Research Article |
Corresponding author: Ján Rudy ( jan.rudy@student.upjs.sk ) Academic editor: Stefano Taiti
© 2018 Ján Rudy, Michal Rendoš, Peter Ľuptáčik, Andrej Mock.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Rudy J, Rendoš M, Ľuptáčik P, Mock A (2018) Terrestrial isopods associated with shallow underground of forested scree slopes in the Western Carpathians (Slovakia). In: Hornung E, Taiti S, Szlavecz K (Eds) Isopods in a Changing World. Title. ZooKeys 801: 323-335. https://doi.org/10.3897/zookeys.801.24113
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The shallow underground of forested scree slopes represents a little-studied subterranean biotope. In this paper, species diversity and depth distribution of terrestrial isopod communities studied in the depth profile (5–95 cm from the surface) of eight forested scree slopes in the Western Carpathians (Slovakia) is discussed. The southern edge of the Western Carpathians where the study sites are located represents the northernmost limit of distribution of obligate subterranean fauna in Europe. The sites differ from each other in type of bedrock, forest composition, slope aspect, and altitude. To sample isopods, a set of three subterranean pitfall traps consisting of a plastic cylinder (Ø 110 mm) and ten plastic cups was buried in each studied scree slope. In total, 252 isopods belonging to eleven species were sampled (1–5 species per site). Of the species found, the blind and depigmented Mesoniscus graniger was the sole species closely associated with deeper parts of the depth profile and was present in most of the sites studied. Another ten species were represented by a small number of individuals and their occurrence deeper in the scree slope profile was rather accidental. A comparison between winter and summer periods indicates apparent differences in seasonal activities of isopods. Ethylene glycol seems to be more appropriate fixative solution for trapping isopods than formaldehyde.
depth distribution, MSS, Oniscidea , shallow subterranean habitat, species diversity, subterranean traps
An extensive labyrinth of air-filled dark voids among the rocky fragments found inside the forested scree slopes represents a peculiar type of shallow subterranean habitat (
Communities of terrestrial isopods dwelling shallowly underground in forested scree slopes have been explored minutely so far only in the Czech Republic (
Previous research in subterranean biology in the Western Carpathians has favored caves (
Our study was carried out successively from November 2008 to January 2016 on 8 forested scree slopes situated in 5 geomorphological units of the Western Carpathians (Slovakia). The studied scree slopes were predominately formed during the Pleistocene to Holocene by frost weathering and they differ in the type of bedrock (Figure
Location of the study sites. 1/ Borinka (Malé Karpaty Mts.), 2/ Belinské skaly (Cerová vrchovina Highlands), 3/ Drienok Valley, 4/ Slope next to the Malá drienčanská Cave, 5/ Collapse above the Veľká drienčanská Cave (three sites are in the Revúcka vrchovina Highlands), 6/ Vysoký vrch Hill, 7/ Doline next to Silická ľadnica Ice Cave (both sites in Slovak Karst), 8/ Malý Ružinok Valley (Čierna hora Mts.).
Characteristics of scree slope sites studied. pH(H20) and C(ox) values, both after
Locality | Bedrock | GPS coordinates | Altitude (m) | Exposition | Sampling period | Sampling days | pH(H2O) | C(ox) |
(5–95 cm) | (5–95 cm) | |||||||
1 | Granitoid | 49°77'N, 17°66'E | 410 | southwest | 15 Jan 2015-16 Jan 2016 | 365 | 4.1-4.7 | 10.8-1.1 |
2 | Basalt | 48°13'N, 19°52'E | 460 | southwest | 15 May 2012–17 Oct 2013 | 520 | 5-6.4 | 3.2-0.5 |
3 | Limestone | 48°32'N, 20°07'E | 315 | north | 15 May 2012–17 Oct 2013 | 520 | 6.6-8.3 | 7.3-1.7 |
4 | Limestone | 48°29'N, 20°04'E | 248 | southwest | 18 Oct 2013–4 Jun 2014 | 229 | – | – |
5 | Limestone | 48°29'N, 20°03'E | 246 | southwest | 18 Oct 2013–4 Jun 2014 | 251 | – | – |
6 | Limestone | 48°31'N, 20°25'E | 328 | southwest | 11 Jun 2014–29 Apr 2015 | 322 | 7.3-8.3 | 12.5-2.3 |
7 | Limestone | 48°33'N, 20°30'E | 489 | west | 11 Jun 2014–29 Apr 2015 | 322 | 6.8-7.9 | 10-3.7 |
8 | Limestone | 48°50'N, 21°06'E | 530 | northeast | 15 Nov 2008–15 Jul 2010 | 607 | 7.7-8.3 | 15.5-8.8 |
1 Scree slope in the Strmina Natural Reserve (Malé Karpaty Mountains) overgrown with beech forest (Fagus). This study site lies on acidic granitoid bedrock but in its immediate vicinity, there is a karst area (Borinka Karst) characterized by several karst formations such as caves and sinkholes. The scree slope profile has four distinct layers: litter and humus (0–5 cm), organo-mineral layer (5–20 cm), a layer consisting of mixture of mineralized soil and rocks (20–75 cm) and scree partially clogged with soil (75–110 cm).
2 Scree slope on basalt bedrock in the Belinské skaly National Nature Monument belonging to the Cerová vrchovina Highlands, an area known for the presence of a number of shallow pseudokarst caves. The scree slope profile is covered with a xerophilous oak-hornbeam forest (Querco-Carpinetum) and its profile consists of three different layers: litter and humus (0–5cm), organo-mineral layer (5–30 cm) and scree with spaces filled substantially with mineralized soils (30–110).
3 Limestone scree slope in the Drienok Valley (Revúcka vrchovina Highlands) situated a few meters below the entrance to the Špaňopoľská Cave. The site is surrounded by beech-hornbeam forest (Fago-Carpinetum) and in the scree slope profile, there are four distinct layers: leaf litter and humus (0–5 cm), organo-mineral layer (5–25 cm), mixture of rocks and soil (25–70 cm) and scree partly filled with soil (70–110 cm).
4 Limestone scree directly at the entrance to the Malá drienčanská Cave without apparent stratification of the profile. The interior of the scree includes a mixture of humus, soil and rocky fragments up to a depth of 30 cm. Below this, large compact boulders predominate.
5 Scree slope within the collapse above the Veľká drienčanská Cave. The slope profile without evident stratification consists predominately of rocky fragments originating from the previously collapsed cave ceiling. The spaces among the large limestone boulders are slightly filled with the mixture of soil and humus. Both sites (4 and 5) are located approximately 10 km west of the Drienok Valley (site 3) and are overgrown with beech hornbeam forest (Fago-Carpinetum).
6 Limestone scree slope in the Slovak Karst National Park situated about 30 m west of the entrance to the Ardovská Cave. The slope is overgrown with dogwood-maple forest (Corno-Carpinetum). On the scree slope surface, there are several large boulders, most of them covered by bryophytes. Three clearly separated layers are recognizable inside the scree slope: a layer consisting of litter and humus (0–15 cm) is followed by organo-mineral layer with admixtures of tiny rocks (15–75 cm) and scree formed by large rock fragments (75–110 cm).
7 Limestone scree slope along the doline near the entrance to the ice cave Silická ľadnica situated in the Slovak Karst National Park. The site is forested by linden-hornbeam, and maple (Tilio-Aceretum with Carpinus betulus) trees and the scree slope profile is divided into three layers: leaf litter and humus (0–5 cm), thick organo-mineral layer (5–30 cm) and scree (30–110 cm).
8 Limestone scree slope in the Sivec National Reserve (Čierna Hora Mountains) including a massive limestone cliff with several shallow caves. The vertical profile of the scree slope covered with linden-maple forest (Tilio-Aceretum) is composed of the following layers: leaf litter and humus (0–15cm), organo-mineral layer (15–45 cm) clearly separated from scree (45–110).
To sample isopods, non-baited subterranean pitfall traps designed by
To describe quantitative and qualitative characteristics of isopod communities, we calculated dominance, constancy, Shannon’s diversity index, and Pielou’s evenness index. The last two indices were first calculated for the material from each scree slope site separately and then collectively for the material from all sites. Due to the low number of isopods sampled, we were not able to perform more complex statistical analysis of our results. Dominance (D) was calculated by the formula D = 100*n/N where n is the number of individuals belonging to the specific species and N is the number of all individuals sampled. Constancy (C) was calculated using the formula C=100*pA/P where pA is the number of study sites on which, the specific species were sampled and P is the total number of study sites. Then after calculations, species were subdivided into the categories reflecting their dominance: subrecedent (D < 1%), recedent (D = 1–2%), subdominant (D = 2–5%), dominant (D = 5–10%), eudominant (D > 10%) and constancy: rare (C < 25%), widespread (C = 25–50%), constant (C = 50–75%), common (C > 75%). Shannon’s diversity index (H’) was calculated by the formula H = -∑(Pi*lnPi), where Pi is the fraction of the entire population made up of species i (proportion of a species is relative to a total number of species present, not encountered). Pielou’s evenness index (J’) was computed by the formula J’ = H’/H’max = H’/lnS where S is the number of species encountered (
In total, 252 isopod specimens belonging to eleven species and six families were sampled from eight investigated scree slope sites (Table
List of sampled isopod species and community characteristics. Abbreviations: C-Constancy: com-common, con-constant, wi-widespread, ra-rare; D-Dominance: ed-eudominant, do-dominant, sd-subdominant, re-recedent, sr-subrecedent. The numbers indicating particular studied scree slopes are stated in Figure
Species | Study sites / ex | C | D | ||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|
1 | 2 | 3 | 4 | 5 | 6 | 7 | 8 | ∑ | (%) | degree | (%) | degree | |
Hyloniscus riparius (C Koch, 1838) | 7 | – | 1 | – | 1 | 2 | – | – | 11 | 50 | con | 4.4 | sd |
Lepidoniscus minutus (C Koch, 1838) | – | – | – | – | – | 25 | – | 2 | 27 | 25 | wi | 10.7 | do |
Ligidium germanicum Verhoeff, 1901 | – | – | – | – | – | – | – | 37 | 37 | 12.5 | ra | 14.7 | do |
Ligidium hypnorum (Cuvier, 1792) | – | – | – | – | – | – | – | 2 | 2 | 12.5 | ra | 0.8 | sr |
Mesoniscus graniger (Frivaldsky, 1865) | – | 7 | 15 | 40 | – | 16 | 14 | 45 | 137 | 75 | com | 54.4 | ed |
Orthometopon planum (Budde-Lund, 1885) | – | – | – | – | – | 4 | – | – | 4 | 12.5 | ra | 1.6 | re |
Porcellium collicola (Verhoeff, 1907) | – | – | – | – | – | 17 | – | – | 17 | 12.5 | ra | 6.8 | sd |
Porcellium conspersum (C Koch, 1841) | – | – | – | – | – | – | 1 | – | 1 | 12.5 | ra | 0.4 | sr |
Protracheoniscus politus (C Koch, 1841) | – | 2 | 1 | – | – | – | 1 | – | 4 | 37.5 | wi | 1.6 | re |
Trachelipus ratzeburgii (Brandt, 1833) | 2 | – | – | – | – | – | – | – | 2 | 12.3 | ra | 0.8 | sr |
Trichoniscus carpaticus Tabacaru, 1974 | – | – | 1 | – | – | – | – | 9 | 10 | 25 | wi | 4.0 | sd |
∑ ex. | 9 | 9 | 18 | 40 | 1 | 64 | 16 | 95 | 252 | 100 | – | 100 | – |
∑spp. | 2 | 2 | 4 | 1 | 1 | 5 | 3 | 5 | 11 | – | – | – | – |
Shannon’s diversity index | 0.53 | 0.53 | 0.63 | 0 | 0 | 1.35 | 0.46 | 1.11 | – | – | – | – | – |
Pielou’s evenness index | 0.2 | 0.24 | 0.22 | 0 | 0 | 0.32 | 0.17 | 0.24 | – | – | – | – | – |
Looking at depth distribution, the vast majority of species were exclusively sampled in the uppermost levels of the depth profile (5–15 cm). Only three species were distributed deeper in higher numbers, M. graniger, Porcellium collicola, and Hyloniscus riparius. The occurrence of other species in the lower parts of the scree slope profile was rather infrequent (Table
A summary overview of the isopod depth distribution in the eight Western Carpathian scree slopes.
Depth (cm) | H. riparius | M. graniger | L. minutus | Li. germanicum | Li. hypnorum | O. planum | P. collicola | P. conspersum | Pr. politus | Tra. ratzeburgii | T. carpaticus | ∑ |
---|---|---|---|---|---|---|---|---|---|---|---|---|
5 | 2 | 1 | 26 | 36 | 2 | 4 | 7 | – | 2 | 2 | 10 | 92 |
15 | 3 | 14 | – | 1 | – | – | 4 | – | 2 | – | – | 24 |
25 | – | 25 | – | – | – | – | 1 | – | – | – | – | 26 |
35 | – | 29 | – | – | – | – | 1 | 1 | – | – | – | 31 |
45 | – | 18 | – | – | – | – | 1 | – | – | – | – | 19 |
55 | 3 | 7 | 1 | – | – | – | – | – | – | – | – | 11 |
65 | – | 11 | – | – | – | – | – | – | – | – | – | 11 |
75 | 1 | 11 | – | – | – | – | 1 | – | – | – | – | 13 |
85 | – | 14 | – | – | – | – | 1 | – | – | – | – | 15 |
95 | 2 | 7 | – | – | – | – | 1 | – | – | – | – | 10 |
∑ | 11 | 137 | 27 | 37 | 2 | 4 | 17 | 1 | 4 | 2 | 10 | 252 |
Assessment of isopod seasonal activity was based on M. graniger sampled on two pairs of sites with the same duration of samplings: the first pair is represented by the scree slopes in the Belinské skaly and Drienok Valley (sites 2 and 3, respectively) while the second pair by the scree slopes next to the Ardovská Cave and ice cave Silická ľadnica (sites 6 and 7, respectively). On the sites 2 and 6, warm/cold (= May-October/November-April) season ratio was almost 50:50 but on the sites 3 and 7, markedly more specimens were collected during the warm sampling period. Taking into account all 4 study sites together, 70% of specimens were collected during the warmer sampling periods (Figure
Regarding pH, more study sites are located on limestone, thus soil pH is alkaline. Only two study sites have acidic soil pH. In comparison of abundance, on alkaline study sites 193 specimens were sampled, but on acidic sites only 18 (soil pH was not measured on study sites 3 and 4). Alkaline study sites are more diverse with average of four species on one study site, against two species on both acidic study sites. Total number of species on alkaline study sites is ten, on acidic study sites it is only four.
Rather scarce communities of terrestrial isopods, in terms of species number, were found to inhabit shallow depths on forested scree slopes in the Western Carpathians. This finding reflects the distributional pattern of terrestrial isopods in Europe with the most important hotspots situated in the Mediterranean regions (
In the case of Isopoda, the typical number of species sampled in various surface habitats, such as forests, groves or pastures, ranges from 3 to7 (
Relative abundance and depth distribution of isopods sampled inside the forested scree slopes clearly reflect the amount of organic residues along the depth profile, which tends to be the highest in the uppermost layers and to decrease downwards the depth profile as observed by
As regards seasonal activity of M. graniger, our results prove the warm period of the year (vegetation period) to be the seasons with higher activity of M. graniger. Seasonal activity of other species was not assessed, due to their low abundance. This indirectly suggests that there is no massive seasonal vertical migration of the isopods into deeper layers of the forest scree slopes. Migration of terrestrial isopods into the deep soil is not necessary, since they can spend winter periods at shallow depths. Fallen leaves and snow cover provide a sufficient isolating layer to prevent lower lethal temperatures to isopods from being reached. Avoiding the uppermost layer of substrate, where the temperature has fallen below freezing point for several winter months, as overwintering isopod strategy could be minimized to move to a depth of a few centimeters under appropriate conditions, when the surface of soil is covered by fallen leaves and snow (
Comparison of fixative solutions ended up more positively for ethylene glycol in which, more than 50% individuals of Isopoda were sampled. This was probably caused by the repelling effect of formaldehyde, since ethylene glycol was confirmed to show neither strong repellent nor strong attractive effect on arthropods (
It is not clear from our research, how pH is affecting terrestrial isopods assemblages, since our species and specimens counts are very low. If we take a look at the dominant M. graniger, we can see that this species is not affected by pH, due to the presence of this species on both alkaline and acidic study sites. The reason why this species is missing from study site 1 is that it is outside the distribution area of this species (
The shallow underground of forested scree slopes in Slovakia is not inhabited by unique terrestrial isopods, but is uncommonly visited by surface (forest) species or by the sole subterranean species sampled (Mesoniscus graniger). The interior of forested scree slope can be considered as a part of subterranean environment inhabited in the long term by fauna specialized to live in permanent darkness. Eleven species were sampled in total, which is more than one third of the autochthonous isopod fauna in Slovakia. Well-preserved status of scree habitats is supported by the presence of the rare species, Mesoniscus graniger, Orthometopon planum, and minute Carpathian endemic Trichoniscus carpaticus. Subterranean pitfall traps with ethylene glycol proved themselves as suitable apparatuses to collect macrofauna from this environment.
We express our gratitude to all the colleagues who enthusiastically helped us during the field work: Martina Červená, Maroš Dzurinka, Peter Fenďa, Jana Frisová, Beáta Haľková, Alexandra Jászayová, Nikola Jureková, Ľubomír Kováč, Katarína Krajčovičová, Michal Krajňák, Vladimír Papáč, Tamara Šašková, and Richard Zamec. Sincere thanks for proofreading of the manuscript are due to Steve J Gregory. The study was supported by the grant 1/0199/14, financed by the Slovak Grant Agency VEGA. Grant 1/0346/18 financed by Slovak Grant Agency VEGA and grant APVV-17-0477 financed by Slovak Research and Development Agency.