Protistology 7 (1), 51–58 (2012) Protistology

Testate amoebae of tundra landscapes

A. A. Bobrov1 and S. Wetterich2

1 Soil Department of Moscow State University, Moscow, 2 Alfred-Wegener-Institut for Polar- and Marine Research, Department of Periglacial Research, Potsdam, Germany

Summary

Testate amoebae (rhizopods) from Russian tundra landscapes of the arctic mainland and islands were studied. In a total of 274 samples analyzed, 215 species and subspecies were found. More than half of the species diversity was represented by hygro- and hydrophilic, and sphagnophilic species of four genera: Difflugia, Centropyxis, Arcella and . Almost all species belong to the cosmopolitan group of testate amoebae. Only Centropyxis gasparella, C. gasparella v. corniculata, C. pontigulasiformis, Difflugiella vanhoornei and Difflugia ovalisima might be attributed to arctic endemics because they have not been reported so far from other regions than the Arctic.

Key words: testate amoebae, tundra, arctic Yakutia, Siberian Arctic

Introduction table, moisture, pH, content of biophilic elements (C, N, P, K, Ca, Mg) by restructuring their Testate amoebae are a group of free-living communities. Testate amoebae can be classified into protozoans having an external shell (testa). Some ecological groups according to their requirements taxa from this group are covered with exogenous concerning moisture (hygrophiles, hydrophiles, mineral material (xenosomes), plant detritus, or xerophiles), pH (acidophiles, calciophiles), habitat endogenous material (idiosomes), such as silica or, preferences (sphagnophiles, soil-inhabiting, aqua- rarely, calcium phosphate plates. Their well-defined tic). Their density in lake sediments, peat and ecological preferences and the relatively good soils can vary from a few hundred to tens of preservation of fossil shells in peats, lake sediments, thousands of shells per cm3. The number of taxa in and buried soils form the basis for the development oligotrophic bogs can reach several tens of species of rhizopod analysis as a method for reconstruction and infraspecific forms. The significance of rhizopod of climate and environmental changes (Meisterfeld, analysis for paleoecological studies is based on the 1977; Tolonen, 1986; Charman et al., 2007, 2009, fact that testate amoebae are permanently affixed to 2010; Booth, 2010; Tsyganov et al., 2011, 2012; the substrate. Their shells are normally destroyed if Sullivan and Booth, 2011). the sediments are redeposited. Therefore, they are Testate amoebae, being inherently aquatic, often the only organisms that can directly indicate respond to environmental changes in ground water the paleoenvironmental conditions during sediment

© 2012 The Author(s) Protistology © 2012 Protozoological Society Affiliated with RAS 52 · A.A. Bobrov and S. Wetterich formation, unlike many other biological remains. and East Siberian Arctic, but also from Alaska (Fig. The study of modern rhizopods in the Arctic was 1, Table 1): Archipelago (1, 2), initiated in the late 19th and early 20th centuries Taymyr Peninsula (3), Western Laptev Sea (4), (Scourfield, 1897; Penard, 1903; Sandon, 1924) Lena Delta (5, 6. 7, 8), Central Laptev Sea region and was continued after a long interval. Moss and (9), New Siberian Archipelago (10, 11), Indigirka lichen pads, soils, and small pools were studied lowland (12) and Seward Peninsula, Alaska (13). in eastern and western Greenland, northwestern The overall modern climate conditions are Spitsbergen, Brabant Island, and some other Arctic harsh and characterized by long (>8 month), severe areas (Bonnet, 1965; Schönborn, 1966; Beyens winters and short cold summers with mean July and Chardez, 1986; Beyens et al., 1986a, 1986b; temperatures of about or below 9 °C, mean January 1991, 1992, 2000; Smith, 1987; Opravilova, 1989; temperatures of about or above -34 °C, and annual Balik, 1994). In a recent study on the rhizopod precipitation from about 80 to 300 mm (Atlas fauna of northeast Greenland (Trappeniers et al., Arktiki, 1985). 2002) special attention was paid to an evaluation of Soils in the area are mainly tundra-gley and quantitative relationships between the composition peaty-gley (histosols and inceptisols) with an active- of testate amoebae soil assemblages and ecological layer thickness of about 30 to 40 cm. The area belongs parameters (pH, organic matter, moisture) of their to the zone of northern tundra. Mosses, grasses and habitats and communities. low shrubs dominate the vegetation, with typical Modern testate amoebae of the Russian Arctic vascular plant species such as Betula exilis, Dryas are almost not described. Only three publications punctata, Salix pulchra, Cassiope tetragona, Oxyria during the last 110 years were devoted to this region. digyna, Alopecurus alpinus, Poa arctica, Carex Rhizopods collected near Murmansk and Vaygach ensifolia, C. rotundifolia, Eriophorum medium, mosses Island in Russian Arctic were studied by Awerinzev Aulacomnium turgidum, Hylocomium alaskanum, and Levander (Beyens et al., 2000). The rhizopods Drepanocladus iniciatus, Calliergon sarmentosum, are not numerous in the moss and aquatic biotopes and lichens Alectoria ochroleuca, Cetraria cuculliata of the coastal areas of the Barents and Kara Seas, and C. hiascus (Atlas Arktiki, 1985). only 45 species, varieties and forms have been found Samples of soil and sediments were suspended there (Beyens et al., 2000). in water and passed through 500 µm mesh to remove Since many years, the East Siberian Arctic large particles. Rhizopod shells were concentrated attracted paleoecologists who studied late Quater- with a centrifuge. A drop of suspension was placed nary and modern environment (Yurtsev, 1981; Sher, on the slide, and the glycerol was added. Normally, 1987a, 1987b). However, data about soil-inhabiting 5 subsamples from each sample were examined at protozoa are still lacking except of one publication 200-400× magnification with the light microscope. where testate amoebae findings of ground surface The PAST software was employed to analyze the samples from Bykovsky Peninsula (Central Laptev data. Sea) are mentioned (Bobrov et al., 2004). Earlier studies showed that (1) the density and biodiversity of testate amoebae in the modern Results and discussion high-latitude Arctic decrease with the decrease in average summer temperatures, i.e. with harsher In a total of 274 surface samples from different climate conditions, and (2) some species respond elements of arctic tundra landscapes, 215 species to lower temperatures by reducing the size of their and subspecies have been identified. More than shells (Smith, 1988). half of the taxa belong to hygro-hydrophilic and The aim of this study is to conduct a detailed sphagnobiontic species of the genera Difflugia, analysis of modern testate amoebae from the East Centropyxis, Arcella, Euglypha (Fig. 2). Most of Siberian Arctic and Alaska, their geographical the identified species belong to the cosmopolitan distribution and ecological specifics. group, including sphagnobionts, hygro-hydrophiles, soil-inhabiting and eurybiontic species (Fig. 3). The ecological structure of the communities was similar Material and methods on arctic islands and on the mainland, and dominated by hygro-hydrophilic species. Outcrops of carbonate Modern testate amoebae communities have rocks ensure a broad presence of calciphiles, mainly been studied from a total of 274 soil, lake sediment represented by Centropyxis plagiostoma (sensu and peat surface samples mainly from the Central lato) which prefers neutral to slightly acidic pH. Protistology · 53

Fig. 1. Map of the Arctic, the Laptev Sea region and the sampling areas: 1 – October Revolution Island; 2 – Bol’shevik Island; 3 – Taymyr Peninsula; 4 – Cape Mamontov Klyk; 5 – Lake Nikolay; 6 – Ebe-Basyn-Sise Island; 7 - Olenyok Channel; 8 – Samoylov Island; 9 – Bykovsky Peninsula; 10 – Bol’shoy Lyakhovsky Island; 11 – Kotel’ny, Maly Lyakhovsky, Stolbovoy, Bel’kovsky islands; 12 – Berelekh River; 13 – Kitluk River.

Eurybiontic species among dominants include Greenland (Beyens and Chardez, 1995, 1997; Centropyxis aerophila, C. constricta v. minuta, Trappeniers et al., 1999). Centropyxis pontigulasi- C. sylvatica, Cyclopyxis eurystoma v. parvula, formis has a broader tolerance and distribution. It Schoenbornia humicola, Euglypha laevis and occurs under water and on mosses on Svalbard, lineare. on Devon and Victoria islands (Canadian Arctic), Testate amoebae species with restricted geo- and West Greenland (Beyens and Chardez, 1995). graphical distribution are of special interest: Difflugia ovalisima was described from moss samples Centropyxis gasparella, C. gasparella v. corniculata, of Devon Island (Beyens and Chardez, 1994), and C. pontigulasiformis, C. vandeli, Difflugia kabulica, Placocista lapponum occurs on Greenland and D. ovalisima, D. serpentrionalis, D. szczepanskii, Northern Sweden (Penard, 1917). Lesquereusia sphaeroides, Lamptoquadrulla sp., Some species also occur within the taiga zone Placocista lapponum, Difflugiella (Cryptodifflugia) as for instance Difflugiella (Cryptodifflugia) bassini angusta, D. bassini, D. minuta, D. pusilla, D. (Bobrov, 2001). The species Centropyxis vandeli was sacculus, D. sacculus v. sakotschawi, D. vanhoornei, described from mountain soils in southern France Pseudodifflugia jungi. Some of these species are (Bonnet, 1958) and found in hydrophilic soil mosses only found in arctic tundra: Centropyxis gasparella, in the Western Rhodopes, Bulgaria (Golemansky C. gasparella v. corniculata, C. pontigulasiformis, et al., 2006). The finding of Lamptoquadrula sp. is Difflugiella vanhoornei, Difflugia ovalisima. The of special interest because the type species of the hygrophilic species Centropyxis gasparella sensu genus (which includes so far only one species) was lato was so far reported from tundra environments described from soils in gallery forests in Côte-d’Ivore in the Canadian Arctic, in Alaska and in Northeast (Bonnet, 1975). Further evidence for rare species 54 · A.A. Bobrov and S. Wetterich

Table 1. List of testate amoebae from the 13 study sites as shown in Fig. 1.

Arcella arenaria, A. arenaria v. compressa, A. arenaria v. sphagnicola, A. artocrea, A. bathystoma, A. catinus, A. costata, A. costata, A. discoides, A. discoides v. scutelliformis, A. gibbosa, A.intermedia, A. megastoma, A. mitrata v. spectabilis f. A (minor), A. rotundata, A. rotundata v. aplanata, A. rotundata v. stenostoma, A. vulgaris, A. vulgaris v. crenulata, A. vulgaris v. wailesi Bullinularia indica, B. gracilis Trigonopyxis arcula Centropyxis aculeata, C. aculeata v. minima, C. aerophila, C. aerophila v. minuta, C. aerophila v. sphagnicola, C. cf. capucina, C. cassis, C. cassis v. spinifera, C. constricta, C. constricta f. minima, C. discoides, C. ecornis, C. ecornis sensu Ogden, Hedley 1980, C. ecornis v. megastoma, C. ecornis v. minima, C. elongata, C. gasparella, C. gasparella v. corniculata, C. gibba, C. kolkwitzi, C. laevigata, C. orbicularis, C. plagiostoma, C. plagiostoma v. oblonga, C. plagiostoma f. A (major), C. plagiostoma f. B (minor), C. plagiostoma f. C (lata), C. platystoma, C. platystoma f. A (minor), C. sylvatica, C. sylvatica v. globulosa, C. sylvatica v. microstoma, C. sylvatica v. minor, C. vandeli Cyclopyxis arcelloides, C. eurystoma, C. eurystoma v. parvula, C. intermedia, C. kahli, C. kahli v. cyclostoma Plagiopyxis callida, P. declivis, P. cf. declivis v. oblonga, P. labiata, P. labiata f. A (longa), P. minuta Heleopera lata, H. petricola, H. petricola v. amethystea, H. petricola v. humicola, H. sphagni, H. sylvatica, H. rosea Hyalosphenia minuta, H. papilio, H. subflava Nebela bigibbosa, N. bohemica, N. galeata, N. flabellum, N. lageniformis, N. militaris, N. minor, N. parvula, N. penardiana, N. tincta, N. tincta v. stenostoma Argynnia dentistoma, A. dentistoma v. lacustris, A. dentistoma v. laevis Schoenbornia humicola, Sch. Viscicula Difflugia ampulla, D. bacillariarum, D. bacillifera, D. brevicola, D. capreolata, D. cratera, D. humilis, D. gassowskii, D. geosphaerica, D. difficilis, D. globularis, D. globulosa, D. globulosus, D. globulus, D. gramen, D. kabulica, D. lata, D. linearis, D. lucida, D. mamilaris, D. mica, D. microstoma, D. minuta, D. molesta, D. nana, D. oblonga, D. oblonga v. gigantea, D. cf. ovalisima, D. parva, D. penardi, D. perfilievi, D. petricola, D. pristis, D. pulex, D. pyryformis, D. rotunda, D. rubescens, D. schurmani, D. serpentrionalis, D. tenius Lagenodifflugia vas, L. sphaeroides Netzelia oviformis Lesquereusia epistomium, L. longicollis, L. modesta, L. spiralis Pontigulasia incise Quadrulella symmetrica Paraquadrulla irregularis, P. penardi, P. cf. rotunda Phryganella acropodia, Ph. acropodia v. australica, Ph. hemisphaerica Assulina muscorum, A. muscorum v. stenostoma, A. seminulum Valkanovia delicatula, V. elegans Sphenoderia fissirostris Tracheleuglypha acolla, T. dentate Placocista glabra, P. lapponum, P. lens, P. jurassica, P. spinosa Euglypha acantophora, E. anadonta, E. anadonta v. magna, E. ciliata, E. ciliata f. glabra, E. compressa, E. compressa f. glabra, E. cristata, E. cuspidata, E. dolioliformis, E. filifera, E. filifera v. magna, E. laevis, E. laevis v. lanceolata, E. rotunda, E. strigosa, E. strigosa f. glabra, E. strigosa v. muscorum, E tuberculata Corythion dubium, C. dubium f. minima, C. dubium v. terricola, C. dubium v. orbicularis, C. pulchellum Trinema complanatum, T. complanatum v. platystoma, T. enchelys, T. lineare, T. lineare v. minuscule, T. lineare v. terricola, T. lineare v. truncatum, T. penardi Wailesella eboracensis Difflugiella angusta, D. apiculata, D. bassini, D. fulva, D. minuta, D. oviformis, D. oviformis v. fusca, D. patinata, D. pusilla, D. sacculus, D. sacculus v. sakotschawi, D. vanhoornei Pseudodifflugia gracilis, P. gracilis v. terricola, P. jungi Archerella flavum that occur in the Arctic comes from the circum- species and subspecies found in this study do not australian species Nebela martiali which has also reflect the total diversity of rhizopods in arctic tund- been found in surface samples from Dikson Island, ra landscapes. Eklips, and Franz Joseph’s Land (Beyens et al., The ordination of testate amoebae assemblages 2000). from different areas of the arctic tundra illustrates An important indicator of species diversity is that most rhizopod communities were rather similar. the relationship between the number of species However, pronounced differences were found e.g. and the number of sites examined (Fig. 4). The between assemblages from moss-lichen tundra of rarefaction curve demonstrates a high heterogeneity October Island (site No. 1 in Fig. 1) and moss- of the data set and suggests that for a more complete shrub polygonal tundra of the Berelekh River (site representation of species diversity much more than No. 12 in Fig. 1). The latter had a more structured 13 sampling sites are required. Therefore, the 215 micro-relief which led to small-scale differences Protistology · 55

in water content and vegetation cover as expressed by higher occurrences of sphagnobiontic and hygrophilic species of the genera Nebela, Difflugiella and Difflugia. According to literature data the list of testate amoebae in the Arctic comprises 291 species and subspecies (Beyens and Chardez, 1995). This inventory is based on more than 1000 samples representing typical soil and aquatic habitats in arctic tundra landscapes, published in studies since the beginning of the 20th century including regions of the North American Arctic. Soil habitats of the Russian forest zone (Bobrov, 1999) are dominated by the following genera: Centropyxis (35 species and subspecies), Euglypha (30), Nebela (20), Trinema (18). Arctic tundra habitats show a different species composition which is dominated by Difflugia (40 species and subspecies), Centropyxis (35), Arcella (20), Euglypha (20) which highlight the broader distribution of hydromorphic habitats in the tundra environment. The genera Geamphorella, Geopyxella, Hooge- nraadia, Planhoogenraadia, Proplagiopyxis, Pseudo- awerinzevia, Schwabia and other have not been found in soil and aquatic habitats of the arctic tundra because these taxa are restricted to pan-tropical and circum-australian or steppe and forest zones of the Holarctic. However, occasional findings of rare species prove that formation of arctic testacean communities is a complicated process. Based on literature and own studies we can conclude that arctic testate amoebae communities include several biogeographic fractions: (1) endemic arctic species; (2) sphagnobiontic species of the tundra and taiga zones; (3) holarctic species of the forest zone; (4) non-holarctic species of the pan-tropical and circum-australian zones; (5) eurybiontic cosmopolitan species. The most interesting groups are arctic endemics and non-holarctic species of the pan-tropical and circum-australian zones, which can be treated as relicts or paleoendemic species. Transportation and distribution of testate amoebae by atmospheric currents or birds also can not be excluded. Further research on biogeographic aspects of arctic testate amoebae is needed to resolve this question (Bobrov et al., 2004)

Acknowledgements

The study has been conducted under the auspices of the joint Russian-German RFBR- DFG project ‘Polygons in tundra wetlands: state Fig. 2. Distribution of arctic testate amoebae and dynamics under climate variability in polar species per genus. regions’ (RFBR grant N 11-04-91332-NNIO-a, 56 · A.A. Bobrov and S. Wetterich

Fig. 3. Ecological groups of testate amoebae in samples from (A) the arctic islands, and (B) the arctic mainland..

DFG grant N HE 3622-16-1). Colleagues from Beyens L. and Chardez D. 1986. Some new and the North-Eastern Federal University, Yakutsk (L. rare testate amoebae from the Arctic. Acta Protozool. Pestryakova), Hamburg University (F. Beermann), 25, 1, 81–91. Moscow State University (L. Kokhanova, V. Beyens L. and Chardez D. 1995. An annotated Tumskoy, E. Zhukova), Herzen State Pedagogical list of testate amoebae observed in the Arctic between University, St. Petersburg (V. Sitalo), and AWI the longitudes 27°E and 168°W. Arch. Protistenkd. Potsdam (L. Schirrmeister, A. Schneider) who 146, 219–233. conducted the fieldwork in the Berelekh River Beyens L., Chardez D. and Landtsheer R. 1986a. area in 2011 are greatly acknowledged. Long-term Testate amoebae communities from aquatic habitats support was provided by the German-Russian in the Arctic. Polar Biology. 6, 197–205. Scientific Cooperation Programs ‘Laptev Sea Beyens L., Chardez D. and Landtsheer R. 2000’ and ‘System Laptev Sea’ which provided 1986b. Testate amoebae populations from moss the frame for joint Russian-German expeditions and lichen habitats in the Arctic. Polar Biology. 5, since 1998 when most of the Siberian samples have 165–173. been obtained. Financial support came also from Beyens L., Chardez D. and Baere D. 1991. the RFBR project N 11-04-01171-a ‘Geography Ecology of aquatic testate amoebae in coastal and ecology of soil inhabiting testate amoebae’. Lowlands of Devon Island (Canadian High Arctic). The fieldwork at the Alaskan study site on Seward Arch. Protistenkd. 140, 23–33. Peninsula was organized by G. Grosse (University Beyens L., Chardez D. and Baere D. 1992. of Alaska Fairbanks) and financially supported The testate amoebae from the Sondre Strofjord by the National Science Foundation (NSF grant region (West-Greenland): their biogeographic N 0732735) and the DFG (DFG grants N SCHI implications. Arch. Protistenkd. 142, 5–13. 530/7-1, WE 4390/2-1 and KI 849/2-1). Additional Beyens L., Chardez D. and Van de Vijver B. support was provided from NASA Carbon Cycle 2000. A contribution to the protist-diversity in the Sciences (grant NNX08AJ37G). polar regions: testate amoebae date from the Russian Arctic. In: Ceulemans R., Bogaert J., Deckmyn G. and I. Nijs (Eds). Topics in ecology. Structure References and function in plants and ecosystems. Wilrijk, University of Antwerpen, pp. 101–110. Atlas Arktiki. 1985. Moscow. GUGK. 204 pp. Bobrov A.A. 1999. Ekologo-geograficheskie (in Russian). zakonomernosti rasprostraneniya i struktur soob- Balik V. 1994. On the soil testate amoebae fauna shestv rakovinnish ameb (Protozoa: Testacea). Eco- (Protozoa: Rhizopoda) on the Spitsbergen Islands logical-geographical regularities in distribution and (Svalbard). Arch. Protistenkd. 144, 365–372. structure of testate amoebae (Protozoa: Testacea) Protistology · 57

P.D.M. and Karofeld E. 2009. Climate drivers for peatland palaeoclimate records. Quaternary Sci. Rev. 28, 19–20, 1811–1819. Charman D.J., Gehrels W.R., Manning C. and Sharma C. 2010. Reconstruction of recent sea-level change using testate amoebae. Quaternary Research. 73, 2, 208–219. Golemansky V., Todorov M. and Temelkov B. 2006. Diversity and biotopic distribution of the Rhizopods (Rhizopoda: Lobosia and Filosia) from the Western Rhodopes (Bulgaria). In: Beron P. (Ed.) Biodiversity of Bulgaria. 3. Biodiversity of Western Rhodopes (Bulgaria and Greece) I. Pensoft and National Museum of Natural History Sofia, pp. 205–220. Meisterfeld R. 1977. Die horizontale und Fig. 4. Rarefaction curve (±95% confidence vertikale Verteilung der Testaceen (Rhizopoden, interval) for the communities of testate amoebae Testacea) in . Arch. Hydrobiol. 79, of the investigated areas according to Fig.1. Sphagnum 319–356. Opravilova V. 1989. Some information on coenoces. Doctor of Scienses Thesis. Moscow State testate amoebae from Spitsbergen. Fauna Norvegica University (in Russian). A. 10, 33–37. Bobrov A.A. 2001. Cryptodifflugia bassini is Penard E. 1903. Notice sur les Rhizopodes du a new species of sphagnobiontic testate Spitzbergen. Arch. Protistenkd. 2, 238–282. (Protozoa, Testacea). Zool. Zhurn. 80, 8, 1010– Penard E. 1917. Observations sur quelques 1013. Protozoaires peu connus ou nouveaux. Ann. Soc. Bobrov A.A., Schirrmeister L., Siegert Ch. and Zool. Suisse. 25, 1–50. Andreev A.A. 2004. Testate amoebae (Protozoa: Sandon H. 1924. Some Protozoa from the soils Testacealobosea and Testaceafilosea) as bioindica- and moss of Spitzbergen. J. Linnean Soc. Zool. 27, tors in the Late Quaternary deposits of the Bykovsky 449–475. Peninsula, Laptev Sea, Russia. Paleogeography, Scourfield D.J. 1897. Contributions to the non- Palaeoclimatology, Palaeoecology. 209, 165–181. marine fauna of Spitzbergen. I. Preliminary note and Bonnet L. 1958. Les thécamoebiens des Bouill- reports on the Rhizopoda. Proc. Zool. Soc. London. ouses. Bulletin de la Société d’Histoire Naturelle de 45, 784–792. Toulouse. 93, 529–543. Schönborn W. 1966. Beitrag zur Ökologie und Bonnet L. 1965. Sur le peuplement thecamoebi- Systematik der Testaceen Spitzbergens. Limno- en de quelques sols du Spitzberg. Bulletin de la logica. 4, 463–470. Société d’Histoire Naturelle de Toulouse. 100, Sher A.V. 1997a. Environmental restructuring 281–293. at the Pleistocene/Holocene boundary in the Bonnet L. 1975. Lamtoquadrula gen. nov. et East Siberian Arctic and its role in mammalian la structure plagiostome chez les Thécamoebiens extinction and establishment of modern ecosystems nébéliformes. Bulletin de la Société d’Histoire (Communication 1). Kriosfera Zemli. 1, 21–29 (in Naturelle de Toulouse. 110, 297–299. Russian). Booth R.K. 2010. Testing the climate sensitivity Sher A.V. 1997b. Environmental restructuring of peat-based paleoclimate reconstructions in mid- at the Pleistocene/Holocene boundary in the continental North America. Quaternary Sci. Rev. East Siberian Arctic and its role in mammalian 29, 720–731. extinction and establishment of modern ecosystems Charman D.J., Blundel A. and Members A. (Communication 2). Kriosfera Zemli. 1, 3–11 (in 2007. A new European testate amoebae transfer Russian). function for palaeohydrological reconstruction on Smith H.G. 1987. A species-poor testate ombrotrophic peatlands. J. Quaternary Sci. 22, 3, rhizopod fauna on Brabant Island. British Antarctic 209–221. Survey Bulletin. 77, 173–176. Charman D.J., Barber K.E., Blaauw M., Smith H.G. 1993. Influence of temperature Langdon P.G., Mauquoy D., Daley T.J., Hughes on test morphology of natural populations of 58 · A.A. Bobrov and S. Wetterich rhizopods in the maritime Antarctic. Abstr. IX Tsyganov A.N., Nijs I. and Beyens L. 2011. Intern. Congress of Protozoology, Berlin, p. 120. Does climate warming stimulate or inhibit soil Sullivan M.E. and Booth R.K. 2011. The protist communities? A test on testate amoebae potential influence of short-term environmental in high-arctic tundra with free-air temperature variability on the composition of testate increase. Protist. 162, 2, 237–248. communities in Sphagnum peatlands. Microbial Tsyganov A.N., R., Nijs I, Cornelissen J.H.C. Ecology. 62, 80–93. and Beyens L. 2012. Sphagnum-dwelling testate Tolonen K. 1986. Rhizopod analysis. In: amoebae in subarctic bogs are more sensitive in the Berglund B.E. (Ed). Handbook of Holocene growing season than in winter: the results of eight- palaeoecology and palaeohydrology. John Wiley, year field climate manipulations. Protist. 163, 3, Chichester, pp. 645–666. 400–414. Trappeniers K., Kerckvoorde A., Chardez D., Yurtsev B.A. 1966. Gipoarkticheskiy botaniko- Nijls I. and Beyens L. 2002. Testacea amoebae geografichesky poyas i proiskhozhdenie ego flory assemblages from soils in the Zackenberg area, (Hypoarctic botanical-geographical belt and origin northeast Greenland. Arctic, Antarctic and Alpine of its flora). Nauka, Moscow-Leningrad, 96 pp. (in Research. 34, 94–101. Russian).

Address for correspondence: A.A. Bobrov. Soil Department of Moscow State University, Vorobievy Gory, 119991, Moscow, Russia, e-mail: [email protected]