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Protistology 7 (1), 51-58 (2012)
Protistology
Testate amoebae of arctic tundra landscapes
A. A. Bobrov1 and S. Wetterich2
1 Soil Department of Moscow State University, Moscow, Russia
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 Euglypha. Almost all species belong to the cosmopolitan group oftestate amoebae. Only Centropyxisgasparella, 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
Testate amoebae are a group of free-living protozoans having an external shell (testa). Some taxa from this group are covered with exogenous mineral material (xenosomes), plant detritus, or endogenous material (idiosomes), such as silica or, rarely, calcium phosphate plates. Their well-defined ecological preferences and the relatively good preservation offossil shells in peats, lake sediments, and buried soils form the basis for the development of rhizopod analysis as a method for reconstruction of climate and environmental changes (Meisterfeld, 1977; Tolonen, 1986; Charman et al., 2007, 2009, 2010; Booth, 2010; Tsyganov et al., 2011, 2012; Sullivan and Booth, 2011).
Testate amoebae, being inherently aquatic, respond to environmental changes in ground water
table, moisture, pH, content of biophilic elements (C, N, P, K, Ca, Mg) by restructuring their communities. Testate amoebae can be classified into ecological groups according to their requirements concerning moisture (hygrophiles, hydrophiles, xerophiles), pH (acidophiles, calciophiles), habitat preferences (sphagnophiles, soil-inhabiting, aquatic). Their density in lake sediments, peat and soils can vary from a few hundred to tens of thousands of shells per cm3. The number of taxa in oligotrophic bogs can reach several tens of species and infraspecific forms. The significance ofrhizopod analysis for paleoecological studies is based on the fact that testate amoebae are permanently affixed to the substrate. Their shells are normally destroyed if the sediments are redeposited. Therefore, they are often the only organisms that can directly indicate the paleoenvironmental conditions during sediment
© 2012 The Author(s)
Protistology © 2012 Protozoological Society Affiliated with RAS
formation, unlike many other biological remains.
The study of modern rhizopods in the Arctic was initiated in the late 19th and early 20th centuries (Scourfield, 1897; Penard, 1903; Sandon, 1924) and was continued after a long interval. Moss and lichen pads, soils, and small pools were studied in eastern and western Greenland, northwestern Spitsbergen, Brabant Island, and some other Arctic areas (Bonnet, 1965; Schonborn, 1966; Beyens and chardez, 1986; Beyens et al., 1986a, 1986b; 1991, 1992, 2000; Smith, 1987; Opravilova, 1989; Balik, 1994). In a recent study on the rhizopod fauna of northeast Greenland (Trappeniers et al., 2002) special attention was paid to an evaluation of quantitative relationships between the composition of testate amoebae soil assemblages and ecological parameters (pH, organic matter, moisture) of their habitats and communities.
Modern testate amoebae of the Russian Arctic are almost not described. Only three publications during the last 110 years were devoted to this region. Rhizopods collected near Murmansk and Vaygach Island in Russian Arctic were studied by Awerinzev and Levander (Beyens et al., 2000). The rhizopods are not numerous in the moss and aquatic biotopes of the coastal areas of the Barents and Kara Seas, only 45 species, varieties and forms have been found there (Beyens et al., 2000).
Since many years, the East Siberian Arctic attracted paleoecologists who studied late Quaternary and modern environment (Yurtsev, 1981; Sher, 1987a, 1987b). However, data about soil-inhabiting protozoa are still lacking except of one publication where testate amoebae findings of ground surface samples from Bykovsky Peninsula (Central Laptev Sea) are mentioned (Bobrov et al., 2004).
Earlier studies showed that (1) the density and biodiversity of testate amoebae in the modern high-latitude Arctic decrease with the decrease in average summer temperatures, i.e. with harsher climate conditions, and (2) some species respond to lower temperatures by reducing the size of their shells (Smith, 1988).
The aim of this study is to conduct a detailed analysis of modern testate amoebae from the East Siberian Arctic and Alaska, their geographical distribution and ecological specifics.
Material and methods
Modern testate amoebae communities have been studied from a total of 274 soil, lake sediment and peat surface samples mainly from the Central
and East Siberian Arctic, but also from Alaska (Fig. 1, Table 1): Severnaya Zemlya Archipelago (1, 2), Taymyr Peninsula (3), Western Laptev Sea (4), Lena Delta (5, 6. 7, 8), Central Laptev Sea region (9), New Siberian Archipelago (10, 11), Indigirka lowland (12) and Seward Peninsula, Alaska (13).
The overall modern climate conditions are harsh and characterized by long (>8 month), severe winters and short cold summers with mean July temperatures of about or below 9 °C, mean January temperatures of about or above -34 °C, and annual precipitation from about 80 to 300 mm (Atlas Arktiki, 1985).
Soils in the area are mainly tundra-gley and peaty-gley (histosols and inceptisols) with an active-layer thickness ofabout 30 to 40 cm. The area belongs to the zone of northern tundra. Mosses, grasses and low shrubs dominate the vegetation, with typical vascular plant species such as Betula exilis, Dryas punctata, Salix pulchra, Cassiope tetragona, Oxyria digyna, Alopecurus alpinus, Poa arctica, Carex
ensifolia, C. rotundifolia, Eriophorum medium,........
Aulacomnium turgidum, Hylocomium alaskanum, Drepanocladus iniciatus, Calliergon sarmentosum, and lichens Alectoria ochroleuca, Cetraria cuculliata and C. hiascus (Atlas Arktiki, 1985).
Samples of soil and sediments were suspended in water and passed through 500 ^m mesh to remove large particles. Rhizopod shells were concentrated with a centrifuge. A drop of suspension was placed on the slide, and the glycerol was added. Normally,
5 subsamples from each sample were examined at 200-400* magnification with the light microscope. The PAST software was employed to analyze the data.
Results and discussion
In a total of 274 surface samples from different elements of arctic tundra landscapes, 215 species and subspecies have been identified. More than half of the taxa belong to hygro-hydrophilic and sphagnobiontic species of the genera Difflugia, Centropyxis, Arcella, Euglypha (Fig. 2). Most of the identified species belong to the cosmopolitan group, including sphagnobionts, hygro-hydrophiles, soil-inhabiting and eurybiontic species (Fig. 3). The ecological structure of the communities was similar on arctic islands and on the mainland, and dominated by hygro-hydrophilic species. Outcrops of carbonate rocks ensure a broad presence of calciphiles, mainly represented by Centropyxis plagiostoma (sensu lato) which prefers neutral to slightly acidic pH.
150°W 180° 150°E
120°E 135°E 150°E
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 Centropyxis aerophila, C. constricta v. minuta, C. sylvatica, Cyclopyxis eurystoma v. parvula, Schoenbornia humicola, Euglypha laevis and Trinema lineare.
Testate amoebae species with restricted geographical distribution are of special interest: Centropyxis gasparella, C. gasparella v. corniculata,
C. pontigulasiformis, C. vandeli, Difflugia kabulica,
D. ovalisima, D. serpentrionalis, D. szczepanskii, Lesquereusia sphaeroides, Lamptoquadrulla sp., Placocista lapponum, Difflugiella (Cryptodifflugia) angusta, D. bassini, D. minuta, D. pusilla, D. sacculus, D. sacculus v. sakotschawi, D. vanhoornei, Pseudodifflugia jungi. Some of these species are only found in arctic tundra: Centropyxis gasparella, C. gasparella v. corniculata, C. pontigulasiformis, Difflugiella vanhoornei, Difflugia ovalisima. The hygrophilic species Centropyxis gasparella sensu lato was so far reported from tundra environments in the Canadian Arctic, in Alaska and in Northeast
Greenland (Beyens and Chardez, 1995, 1997; Trappeniers et al., 1999). Centropyxis pontigulasiformis has a broader tolerance and distribution. It occurs under water and on mosses on Svalbard, on Devon and Victoria islands (Canadian Arctic), and West Greenland (Beyens and Chardez, 1995). Difflugia ovalisima was described from moss samples of Devon Island (Beyens and Chardez, 1994), and Placocista lapponum occurs on Greenland and Northern Sweden (Penard, 1917).
Some species also occur within the taiga zone as for instance Difflugiella (Cryptodifflugia) bassini (Bobrov, 2001). The species Centropyxis vandeli was described from mountain soils in southern France (Bonnet, 1958) and found in hydrophilic soil mosses in the Western Rhodopes, Bulgaria (Golemansky et al., 2006). The finding of Lamptoquadrula sp. is of special interest because the type species of the genus (which includes so far only one species) was described from soils in gallery forests in Cote-d’Ivore (Bonnet, 1975). Further evidence for rare species
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 19S0, 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-australian species Nebela martiali which has also been found in surface samples from Dikson Island, Eklips, and Franz Joseph’s Land (Beyens et al., 2000).
An important indicator of species diversity is the relationship between the number of species and the number of sites examined (Fig. 4). The rarefaction curve demonstrates a high heterogeneity of the data set and suggests that for a more complete representation of species diversity much more than 13 sampling sites are required. Therefore, the 215
species and subspecies found in this study do not reflect the total diversity ofrhizopods in arctic tundra landscapes.
The ordination of testate amoebae assemblages from different areas of the arctic tundra illustrates that most rhizopod communities were rather similar. However, pronounced differences were found e.g. between assemblages from moss-lichen tundra of October Island (site No. 1 in Fig. 1) and moss-shrub polygonal tundra of the Berelekh River (site No. 12 in Fig. 1). The latter had a more structured micro-relief which led to small-scale differences
| Difflugia 1
Centropyxis
Arcella
WIFIrlha Difflugiella Nebela Trinema Heleoptera Cyclopyxis Plagioplyxis Corythion Placocista Lesquereusia Argynnia Assulina Hyalosphenia Paraquadrulla Phryganella Pseudodifflugia Bullinularia Lagenodifflugia Schoenbornia Tracheleuglypha Valkanovia Archerella Netzelia Pontigluasia Quadrulella Trigonopyxis Wailesella pr
11111111111111111111111111111111111111111
0 10 20 30 40
Number of species
Fig. 2. Distribution of arctic testate amoebae species per genus.
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 and dynamics under climate variability in polar regions’ (RFBR grant N 11-04-91332-NNI0-a,
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 the North-Eastern Federal University, Yakutsk (L. Pestryakova), Hamburg University (F. Beermann), Moscow State University (L. Kokhanova, V. Tumskoy, E. Zhukova), Herzen State Pedagogical University, St. Petersburg (V. Sitalo), and AWI Potsdam (L. Schirrmeister, A. Schneider) who conducted the fieldwork in the Berelekh River area in 2011 are greatly acknowledged. Long-term support was provided by the German-Russian Scientific Cooperation Programs ‘Laptev Sea 2000'' and ‘System Laptev Sea’ which provided the frame for joint Russian-German expeditions since 1998 when most of the Siberian samples have been obtained. Financial support came also from the RFBR project N 11-04-01171-a ‘Geography and ecology of soil inhabiting testate amoebae’’. The fieldwork at the Alaskan study site on Seward Peninsula was organized by G. Grosse (University of Alaska Fairbanks) and financially supported by the National Science Foundation (NSF grant N 0732735) and the DFG (DFG grants N SCHI 530/7-1, WE 4390/2-1 and KI 849/2-1). Additional support was provided from NASA Carbon Cycle Sciences (grant NNX08AJ37G).
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Address for correspondence: A.A. Bobrov. Soil Department of Moscow State University, Vorobievy Gory, 119991, Moscow, Russia, e-mail: [email protected]
