Testate amoebae communities from caves of some territories in European Russia and North-Eastern Italy Текст научной статьи по специальности «Биологические науки»

Protistology 7 (1), 42-50 (2012)

Protistology

Testate amoebae communities from caves of some territories in European Russia and North-Eastern Italy

Yuri Mazei1, Olga Belyakova1, Alisa Trulova1, Laura Guidolin2 and Olimpia Coppellotti2

1 Department of Zoology and Ecology, Penza State Pedagogical University, Penza, Russia

2 Department of Biology, University ofPadova, Padova, Italy Summary

The species composition of testate amoebae in caves from European Russia and North-East Italy was studied. Twenty-seven species were identified from various habitats inside caves (moist substratum on floor, guano, sediments of cave streams and pools, water droplets and bacterial mats on rocky surfaces). In caves of simple structure (without differing types of habitats), the species richness of testate amoebae was far lower than in that from habitats outside the caves. In heterogeneous caves, species diversity of testate amoebae reached comparable levels with rhizopod communities from soil litter and mosses growing on rocks and soils. The abundances of testate amoebae in all cases decreased significantly inside caves. Widely distributed eurybiont testate amoebae species shape the speleo-communities. The total list of testate amoebae found in caves, based on currently available and published data, amounts to 82 taxa.

Key words: testate amoebae, caves, Italy, Russia

Introduction

Testate amoebae are unicellular organisms inhabiting a range of biotopes in the biosphere including freshwaters, wetlands and soils (Chardez, 1967). Communities from these habitats are well-known and have been intensively studied over the last century. The most abundant and diverse testate amoebae assemblages are found to exist in wet soils with high organic content and low rates of decomposition as well as in nutrient-rich freshwater sediments (Geltzer et al., 1985). However, the peculiar traits which characterize

the communities from untypical habitats (derived from those mentioned above) are still poorly known. Two hypotheses may be proposed. First, protozoan assemblages are characterized by peculiar species composition in such biotopes as epiphytic mosses and lichens, hollows in tree trunks, wet substrates on the walls and floors ofcaves, etc. Second, species sets in non-typical habitats represent simplified variants of those communities inhabiting wet soils, bogs and freshwater sediments.

Information concerning cave-dwelling protozoa is still not sufficient to reveal general patterns of biodiversity in the range ofcave habitats, geographical

© 2012 The Author(s)

Protistology © 2012 Protistological Society Affiliated with RAS

regions and types of caves. Several studies have been devoted to free-living protozoa inhabiting various caves (Gittleson and Hoover, 1969, 1970; Sudzuki and Hosoyama, 1991; Coppellotti and Guidolin, 1999, 2001, 2003; Guidolin and Coppellotti, 1999; De Luca et al., 2005). Primary attention has been paid to certain groups like ciliates, naked amoebae and flagellates (Coppellotti and Guidolin, 1999, 2003; Mulec, 2008; Bastian et al., 2009; Walochnik and Mulec, 2009). Few papers have focused on or contain information about testate amoebae (Griepenburg, 1933; Decloitre, 1955; Varga, 1959, 1963; Chibisova, 1967; Delhez and Chardez, 1970; Golemansky and Bonnet, 1994). Thus, the aim of the present study was to describe the species composition and community structure of testate amoebae from differing biotopes in various types of caves in European Russia and North-East Italy.

Material and methods

This study was conducted in 2009—2010. Samples were taken from three regions (Fig. 1): (I) North-East Italy (Veneto Region), (II) Middle Volga region in Russia (Samara Territory), and (III) Northern Urals in Russia (Komi Republic). In each cave, major habitats (including moist substrates on the floor, guano, sediments of cave streams and pools, water droplets and bacterial mats on rocky surfaces) were studied in triplicate. Altogether, 19 habitats (57 samples) were analysed: 7 from NE Italy, 12 from Middle Volga region, and 1 from the Northern Urals. The cave in the Berici Hills called the “Covolo della Guerra” (“War Cave”) was studied in NE Italy (Coppellotti and Guidolin, 1999). It is the most heterogeneous of all those studied, in that it represents different types of substrates for testate rhizopods. Artificial caves (adits) in the limestone Zhiguli mountains were studied in the Samara Territory (Smirnov et al., 2007; Smirnov and Vekhnik, 2011). One small cave was studied in a bank of the river Pechora within the Pechora-Ilych biosphere reserve (Gorchakovskii and Kharitonova, 2007; Bobkova et al., 2010). Testate amoebae from mosses growing on the surfaces of calcareous rocks as well as soil litter and mosses growing on soils in front of caves were analysed for comparisons with cave communities.

Samples were investigated following the procedure described in detail earlier (Mazei et al., 2011) with an Axiostar plus microscope (Zeiss, Germany) under 160x magnification.

Fig. 1. Regions studied are marked by black circles: I — North-East Italy; II — Middle Volga region, Russia; III — Northern Urals, Russia.

Results

Twenty-seven testate amoebae species were identified during our survey (Table 1). The most diverse genera were Centropyxis and Euglypha (Fig. 2). The most peculiar species composition was discovered in the cave of the Veneto Region. Many taxa were identified only from this cave (Centropyxis cassis spinifera, C. aculeata oblonga, Cyclopyxis kahli, Difflugia levanderi, Heleopera sylvatica, Cyphoderia ampulla, C. trochus). Some species common within the cave were absent in the biotopes outside (Table 1). All the species belonged to the limnophilous group and indicated moist conditions in this cave. The peculiarity of species composition in the adits of the Samara Territory was due to the development of species common to mosses (Assulina seminulum, Hyalosphenia papilio, Arcella arenaria compressa). Only two species were found in three samples from the cave on the bank of Pechora.

The set of dominant species in caves (Table 2) contained widely distributed eurybiont taxa such as Centropyxis aerophila, Phryganella hemisphaerica, Phryganella acropodia, Euglypha rotunda. However, the species dominant in each region were different. The freshwater species Centropyxis aculeata oblonga was the most abundant in the “Covolo della Guerra”. In the Middle Volga area moss-dwelling taxa Nebela tincta and N. parvula dominated.

The maximal species richness (21 species) was observed in the most biotopically heterogeneous “Covolo della Guerra”. Abundances varied form 0 (7 samples were empty) to 5200 individuals per gram ofabsolutely dry substrate, and averaged 1000 ind./g.

Fig. 2. Scanning electron micrographs of selected testate amoebae found in caves: a — Phryganella hemisphaerica, b — Trinema complanatum, c — Euglypha tuberculata, d — Nebela tincta, e — Centropyxis aerophila, f — Cyphoderia ampulla. Scale bar: 10 ^m.

The diversity of testate amoebae in biotopes outside caves was similar (19—24 species) in the different regions (Table 2), with abundances of up to 25000 ind./g. According to the Mann-Whitney test, the differences were significant (p<0.05).

The three regions differed considerably in the structure of total species diversity (Fig. 3). In NE Italy the proportions of species found only inside caves, others only outside, and some in both habitats, were similar; in other words, the specificity of species composition inside and outside the cave was equal. In contrast, the peculiarity of species sets in Russian caves (which are much smaller [in the Urals] and less heterogeneous [in the Middle Volga]) was lower than those from soil habitats in surrounding forests.

Discussion

Our findings show that in caves of simple structure (without differing types of habitats, e.g. guano, sediments of freshwater streams and pools, microbial mats, etc.) the species richness of testate amoebae is far lower than those from habitats outside caves. Otherwise, in heterogeneous caves, the species diversity of testate amoebae reached levels comparable to those ofrhizopod communities from soil litter and mosses growing on rocks and soils. However, the abundances of testate amoebae in all cases decreased significantly inside caves if compared with outside areas. Widely distributed eurybiont testate amoebae species shape the speleocommunities. We did not find any specific

Table 1. Testate amoebae identified from various caves*.

Taxa Present study Literature data

Italy Volga region Urals Decloitre, 1955 Chibisova, 1967 Delhez, Chardez, 1970 Golemansky, Bonnet, 1994 Coppellotti, Guidolin, 1999

Arceíía arenaria compressa Chardez, 1974 - + - - - - - -

A. discoides Ehrenberg, 1847 - - - - + - - -

A. papyracea Playfair, 1914 - - - + - - - -

Arceíía sp. - - - - - - - +

Centropyxis acuíeata oblonga Deflandre, 1929 + - - - + - - -

C. aerophiía Deflandre, 1929 + + + - - + - -

C. a. sphagnicoía Deflandre, 1929 + + - - - + - -

C. a. minuta Chardez - - - - - + - -

C. cassis (Wallich, 1864) Deflandre, 1929 - - - - - + - -

C. c. spinifera (Playfair,1918) Deflandre, 1929 + - - - - - - -

C. constricta (Ehrenberg, 1841) Deflandre, 1929 - - - - + - - -

C. irreguíaris Decloitre, 1955 - - - + - - - -

C. íaevigata Penard, 1890 + - - - - - + -

C. minuta Deflandre, 1929 - - - + - + - -

C. orbicuíaris Deflandre, 1929 - - - - + - - -

C. píagiostoma Bonnet et Thomas, 1955 - - - - + - - -

C. píatystoma (Penard, 1890) Deflandre, 1929 - - - + + - - -

C. spinosa (Cash, 1909) Deflandre, 1929 - - - - + - - -

Cycíopyxis arceííoides (Penard, 1902) Deflandre, 1929 - - - - + - - -

C. bathystoma Chibisova, 1967 - - - - + - - -

C. eurystoma Deflandre, 1929 - - - + - - + -

C. kahíi Deflandre, 1929 + - - - + - - -

C. k. grandis Chibisova, 1967 - - - - + - - -

C. penardi minor (Penard, 1911) Deflandre, 1929 - - - - + - - -

Trigonopyxis arcuía Leidy, 1879 - - - + - - - -

Píagiopyxis caííida Penard, 1910 - - - - + + + -

P. decíivis Thomas,1958 - - - - - - + -

P. minuta Bonnet, 1959 - - - - - - + -

Difflugia aveííana Penard, 1890 - - - - + - - -

D. aveííana gigas Gauthier-Lievre et Thomas, 1958 - - - - + - - -

D. bryophiía (Penard, 1902) Jung, 1942 - - - + - - - -

D. curvicoíis trogíodyta Delhez et Chardez, 1970 - - - - - + - -

Table 1. (Continuation).

Taxa Present study Literature data

Italy Volga region Urals Decloitre, 1955 Chibisova, 1967 Delhez, Chardez, 1970 Golemansky, Bonnet, 1994 9 9 , & ° c n ou CG

D. e/ongata Penard, 1905 - - - - + - - -

D. /ebes Penard, 1893 - - - - + - - -

D. /evanderi Playfair,1918 + - - - - - - -

D. /ucida Penard, 1890 + - - - - - - -

D. penardi Hopkinson,1909 - - - - + - - -

D. ob/onga Ehrenberg, 1838 - - - - + - - -

Difflugia sp. - - - - - - - +

Pontigu/asia incisa Rhumbler, 1896 - - - - + - - -

Lesquereusia spira/is (Ehrenberg, 1840) Butschli, 1888 - - - + - - - -

Hya/osphenia minuta Cash, 1891 - - - + - - - -

H. papi/io Leidy, 1879 - + - - - - - -

H. shoutedeni van Oye, 1926 - - - + - - - -

He/eopera picta Leidy, 1879 - - - + + - - -

H. petrico/a Leidy, 1879 - - - + - - - -

H. sy/vatica Penard, 1890 + - - + - - - -

Argynnia caudata (Leidy, 1879) Vucetich, 1974 - - - + - - - -

A. dentistoma (Penard, 1890) Vucetich, 1974 - - - + - - - -

Nebe/a parvu/a Cash, 1909 - + - - - - - -

N. penardiana Deflandre, 1936 - - - + - - - -

N. tincta Leidy, 1879 - + - - - - - -

Quadru/e//a e/egans Gauthier-Lievre, 1953 - - - + - - - -

Q. symmetrica curvata Wailes, 1912 - - - + - - - -

Q. symmetrica tubu/ata Gauthier-Lievre, 1953 - - - + - - - -

Q. symmetrica /ongico//is Taranek, 1882 - - - + - - - -

Phrygane//a acropodia (Hertwig et Lesser, 1874) Hopkinson, 1909 + + - + - + + -

Ph. a. penardi Decloitre, 1955 - - - + - + - -

Ph. hemisphaerica Penard, 1902 - + + - - - - -

Cryptodifflugia oviformis Penard, 1890 - - - - - - - +

Assu/ina seminu/um (Ehrenberg, 1848) Leidy, 1879 - + - - - - - -

Eug/ypha ci/iata g/abra Wailes,1915 + - - - - - - -

E. /aevis Perty, 1849 - - - - - + - -

Table 1. (Continuation).

Taxa Present study Literature data

Italy Volga region Urals Decloitre, 1955 Chibisova, 1967 Delhez, Chardez, 1970 Oï c at, E £ " ¡= oo Coppellotti, Guidolin, 1999

E. rotunda Wailes,1915 + + - + - - + -

E. strigosa (Ehrenberg, 1871) Leidy, 1878 + - - - - - - -

E. tuberculata Dujardin, 1841 + - - + - - - +

E. t. minor Taranek, 1882 - - - + - - - -

Placocista glabra minima Decloitre, 1955 - - - + - - - -

P. lens Penard, 1899 - - - + - - - -

Sphenoderia fissirostris Penard, 1890 - - - + - - - -

S. minuta Deflandre, 1931 - - - + - - - -

Tracheleuglypha acolla Bonnet et Thomas, 1955 - - - - - + + +

T. a. elongata Delhez et Chardez, 1970 - - - - - + - -

Cyphoderia ampulla (Ehrenberg, 1840) Leidy, 1879 + - - - - + - -

C. dentata Lepsi, 1957 - - - - - - - +

C. grandis Penard, 1890 - - - - - - - +

C. trochus Penard, 1899 + - - - - - - -

Trinema complanatum Penard, 1890 + + - + - - - -

T. enchelys (Ehrenberg, 1838) Leidy, 1878 + + - + - - + +

T. lineare Penard, 1890 + - - + - + + -

Corythion dubium Taranek,1881 + - - - - - - -

C. orbicularis (Penard, 1910) Iudina, 1996 + - - - - - - -

Number of species 21 12 2 32 21 14 10 8

* Data include information from various habitats in darkness inside caves; "+" present; "-" not registered.

forms. However, two organisms were not identified at species level.

Lack of specific taxa in caves has already been reported earlier (Chibisova, 1967). Among 21 testate amoebae species and forms discovered in 8 caves from different parts of the Soviet Union, the above author described one new taxon (Table 1) and concluded that the whole species set was common to freshwaters and soils. Decloitre (1955) and Delhez and Chardez (1970) described 2 new taxa in each paper. However, their species lists also include species primarily distributed elsewhere (Table 1). Until now, 82 species and subspecific taxa

of testate amoebae have been reported as living in true (unlighted) cave habitats (Table 1).

Golemansky and Bonnet (1994) interpreted testate amoebae fauna in caves as being composed of trogloxenes, ordinary and cosmopolitan organisms. The population of testate rhizopods seems to have a triple origin (Golemansky and Bonnet, 1994). First, it includes aquatic taxa of the genera Arcella, Centropyxis, Cyphoderia, Difflugia, Eugly-pha, Pontigulasia, Sphenoderia, etc. We found representatives of this group in the “Covolo della Guerra”, which contains suitable habitats. Second, the population includes rhizopods inhabiting mosses

Table 2. Relative abundance (% of total abundances) of dominating species and total species numbers of testate amoebae in different regions and biotopes.

Taxon Region and biotope investigated

NE Italy Middle Volga Northern Urals

cave moss cave moss cave moss

Centropyxis aerophila 10.8* 22.6 7.3 19.6 33.4 17.1

Phryganella hemisphaerica 0.0 1.8 3.6 1.9 66.6 10.4

Phryganella acropodia 5.2 28.0 30.4 5.4 0.0 10.3

Euglypha rotunda 10.1 0.4 8.1 2.2 0.0 24.3

Nebela tincta 0.0 0.0 26.3 8.0 0.0 0.7

Centropyxis aerophila sphagnicola 8.5 4.5 1.8 9.0 0.0 0.0

Euglypha ciliata glabra 8.8 0.0 0.0 12.1 0.0 1.9

Trinema enchelys 12.2 0.0 4.2 3.1 0.0 0.0

Cyclopyxis kahli 0.8 18.3 0.0 0.1 0.0 0.0

Arcella arenaria compressa 0.0 0.8 3.6 5.4 0.0 7.0

Heleopera sylvatica 2.9 11.4 0.0 0.0 0.0 0.0

Centropyxis aculeata oblonga 13.6 0.0 0.0 0.0 0.0 0.0

Nebela parvula 0.0 0.0 11.1 0.0 0.0 0.0

Number of species 21 20 12 24 2 19

* Relative abundances exceeded 10% are in bold.

of the genera Centropyxis, Cyclopyxis, Heleopera, Nebela, Hyalosphenia, Phryganella, Euglypha, Assulina, Tracheleuglypha, Corythion, Trinema etc. We found members of this group in large, more or less heterogeneous caves, both natural (in Italy) and artificial (in Middle Volga region). Third, it comprises soil-dwelling protozoa of the genera Centropyxis, Cyclopyxis, Phryganella, Assulina, Tracheleuglypha, Trigonopyxis, Trinema, etc., since we identified such organisms in all caves. The smallest cave of those investigated in this study (in the Northern Urals) is inhabited solely by this group of the most eurybiont amoebae.

As in our study, Golemansky and Bonnet (1994) emphasized that the density of testate amoebae in caves is low. Many habitats do not reveal the shells of amoebae (Delhez and Chardez, 1970), although density increased in habitats enriched in organic matter (e.g., guano). Nevertheless, as part of the microbial community, testate amoebae may play an important role in the structuring and functioning of the whole speleo-ecosystem. Microorganisms in caves have been shown to be involved in lithogenic processes, e.g., speleothem deposition and cavern enlargement (Engel et al., 2004; Cacaveras et al., 2006; Mulec et al., 2007; Mulec, 2008) and litholitic processes. Testate amoebae may be transported inside caves by infiltrating superficial waters, by air, or transported by troglophilic and trogloxenic animals, and may subsequently develop considerably

in this milieu, in which high abundances ofbacteria, fungi, heterotrophic flagellates and “naked” amoebae are found. In such habitats, usually rich in biogenic elements, testate rhizopods play an important role as a trophic link between bacteria and small metazoans in the functioning of the food web in the whole speleo-ecosystem (Golemansky and Bonnet, 1994; Coppellotti and Guidolin, 2003).

Acknowledgements

Authors are grateful to Sergei Titov for aid during sampling in the “Covolo della Guerra” and to Dmitry Smirnov for help in the field trip in the Zhiguli mountains. This work was supported by a grant from the University of Padova (International Relations) and the Russian Foundation for Basic Research (grant no. 10-04-00496a) to Yuri Mazei.

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Address for correspondence: Olimpia Coppellotti. Department of Biology, University of Padova, Via U. Bassi 58/B, 35131 Padova, Italy, e-mail: olimpia.coppellotti@unipd.it