et al. [14] identified 71 collembolan species based on a single sampling and a similar number of sites (five). Thus in the present study the overall species number clearly reflected the greater number of samples collected. Apparent difference was seen in species richness and in diversity indices between beech wood and other forest stands. Similarly Weiner [34] noticed the highest soil Collembola species richness in the beech stands compared to other forest or open vegetation associations in the Pieniny Mts. karst region (Western Carpathians). In the present study rather high species number was recorded in beech wood, i. e. 108 species in total, compared with literature data concerning European beech forests [11,20,22,34,35] where this parameter varied between 38–64 species. The quality of plant litter may explain high collembolan diversity in beech stand, the parameter with

european journal of soil biology 44 (2008) 463–472

471

Fig. 2 – CCA ordination analysis of the community data matrix from sites in the Za´diel Valley (eigenvalue of axis 1, 0.62; 2, 0.29. For site numbers see Section 2; for environmental variables abbreviations see Table 1; for species abbreviations see Table 3).

a critical role in ecosystem properties and function [2]. Beech litter in this study had obviously higher C/N ratio compared to litter of other study sites (Table 1). Leaf litter of the European beech (Fagus sylvatica) contains higher amounts of lignin and decomposes the most slowly because of high concentration of polyphenol-protein complexes compared to other deciduous leaves [19,29]. Such conditions favour higher densities and diversity of fungal communities, the predominant microorganisms in such soils [19]. Thus, the high collembolan species richness in the beech wood may be associated with the richness of the decomposer fungal communities. Comparisons have been made between the soil fauna of beech forest on a mull on limestone and moder on acid soil in the same geographic and climatic region (Germany) [28]. In comparison to mull conditions the moder forest was characterised by higher numbers of mesofaunal, microphytophagous animals. Characteristics of the beech wood stand in the present study seem to be similar, the C/N ratio is slightly higher to values for mull that are usually less than 15 [29]. The specificity of Collembola community of the beech stand was clearly documented by ordination CCA analysis. On the other hand, the analysis did not show the principal differences in the community structure of the inversed sites. Five of totally eight Carpathian/Western Carpathian endemics recorded prevailed in the inversed (cold and wet) stands of beech and maple-hornbeam wood (3,4), Micranurida vontoernei, Deutonura stachi, Orthonychiurus rectopapillatus, Tetracanthella montana and Plutomurus carpaticus. Jevania weinerae represents an endemic species of the Western Carpathians,

formerly considered to be distributed in a micro-range limited to the Pieniny Mountains [15, 37].

Acknowledgements The study was funded by grants from the Slovak Scientific Grant Agency VEGA nos. 1/0441/03 and 1/3267/06. We thank the Administration Office of the Slovak Karst National Park (Brzotı´n) for kind assistance during this study. We are very grateful to botanist P. Mra´z (P.J. Sˇafa´rik University, Kosˇice, Slovakia) for his thorough help in vegetation analysis of the research plots. J. Kalcˇı´k and T. Pı´cek (Institute of Soil biology ˇ eske´ Budeˇjovice, Czech Republic) performed soilCAS, C chemical analyses.

references

[1] J.M. Blair, R.W. Parmelee, R.L. Wyman, A comparison of the forest floor invertebrate communities of four forest type in the northeastern US, Pedobiologia 38 (1994) 146–160. [2] T. Bolger, The functional value of species biodiversity – a review, Proc. R. Ir. Acad. B 101 (2001) 199–204. [3] G. Bretfeld, in: W. Dunger (Ed.), Synopses on Palaearctic Collembola. Vol. 2, Symphypleona, 71, Abh. Ber. Naturkundemus Go¨rlitz, 1999, pp. 1–318. [4] P. Cassagnau, F. Lauga- Reyrel, Sur le polymorphisme et le cycle sexuel du Collembole Superodontella lamellifera

472

[5]

[6]

[7]

[8] [9]

[10]

[11]

[12]

[13] [14]

[15]

[16]

[17]

[18]

[19] [20]

european journal of soil biology 44 (2008) 463–472

(Axelson) dans les Pyre´ne´es, Ann. Soc. Entomol. France NS 28 (1992) 371–384. M. Chagnon, C. He´bert, D. Pare´, Community structures of Collembola in sugar maple forests: relation to humus type and seasonal trends, Pedobiologia 44 (2000) 148–174. D.A. Crossley, J.M. Blair, A high efficiency, ‘‘low-technology’’ Tullgren-type extractor for soil microarthropods, Agric. Ecosyst. Environ. 34 (1991) 187–192. J. Cˇarnogursky´, Chvostoskoky (Collembola), in: nı´k, E. Karasova´ (Eds.), Slovensky´ kras, chra´nena´ M. Rozloz krajinna´ oblastˇ – biosfe´ricka´ rezerva´cia, Osveta, Martin (1994), pp. 154–157. H. Gisin, Collembolenfauna Europas, Museum de Gene´ve, 1960. M. Hasegawa, The response of collembolan community to the amount and composition of organic matter of a forest floor, Pedobiologia 46 (2002) 353–364. S. Kalu´z, Poˆdne roztocˇe (Acarina) v podmienkach teplotnej inverzie chra´nene´ho prı´rodne´ho vy´tvoru Silicka´ l’adnica. Ochrana prı´rody, Nat. Tutela 2 (1993) 65–80. H. Kopeszki, Collembolan fauna in Vienna beech wood in relation to litter accumulation and depletion, Pol. Pismo Entomol. 64 (1995) 357–362. N. Kostu´rova´, L. Kova´cˇ, D. Miklisova´, Abundance and diversity of soil Collembola (Hexapoda) assemblages in the Za´diel Valley, Slovak Karst (Slovakia), Proc. 7th Central European Workshop on Soil Zoology, 14–16 April 2003, Cˇeske´ Budeˇjovice, Czech Republic, 2005, pp. 53–59. L. Kova´cˇ, Stachorutes ruseki sp. n. (Collembola, Neanuridae) from Slovakia, Biologia (Bratisl.) 54 (1999) 135–138. nı´k, Soil arthropod L. Kova´cˇ, M. Taka´cˇova´, M. Rozloz communities of the Slovak Karst-Biosphere Reserve with special reference to Collembola (Hexapoda), in: E. To´th, R. Horva´th (Eds.), Proceedings of the Research Conservation Management Conference, 1–5 May 1996, Aggtelek National Park Directorate, Aggtelek, Hungary, 1997, pp. 427–436. L. Kova´cˇ, J. Magdova´, D. Miklisova´, Introductory monitoring of Collembola (Hexapoda) in the Pieniny Mts. (Western l (Eds.), Studies Carpathians), in: K. Tajovsky´, V. Balı´k, V. Piz on Soil Fauna in Central Europe., Proc. 6th Central European Workshop on Soil zoology, 23–25 April 2001, Cˇeske´ Budeˇjovice, Czech Republic, Institute of Soil Biology AS CR, Cˇeske´ Budeˇjovice, 2002, pp. 83–92. L. Kova´cˇ, N. Kostu´rova´, D. Miklisova´, Comparison of collembolan assemblages (Hexapoda, Collembola) of thermophilous oak woods and Pinus nigra plantations in the Slovak Karst (Slovakia), Pedobiologia 49 (2005) 29–40. J. Kubı´kova´, J. Rusek, Development of xerothermic rendzinas – a study in ecology and soil microstructure. Rozpravy CˇSAV, Rˇada Mat. Prˇ´ır. Veˇd, Academia, Praha 86 (1976) 1–80. N.A. Kuznetsova, A.I. Krest’yaninova, Dynamics of springtail communities (Collembola) in hydrological series of pine forests in southern taiga, Entomol. Rev. 78 (1998) 969–981. P. Lavelle, A.V. Spain, Soil Ecology, Kluwer Academic Publishers, 2001, pp. 1–654. J. Materna, Horizontal distribution and species diversity of Collembola in mountain beech and spruce forests. Ph.D.

[21]

[22]

[23]

[24]

[25]

[26]

[27]

[28]

[29]

[30]

[31]

[32]

[33] [34] [35] [36]

[37]

thesis, Univ. South Bohemia, Cˇeske´ Budeˇjovice, Czech Republic, 2004, pp. 1–84. B. McCune, Multivariate Analysis on the PC-ORD System. A Software Documentation Report. HR1 Report No. 75, Indianapolis, Indiana, 1987. H. Petersen, Population dynamics and metabolic characterization of Collembola species in a beech forest ecosystem, in: D. L. Dindall (Ed.) Soil Biology as Related to Land Use Practices, Environmental Protection Agency, Washington, D. C., 1980, pp. 806–833. R.J. Pomorski, Onychiurinae of Poland (Collembola: Onychiuridae), Polish Taxonomical Society, Wroclaw (1998) 1–201. J.F. Ponge, Biocenoses of Collembola in Atlantic temperate grass–woodland ecosystems, Pedobiologia 37 (1993) 223–244. M.B. Potapov, Isotomidae, in: W. Dunger (Ed.), Synopses on Palaearctic Collembola. Vol. 3, Abh. Ber. Naturkundemus Go¨rlitz 73, 2001, pp. 1–603. } llo } s, M. Uhrin, E. Karasova´, Slovensky´ nı´k, F. Szo M. Rozloz kras – Slovak Karst Biosphere Reserve, in: J. Jenı´k, F. Price (Eds.), Biosphere Reserves on the Crossroads of Central Europe, Czech Republic – Slovak Republic, Czech National Committee for UNESCO MAB programme, Empora, Prague, 1994, pp. 113–128. icˇka, M. Zacharda, Arthropods of stony debris in the V. Ru˚z Krkonosˇe Mountains, Czech Republic, Arc. Alp. Res. 26 (1994) 332–338. M. Schaefer, J. Schauermann, The soil fauna of beech forests: comparison between a mull and a moder soil, Pedobiologia 34 (1990) 299–314. J.M. Swift, O.W. Heal, J.M. Anderson, Decomposition in Terrestrial Ecosystems. Studies in Ecology, Vol. 5, Blackwell, Oxford, 1979. C.J.F. Ter Braak, CANOCO – a Fortran Program for Canonical Community Ordination by (Partial), (Detrended), (Canonical) Correspondence Analysis and Redundancy Analysis, Groep landbouw Wiskunde, Wageningen, 1988. J.-M. Thibaud, H.-J. Schulz, M.M da Gama, Hypogastruridae, in: W. Dunger (Ed.), Synopses on Palaearctic Collembola, Vol. 4. Abh. Ber. Naturkundemus Go¨rlitz 75 (2004) 1–287. H.A. Verhoef, A.J. van Selm, Distribution and population dynamics of Collembola in relation to soil moisture, Hol. Ecol. (1983) 387–394. J.A. Wallwork, Ecology of Soil Animals, McGraw-Hill, London, 1970. W.M. Weiner, Collembola of the Pieniny National Park in Poland, Acta Zool. Cracov. 25 (1981) 417–500. W. Wolters, Long-term dynamics of collembolan community, Appl. Soil Ecol. 9 (1998) 221–227. M. Zacharda, Glacial relict Rhagidiidae (Acari: Prostigmata) from superficial underground enclosures in the Krkonosˇe Mountains, Czechoslovakia, J. Nat. Hist. 27 (1993) 47–61. B. Zimdars, W. Dunger, Tullbergiinae Bagnall, 1935, in: W. Dunger (Ed.), Synopses on Palaearctic Collembola, Vol. 1, Abh. Ber. Naturkundemus Go¨rlitz 68 (1994) 1–71.