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Protistology 7 (2), 71-78 (2012)
Protistology
Distribution of soil testate amoeba assemblages along catenas in the northern taiga zone (Karelia, Russia)
Andrey N. Tsyganov, Elena A. Embulaeva and Yuri Mazei
Department of Zoology and Ecology, Penza State Pedagogical University, Penza, Russia
Summary
Topography is one of the main factors, which regulate composition and functioning of terrestrial ecosystems. However, the relationships between topography and soil protozoa remain poorly understood. We studied the distribution of testate amoeba assemblages in soil biotopes located at various topographic positions along two topographical gradients (catenas) in a forest site in the north taiga zone (Karelia, Russia). The variation in testate amoeba assemblages was estimated using univariate assemblage characteristics (the abundance and species number) and the species composition. The results of our study show that the species number increased from the upper to the lower catenary positions. This indicates the more favourable environmental conditions for testate amoebae in wet and nutrient rich low-lying accumulative positions. The species composition of testate amoeba assemblages changed along the catenas depending on the position of biotopes. The effects of topography on the species compositions decrease at the lower positions so that assemblages there have more similar composition. Our results show the important role of topography in regulation of spatial patterns of soil protozoa and demonstrate that other environmental variables can modify effects of topography.
Key words: catena, north taiga, soil, testate amoebae, topography
Introduction
Understanding how topography influences the distribution and the characteristics of soil protozoan communities at the landscape level is important for a better management of terrestrial ecosystems and preservation of biodiversity. Soil protozoa represent a common and diverse component ofsoil ecosystems (Foissner, 1987). They play an important role in soil decomposer food webs as secondary and higher level consumers. By grazing on bacteria, they increase
bacterial turnover rates and thereby the release of nutrients immobilised in bacterial tissue (Bardgett and Griffith, 1997; Couteaux and Darbyshire, 1998; Bonkowski, 2004). These feeding activities result in a greater availability of nutrients for plant uptake. Soil protozoa are very sensitive to soil properties such as moisture, particle size composition, concentrations of organic matter, nutrients, etc. (Foissner, 1987). At the landscape level, all these soil properties are strongly regulated by topography which is one of the main soil-forming factors (Bockheim et al., 2005).
© 2012 The Author(s)
Protistology © 2012 Protozoological Society Affiliated with RAS
Therefore, topography can be an important factor of the spatial distribution of soil protozoa at the landscape level as well. However, the relationships between topography and community characteristics of soil protozoa remain poorly understood.
One of the most interesting groups of soil protozoa for ecological studies is testate amoebae. Testate amoebae are free-living protozoa which are characterised by the presence of an external shell, sometimes referred to as a test. Empty shells of testate amoebae remain intact after organism death so that testate amoebae can be identified to the species level and enumerated in samples by ‘direct’ microscope counting (Foissner, 1987). This helps to avoid the difficulties associated with labourintensive cultivation techniques which are necessary for studies ofmany other groups ofprotozoa. Testate amoebae constitute a considerable part of soil biota in terms of biomass and biodiversity (Schonborn, 1992; Finlay, 2002; Schroter et al., 2003; Esteban et al., 2006). They prey on a wide range of organisms, including bacteria, protozoa, microalgae, fungi and micrometazoa (Gilbert et al., 2000; Wilkinson and Mitchell, 2010). Testate amoebae are very sensitive to variation in substrate moisture (Lousier, 1974a, 1974b; Mazei and Tsyganov, 2007; Sullivan and Booth, 2011), temperature (Tsyganov et al., 2011, 2012), vegetation (Ledeganck et al., 2003; Sutton and Wilkinson, 2007), etc. Thus, testate amoebae can be used as model organisms for ecological studies on protozoa.
Numerous studies on soil and ecosystem patterns at the landscape level has shown that catena concept is a useful tool for understanding the role of topography in regulation of those patterns (Klink, 2002 and references therein). The concept of catena was first developed in soil science by Milne (1935) who defined it as a sequence of soils developed from similar parent material under similar climatic conditions but whose characteristics differ because of variations in topography (i.e. relief) or, more specifically, slope and drainage conditions. Subsequently, the soil concept was applied for ecological studies so that “soil sequence” could be replaced by “biotope sequence”. Normally, the upper limit of catenas is defined by eluvial soils, which receive mainly atmospheric precipitation and are subjected to material removal due to downward water flows. The lower catena limits represent alluvial sites which accumulate water and materials and can be influenced by ground waters. The ecological catena concept can help to study the relationships between topography and soil protozoa while keeping the influence ofthe other factors, such as climate and parent material, constant.
So far, the distribution of soil testate amoebae along catenas has been studied by Bobrov (1999) and Rakhleeva (2000). These studies have shown that testate amoeba assemblages are characterised by well-defined patterns in biotope sequences along catenas. It has been also shown that the variation in testate amoeba assemblages depends on catena type. The aim of this work is to study the distribution of soil testate amoeba assemblages in the most typical regional ecosystem types located at various topographic positions along catenas in the north taiga zone (Karelia, Russia). This work focuses on the univariate assemblage characteristics and the species composition oftestate amoeba assemblages. We expected to observe (1) the increasing species number from eluvial to alluvial positions along catenas; (2) and changes in species composition of testate amoeba assemblages.
Material and methods
Study site
The study was performed in a taiga area (the Black River village; 66°31’17’’N, 32°58’07’’E) located on the shore of the Kandalaksha Gulf, the White Sea (Karelia, Russia). Typical catenas in the area are characterized by pine (Pirns sylvestris) forest on elevated parts, by spruce (Picea obovata) and birch (Betula pendula) forests in transitional zones and by flood-meadows (dominated by Carex spp.) in alluvial (accumulative) parts. For this study, we selected two catenas which had slightly different accumulative parts. The first catena had a flood meadow located in the floodplain of a small river (the Black River). The second catena had a flood meadow which turned into a salt marsh located in the Graysnaya Bay (the Gryasnaya Guba).
Sampling strategy
Soil samples for testate amoeba analysis were collected on the 17 of June, 2007. At each catenary position, we dug three holes (1x1 m square) to reveal the profile of the upper soil layers. The holes were located in different micro-biotopes (i.e. litter, Pleurozium schreberi moss and Cladonia spp. lichen in the pine forests; litter, mosses Hylocomnium splendens and Sphagnum spp. in the spruce forests; litter and Sphagnum spp. moss in birch forests; litter in the meadows) in order to cover the natural heterogeneity of the sites. Then we sampled the litter (or moss/lichen) layer (A0) and the upper 2 cm of the underlying layer (A:) from a side of the
holes. Samples of 5x5 cm were cut out with a soil knife and were kept in sealed plastic bags until the analysis. This sampling strategy resulted in a total of 24 samples.
T ESTATE AMOEBA ANALYSIS
The samples were prepared for counting testate amoebae following a modified version ofwater based sieving procedure (Hendon and Charman, 1997). Five grams of the substrate from each sample were mixed with arbitrary amount of water and were left soaking for 24 hours. After that, the mixture was thoroughly shaken for 10 min for extraction of testate amoebae from soil particles. The suspension was passed through sieves with mesh openings of 0.5 — 1 mm in order to remove big particles which can cover testate amoebae during counting. The sieving residue was gently washed with water. The mixture was left for sedimentation for 24 hours. After that, the supernatant was carefully poured off. The sedimentation was repeated once again so that the volume of the concentrate was 10 ml. Two millilitres of the concentrate were placed in a Petri dish and were diluted with arbitrary amount of water in order to obtain concentrations and volume suitable for microscopy. The suspension was left to settle down for several minutes. Then, testate amoebae were identified and counted by direct counting at a magnification of x160 using a dissection light microscope Olympus CX41RF (Olympus Corporation, Japan). Two subsamples were analysed. A minimum total of 150 shells were counted in each sample. The obtained counts were calculated to 1 g of absolutely dry substrate weight.
Data analysis
Changes in testate amoeba assemblages were estimated using univariate assemblage characteristics and the species composition. The following assemblage characteristics were calculated: (1) the total abundance of testate amoebae (ind. g—1 absolutely dry substrate weight); (2) the total species number per biotope. The variation in the species composition was analysed using the species abundance matrix. The matrix was subjected to Principal Component Analysis (PCA) which is a useful tool for visualisation and description of changes in species composition. In order to eliminate unwarranted effects of rare species on the results of the multivariate analysis we removed species, which were encountered in only one sample before the analysis. The final data set for the multivariate analysis contained 29 taxa (see Table 1). After
that, the species data were Hellinger-transformed (function ‘decostand’ in the package ‘vegan’, Oksanen et al., 2012). The Hellinger transformation helps to avoid problems arising from Euclidian distance when the distance between two site sharing no species in common can be smaller than between two sites sharing common species (Legendre and Gallagher, 2001). The numerical calculations and statistical analyses were performed in the R language environment (R Core Team, 2012).
Results
General observations
The analysis of the samples revealed 42 testate amoeba taxa belonging to 16 genera (Table 1). Living individuals were observed for 13 taxa only. The testate amoeba assemblage was dominated by six taxa: Nebela collaris (20.1%), Euglypha rotunda (12.4%), Trinema complanatum (7.4%), Trigonopyxis arcula (6.1%), Nebela militaris (6.1%), and Centropyxisaerophilav. sphagnicola (5.3%). All these species were also characterised by relatively high occurrence (> 30% of all samples, see Table 1) and therefore constituted the core of the testate amoeba assemblages at the site. The assemblages were also characterised by a considerable number of testate amoeba taxa (20 taxa) with low occurrence (they were encountered in less than 10% of the samples).
Univariate assemblage characteristics
The patterns of the total species number per biotope differed between the catenas. The first catena was characterised by the gradually increasing total species number per biotope from the pine forest to the meadow, i.e. from the eluvial position to the accumulation zone (Fig. 1, A). In the second catena, the total species number per biotope increased from pine forest till birch forest (from 15 to 31 taxa) and then drastically dropped down to 11 taxa in the meadow (Fig. 1, A). The variation in the abundance of testate amoebae was similar to the patterns in the total species number per biotope along the second catena but had no clear patterns along the first catena (Fig. 1, B).
Assemblage composition of testate amoebae
The results of the PCA indicate that the species composition of the testate amoeba assemblages
Table 1. Occurrence and mean abundances (ind. g-1 substrate weight) of testate amoebae in two catenas in the northern taiga zone (Karelia, Russia). The taxa are sorted in the descending order of their occurrence. The occurrence was calculated as the percentage of the number of samples in which the taxon was encountered. Species abundances which are greater than 5% of the mean total abundance in a biotope are shown in bold. Empty cells denote null concentrations. Species codes used in the figures are also indicated. Species marked with an
asterisk were excluded from the multivariate analysis.
Species names Codes Catena 1 (freshwater flood-meadow) Catena 2 (salt marsh)
Pine forest Spruce forest Birch forest Flood- meadow Pine forest Spruce forest Birch forest Flood- meadow
Common species (occurrence >50%)
Euglypha rotunda Eug.rot 36.5 21.4 125.0 114.8 14.4 627.7 520.0 125.1
Trinema complanatum Trn.com 107.2 14.6 151.3 96.7 29.1 37.9 425.7 75.7
Nebela collaris Neb.col 215.2 38.8 262.2 722.7 139.2 456.8 521.9 204.5
Centropyxis aerophila Cen.aer 38.9 78.9 63.3 87.1 22.0 14.8 92.3 7.2
Centropyxis aerophila v. sphagnicola Cen.aes 7.9 36.2 69.1 12.4 211.0 149.2 184.0
Cyclopixis kahli Cyc.kah 57.9 40.5 42.7 34.5 12.6 25.3 7.1
Common species (oc currence 10-50%)
Phryganela acropodia Phr.acr 140.5 32.6 41.6 95.1 7.1 35.3 81.8
Trigonopixis arcula Tri.acr 101.9 387.6 31.8 232.4 25.4
Euglypha laevis Eug.lae 166.7 25.8 34.0 72.9 206.4
Nebela militaris Neb.mil 7.9 198.2 215.4 192.3 161.7
Centropyxis sylvatica Cen.syl 210.7 102.3 32.2 17.0 5.3 7.1
Plagiopixis declivis Pla.dec 10.4 43.9 25.8 106.3 98.6
Tracheleuglypha dentata Tra.den 51.7 36.1 96.0 49.8
Arcella intermedia Arc.int 10.4 8.5 353.9
Corythion dubium v. terricola Cor.dut 87.7 35.6 21.6 7.1
Arcella catinus Arc.cat 142.1 31.4 440.5 44.4
Arcella arenaria Arc.are 258.4 55.9 18.3
Cyclopyxis eurystoma Cycl.eur 166.1 7.3
Euglypha ciliata Eug.cil 10.5 92.5 20.4
Assulina muscorum Ass.mus 62.3 18.1 28.8
Arcella vulgaris Arc.vul 7.9 43.9 17.0 31.7
Heleophera sylvatica Hel.syl 10.4 18.1 73.3
Rare species (occurrence <10%)
Trinema lineare Trn.lin 54.2 56.4
Corythion dubium v. orbicularis Cor.duo 14.8 85.5
Padaungiella wailesi Pad.wai 51.7 7.1
Centropyxis platystoma Cen.plt 36.6 20.4
Cyclopyxis arcelloides Cyc.arc 20.8 35.3
Trinema enchelys Trn.ech 35.3 20.4
Centropyxis plagiostoma Cen.pla 8.5 7.1
Arcella artocrea v. pseudocatinus* Arc.arp 34.3
Argynnia (Nebela) dentistoma* Arg.den 14.4
Difflugia oblonga* Dif.obl 108.2
Euglypha rotunda v. obliqua* Eug.roo 61.3
Euglypha ciliata f. glabra* Eug.cig 42.7
Table 1. (Continuation).
Species names Codes Catena 1 (freshwater flood-meadow) Catena 2 (salt marsh)
Pine Spruce Birch Flood- Pine Spruce Birch Flood-
forest forest forest meadow forest forest forest meadow
Centropyxis elongata* Cen.elo 21.4
Euglypha inaquelis* Eug.ina 21.4
Centropyxis aculeata* Cen.acu 18.3
Nebela tincta* Neb.tin 18.3
Arcella dentata v. trapezica* Arc.det 12.6
Euglypha denticulata* Eug.den 12.6
Nebela parvula* Neb.par 7.1
varied in the biotopes along the catenas and that this variation was catena-specific (Fig 2, A). The fist principal component explained 35.4% of the total variation in the species composition. This component was associated with changes in the species composition in the biotopes along the catenas (Fig 2, A). In both catenas, the eluvial parts (pine forest and spruce forest) were characterised by different species composition of testate amoeba assemblages whereas the alluvial parts (birch forest and meadow) had similar species composition (Fig 2, A). Therefore, three types of testate amoeba assemblages can be distinguished along the catenas. The second principal component explained 23.4% of the total variation in the species composition of the testate amoeba assemblages. The component was related to the differences between the catenas showing that the changes in the species composition in the biotopes were specific for each catena.
The species composition of testate amoebae in the pine forest on the first catena was characterised by species with wide ecological preferences Centropyxis sylvatica, Euglypha laevis and Phryganella acropodia. The spruce biotope located below on the catena had a specific species composition and was dominated by moss-dwelling species Trigonopyxis arcula, Arcella arenaria and Arcella catinus. The typical species in the birch and meadow biotopes on the first catena were Nebela collaris, Trinema complanatum, Plagiopyxis declivis. The pine biotopes on the second catena were dominated by Arcella catinus which was replaced by Arcella intermedia and Nebela militaris in the spruce biotopes. The birch and meadow biotopes on the second catena were characterised by Centropyxis aerophila v. sphagnicola, Euglypha rotunda and Nebela collaris.
Fig. 1. Univariate characteristics (A — total abundance, B — the total species number) of soil testate amoeba assemblages in pine forest, spruce forest, birch forest and meadow biotopes located along two catenas in the north taiga zone.
cm
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o
d
LO
d
A
op1
: om1
os1 • ob1
L *.b2
*s2 .m2
• p2 |
i 1.0 I I I -0.5 0.0 0.5 i 1.0
PC1 (35.4%)
CM
d
o
d
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d
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o
B Cen.syl •
Tri.acr Plidec Eu°lae Cyc.kah ! Phracr , Cen,aer Arc.vul ! t- Trn.com a 'Of L Hel.syl Ass.mus.Pad.wai Tr„ ,■ Neb col Arc. are • Cyc.arcTrnlin C£n.Qia Tra.den
•Cor.duoEug.cil ; Trn.ech Cor. dut ; Arc. int Cen Ptt Eug.rot Cen.aes
Arc. cat ; Neb.mil
I -0.3 I I I I -0.2 -0.1 0.0 0.1 PC1 (35.4%) I 0.2
Fig. 2. Ordination diagrams illustrating the results of the analysis of principal components (PCA). A — Distance biplot of site scores (scaling 1). White circles represent the first catena; the black circles represent the second catena. The lowercase letters in the diagram indicate the investigated biotopes (p — pine forest, s — spruce forest, b — birch forest, m — meadow). B — Correlation biplot of species scores (scaling 2). The ordination was performed on the correlation matrix ofthe Hellinger-transformed abundances ofthe testate amoeba species which were encountered in more than one sample (see Table 1 for the species codes). The number in the parentheses is the proportion of the variation explained by each principal component.
Discussion
General observations
The testate amoeba assemblage at the site was characterised by relatively high taxonomic diversity and a considerable proportion of taxa with low occurrence. The assemblage was dominated by soil, moss-dwelling and ubiquitous species. The considerable proportion of moss-dwelling (Nebela collaris, Nebela militaris, Trygonopyxis arculla, etc.) species can be explained by the presence of reach moss vegetation in the biotopes on the studied catenas. The observed species were previously reported to be typical for soil and bog ecosystems in the studied region (Bobrov, 1999; Mazei and Bubnova, 2009; Mazei et al., 2009a, 2009b, 2010). Overall, the taxonomic composition of the testate amoeba assemblages at the site was typical for soil biotopes in the northern taiga zone suggesting that our findings can have bearing for other ecosystems beyond the studied location.
Univariate assemblage characteristics
The results show that the total species number of soil testate amoebae increases from eluvial to alluvial
positions on catenas, however the patterns can be affected by local environmental conditions such as the negative influence of sea water. Previous studies demonstrated various types ofthe distribution ofthe species number along catenas (Rakhleeva, 1998, 2000; Bobrov, 1999). These patterns can be linear (either increasing or decreasing downwards), bell-or U-shaped. The downward increase in the species number which was observed in the present study can be explained by accumulation ofwater and nutrients which can sustain more diverse testate amoeba assemblages (Mitchell et al., 2000; Finlay and Fenchel, 2001). However, it is difficult to explain the absence of any edge effects at the transitional positions because ecotone communities of soil protozoa remain poorly understood. Therefore, the distribution of the species number of soil protozoa along catenas is a result of complex interaction of topography, local environmental conditions and edge effects.
Assemblage composition of testate amoebae
The results of our study indicate that the species composition oftestate amoeba assemblages varies in the biotopes along the catenas and that this variation is catena-specific. The changes in the species composition were mostly related to the variation in
the proportions of moss- and Sphagnum-dwelling species which were replaced by soil species in some biotopes. However, it is difficult to distinguish any general trends in terms of species responses which could be directly linked to variation in environmental variables along catenas. Previous studies also reported that species composition of soil testate amoeba assemblages was related to topographical positions along catenas (Rakhleeva, 1998, 2000; Bobrov, 1999). The variation in the species composition was explained by changes in water regime and soil characteristics. In most cases, three types of testate amoebae assemblages which correspond to eluvial, transitional and alluvial catenary positions could be distinguished. Our results also demonstrate that the above mentioned positions on the studied catenas were characterised by specific species compositions of testate amoeba assemblages. Moreover, the accumulative positions and the transitional position right next to it were characterised by similar species composition that could be explained by influence offloods and ground waters.
Conclusions
Overall, our results demonstrate the total species number and the species composition of soil testate amoeba assemblages vary along catenas located in the northern taiga zone. The total species number decreases from the upper to the lower catenary positions as a result of more favourable environmental conditions for testate amoeba in wet and nutrient rich low-lying accumulative sites. However, topography-independent variation in environmental conditions, for example sea water influence, can considerably affect the patterns. Topographical position also influences species composition of testate amoeba assemblages and the effects of topography decrease at the lower positions so that assemblages there have more similar composition. our results support the hypothesis about the important role oftopography in regulation of spatial patterns of soil protozoa and show that other environmental variables can modify effects of topography.
Acknowledgements
We are thankful to igor v. Burkovsky for the assistance and accommodation during the field campaign. This work was supported by the Russian Foundation for Basic Research (grant 10-04-00496-a) and grant of the President of Russian Federation (grant MD-4426.2012.4).
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Address for correspondence: Andrey N. Tsyganov. Department of Zoology and Ecology, Penza State Pedagogical University, Lermontov str. 37, 440026, Penza, Russia; e-mail: andrey.tsyganov@bk.ru
