CC BY
30
Protistology 11 (1), 3-19 (2017) Protistology
Centrohelids in the mires of Northern Russia
Kristina I. Prokina1, Dmitriy G. Zagumyonnyi2 and Dmitriy A. Philippov1
1 Papanin Institute for Biology ofInland Waters, Russian Academy of Sciences, Borok, Russia
2 Voronezh State University, Voronezh, Russia
| Submitted May 8, 2017 | Accepted June 13, 2017 |
Summary
The species composition and morphology of centrohelid heliozoa collected from mire water bodies of different types in the North of the European part of Russia were studied. Eighteen species from five genera and four families, two species with an uncertain systematic position and some unidentified Heterophrys-like organisms were found (Arkhangelsk Region — 9 species, Republic of Karelia — 7, Vologda Region — 9). Three species (Pterocystis paliformis, P. striata, P. tropica) are new for Russia. Nine species are new for Arkhangelsk Region (Acanthocystis penardi, A. trifurca, A. turfacea, Choanocystis symna, P. pinnata, P. tropica, Raineriophrys echinata, R. kilianii). Eight species are new to the centrohelid diversity of the Vologda Region (Acanthocystis lyra, A. aff. takahashii, A. trifurca, Polyplacocystis symmetrica, Pterocystis pinnata, P. tropica, Raphidiophrys intermedia). Four species are new for the Republic of Karelia (Pterocystis paliformis, P. striata, P. tropica, Raphidiophrys minuta). The species composition ofthe mires of the Arkhangelsk Region and the Vologda Region has much more in common in comparison with the centrohelid diversity of the Republic of Karelia. The most favourable conditions for the presence of high centrohelid species diversity occurred in the minerotrophic mires (15 species, incl. 5 — in mire streams, 7 — in space between hummocks, 9 — in flarks of the aapa mires), in comparison with the water bodies of ombrotrophic mires (4 species, incl. 2 — in laggs and 2 — in hollows of the raised bogs).
Key words: centrohelids, species diversity, mires, mire water bodies, morphology, species composition
Introduction
Centroplasthelida Febvre-Chevalier et Febvre, 1984, a monophyletic group of the predatory amoeboid organisms (Durrschmidt and Patterson, 1987; Cavalier-Smith and von der Heyden, 2007), was one of the last substantially diverse groups of eukaryotes with an uncertain systematic position until recent years. Centrohelids are sister clade
of haptophytes and together they form Haptista, related to SAR (Stramenopiles, Alveolates, Rhiza-ria) (Burki et al., 2016). The cells of centrohelids are covered with siliceous scales having variable shapes and dimensions or more or less uniform organic spicules. The structure of siliceous components of external envelope is very important for the species identification, which usually requires electron microscopy (Nicholls, 1983; Siemensma, 1981;
doi:10.21685/1680-0826-2017-11-1-1 © 2017 The Author(s)
Protistology © 2017 Protozoological Society Affiliated with RAS
Wujek, 2003a). Centrohelid heliozoans are cosmopolitan free-living aquatic organisms, more frequently recorded in freshwater (possibly because of more intensive study in comparison to marine habitats). The information on diversity and ecology of this group of protists is very fragmentary and require a further study.
The high taxonomic diversity of centrohelids was observed in sphagnum bogs (Rainer, 1968; Siemensma, 1981). Information on their species diversity in paludified and Sphagnum habitats in Russia is very scarce and present in the few papers without mentioning the specific mires microbiotopes (Leonov, 2009, 2010, 2012; Leonov and Plotnikov, 2009; Leonov and Mylnikov, 2012). The centrohelid diversity in mires and paludified habitats in the Northern European part of Russia is almost unexplored.
The aim of the present study was to investigate the diversity of centrohelid heliozoans in the particular mire water bodies in the North of the European part of Russia, using scanning and transmission electron microscopy.
Material and methods
Field studies were carried out in June, August and September 2015 by D.A. Philippov on one lake and seven mires in the Arkhangelsk Region, Vologda Region and Republic of Karelia (Russia). Several types of mire water bodies (lake, stream, lagg, space between hummocks, flark, and hollow) were studied in each mire. Temperature (t), pH and conductivity (EC) of the water samples (Table 1) were measured using a Mettler-Toledo SevenGo Duo pH/conductivity SG23 meter.
Water samples were transferred to the laboratory in 15 ml plastic tubes in the darkness at the temperature 4° C. The organisms in water samples were cultured in Petri dishes for two weeks, and the heterotrophic flagellates Parabodo caudatus (Dujardin, 1841) Moreira, Lopes-Garcia et Vicker-man, 2004 were used as a feeding source. Preparations for studying of scales were carried out according to the described methodology (Moestrup and Thomsen, 1980; Mikrjukov, 2002), and observed in transmission (JEM-1011) and scanning (Joel JSM-6510 LV) electron microscopes. Centrohelids were identified according to following publications: Nicholls, 1983; Durrschmidt, 1985, 1987a, 1987b; Croome, 1896, 1987; Siemensma and Roijackers, 1988a; Mikrjukov and Croome, 1998; Mikrjukov,
2002; Leonov, 2009, 2012; Leonov and Plotnikov, 2009; Leonov and Mylnikov, 2012; Zlatogursky, 2014b; Kosolapova and Mylnikov, 2015; Plotnikov and Ermolenko, 2015; Gerasimova and Plotnikov, 2016.
Results
Eighteen species from six genera and four families were observed. The distribution of species in the water samples is presented in Table 2. The centrohelid taxonomy presented by V.V. Zlato-gursky (Zlatogursky, 2014a) is used.
Class Centroplasthelida Febvre-Chevalier et Febvre, 1984
Order Acanthocystida Cavalier-Smith, 2012 Family Acanthocystidae Claus, 1874 emend. Cavalier-Smith et von der Heyden, 2007 Genus Acanthocystis Carter, 1863
Acanthocystis lyra Gerasimova et Plotnikov, 2016 (Fig. 1, a-c).
There were 3 types of spine scales. The first type is 4.97-7.11 ^m in length, bifurcated on the lyre-shaped tip. There are 6 teeth on the inner side of each sharp branch. The length of the bifurcated tip covers 10.2-17.1% ofthe total scale length. The base of these spine scales is 0.71-0.89 ^m in diameter. The second type of scales is 3.03-3.46 ^m in length, with similar structure except for widely bifurcated tip (25.5-32.3% of the total length of the scale) and base 0.56-0.63 ^m in diameter. The third type of spine scales is 2.33-3.00 ^m in length, possesses remarkable primary and secondary bifurcations. The base of this type of spine scales is 0.65-0.82 ^m in diameter. The shafts of all type of spine scales are 0.15-0.18 ^m in diameter.
The scales of one cell were observed from sample 8 (Table 2).
The morphology and size of scales are in agreement with those described by E.A. Gerasimova and A.O. Plotnikov from South-East of the European part of Russia (Gerasimova and Plotnikov, 2016).
Acanthocystis pectinata Penard, 1889 emend. Nicholls, 1983 emend. Siemensma et Roijackers, 1988 (Fig. 1, g)
Spine scales of two types were present. The first type of spine scales is 6.8-9.5 ^m in length. The hollow cylindrical shaft is 0.29-0.33 ^m in
Table 1. Characteristics of the studied mire water bodies and sample collection sites.
Place, wetland Mire water bodies Sample collection site
Type of water bodies* Coordinates pH t°C EC (mkSm/sm) Sample # Microbiotopes Date
Arkhangelsk Region, Pinega District, mire Nizinnoe Sp N 64°33'21.5" E 43°19'14.9" 5.8 14 52.2 1 herbaceous habitat 07.08.2015
2 Bryales habitat
ibid., mire Tretje St N 64°33'17.6" E 43°20'19.5" 6.1 15 48.5 3 water column 07.08.2015
4 bottom detrital matter
ibid., mire Udebnoe Ho N 64°32'51.7" E 43°22'01.3 4.2 16 48.6 5 Carex rostrata-Sphagnum habitat, bottom detrital matter 09.08.2015
ibid., mire Velboloto Ho N 64°36'34.3" E 43°14'38.5" 4.2 18 31.8 6 Scheuchzeria-Hepaticae degraded habitat 11.08.2015
Vologda Region, Syamzha District, mire Shichengskoe Lg N 59°56'42.5" E 41°17'07.5" 5.5 24 - 7 Menyanthes- Scheuchzeria-Utricularia habitat 27.07.2015
St N 59°56'25.0" E 41°16'06.0" 6.6 15 - 8 bottom detrital matter
Vologda Region, Vytegra District, mire Piyavochnoe Fl N 60°46'57.5" E 36°50'34.7" 5.7 10 - 9 Carex lasiocarpa-Rhynchospora-Scorpidium habitat, bottom detrital matter 12.09.2015
Republic of Karelia, Loukhi District, near "Kartesh", mire Boloto#1 Fl N 66°21'17.5" E 33°34'07.4" 6.6 10 - 10 Carex livida-Menyanthes habitat, water column 20.06.2015
11
12 ibid., bottom detrital matter
ibid., mire Boloto#2 Fl N 66°20'26.3" E 33°32'40.2" 5.1 13 - 13 Menyanthes-Sphagnum habitat, bottom detrital matter 21.06.2015
ibid., lake Krugloe Lk N 66°20'29.3" E 33°36'07.2" 5.9 16 - 14 bottom detrital matter 23.06.2015
* Mire water bodies: Lk - lake, Sp - space between hummocks, St - stream, Lg - lagg, Fl - flarks (in minerotrophic mires), Ho - hollows (in ombrotrophic mires).
diameter, apex with 5—7 small marginal teeth. The funnel-shaped base is 0.8— 1.1 pm in diameter with the marginal rim on the inner side. Second type — short numerous spine scales, 2.3—3.6 pm in length. Bowl-shaped apex with 6—8 large and widely divergent teeth connected by a membrane. Size and shape of base and shaft of spine scales are the same as for the first type. Spine scales with intermediate size and shape were rarely found. Plate scales oval or pear-shaped, 2.2—3.3x1.6—2.0 pm. Indistinct radial ribs and small marginal rim on the one side of plate scales are present.
The dimensions and morphology of scales are in agreement with those given by other authors, except for the smaller plate scales described by K.H. Nicholls (1983) - 2.3x 1.4 pm, and F.J. Siemensma and M.M. Roijackers (1988a) — 1.6-2.5 pm. Some authors described the different length of spine scales: A.O. Plotnikov and E.A. Ermolenko described smaller spine scales of the short type — 1.6—2.7 pm (Plotnikov and Ermolenko, 2015); M.M. Leonov and A.O. Plotnikov (Leonov and Plotnikov, 2009; Leonov, 2012) observed larger spine scales of the long type
(up to 15 pm).
Scales of only a few cells from sample 14 (Table 2) were observed.
Previous reports of this species were from freshwaters of the European part of Russia (Mik-rjukov, 1993a; Leonov and Plotnikov, 2009; Leonov, 2010, 2012; Leonov and Mylnikov, 2012; Ermolenko and Plotnikov, 2013; Plotnikov and Ermolenko, 2015), Ukraine (Gaponova, 2009), Estonia (Mikrjukov, 1993b), Sweden, Netherlands (Siemensma, 1981; Siemensma and Roijackers, 1988a), Ethiopia (Prokina et al., 2017a), India (Wujek and Saha, 2006); USA (Wujek, 2003a, 2006), Canada (Nicholls, 1983), Australia (Croome, 1986), Chile, New Zealand, Malaysia, Sri Lanka (Durrschmidt, 1987a; Prokina and Mylnikov, 2017).
Acanthocystis penardi Wailes, 1925 [synonyms: A. spinifera Greeff, 1869; al. heterospina Nicholls, 1983] (Fig. 1, h—j).
Spine and plate scales from a single cell occupied an area 22.8—44.3 pm in diameter. Spine scales are 2.4—16.5 pm in length, with rounded base, 0.8—1.4
Table 2. Distribution of the observed species of Centrohelida (the sample numbers correspond to those in Table 1).
Species Microbiotopes (samples) Mire water bodies Region
1 2 3 4 5 б 7 в 9 10 11 12 13 14 Lk St Sp Lg Fl Ho A V K
Acanthocystis lyra - - - - - - - + - - - - - - - + - - - - - + -
A. pectinata + + +
A. penardi - + - - - - - - - - + + - + + - + - + - + - +
A. aff. takahashii - - - - - - - - + - - - - - - - - - + - - + -
A. trifurca - + + - - - - - + - - - - - - + + - + - + + -
A. turfacea "gigas" - - + + - - - + - - - - - - - + - - - - + + -
A. turfacea "viridis" - + - - - - + - - - - - - - - - + + - - + + -
Polyplacocystis ambigua + + +
P. symmetrica - - - - - - - - + - - - - - - - - - + - - + -
Choanocystis symna + - - - - - - - - - - - - - - - + - - - + - -
Pterocystis paliformis - - - - - - - - - - - - + - - - - - + - - - +
P. pinnata - + - - - - - + - - - - - - - + + - - - + + -
P. striata - - - - - - - - - - - + - - - - - - + - - - +
P. tropica + + - + + - + - - + + - + - + + +
Raineriophrys echinata - - - - + - - - - - - - - - - - - - - + + - -
R. kilianii - + - - - - - - - - - - - - - - + - - - + - -
Raphidiophrys intermedia - - - - - - + - - - - - - - - - - + - - - + -
R. minuta - - - - - - - - - - - - + - - - - - + - - - +
Heterophrys-like organisms - - - - - + - - + - - - - - - - - - + + + + -
Total 2 s 2 1 1 1 2 4 4 1 2 2 3 3 3 s 7 2 9 2 9 9 7
* Regions: A - Arkhangelsk Region, V - Vologda Region, K - Republic of Karelia.
^m in diameter. The hollow cylindrical shaft is 0.22—0.40 ^m in diameter, apex with 5—12 marginal teeth. Elliptical plate scales are 2.5—3.8x1.7—2.6 ^m, with slightly fringed margin, without axial thickening. Papillae were present on the external surface.
This species was described by G.H. Wailes in 1925 (Wailes, 1925) using a light microscopy, and redescribed by F.J. Siemensma in 1981 using the electron microscopy (Siemensma, 1981). Size and morphology of scales are similar to those given by many other authors, but M.M. Leonov described larger sizes for spine scales (up to 30 ^m) (Leonov, 2009, 2012).
The scales of four cells from sample 14, three cells from 12, ten cells from 2, and a few scales from 11 (Table 2) were observed.
Previous reports were from freshwaters of the European part of Russia (Mikrjukov, 1993a; Leonov and Plotnikov, 2009; Leonov, 2009, 2010, 2012; Leonov and Mylnikov, 2012; Zlatogursky, 2014a), Ukraine (Gaponova, 2009), Estonia (Mikrjukov, 1993b), Mongolia (Kosolapova and Mylnikov, 2015), Netherlands (Siemensma, 1981), Ethiopia (Prokina et al., 2017a), USA (Wujek, 2015), Canada
([as A. heterospina] Nicholls, 1983), India ([as A. spinifera] Wujek and Saha, 2006), Chile, Malaysia (Durrschmidt, 1987a; Prokina and Mylnikov, 2017), Nigeria (Wujek et al., 2007), and from marine waters of Sweden ([as A. spinifera] Siemensma and Roijackers, 1988a).
Acanthocystis afff. takahashii Durrschmidt, 1987 (Fig. 2, a-c).
Spine and plate scales from a single cell occupied an area 21.9-31.7 ^m in diameter. Straight spine scales are 2.7-8.9 ^m in length. The roundish cup-shaped base is 2.7-8.9 ^m in length, with the narrow marginal rim. The hollow cylindrical shaft is 0.180.27 ^m in diameter, at the apex divided into three pointed branches connected by a membrane. There are 2 small teeth at the lateral side of each branch. The most distant part of the apex of spine scales is 0.48-0.83 ^m in diameter. Elliptical plate scales are 2.2-3.3x1.2-2.1 ^m, with about 50 longitudinally oriented radial ribs and central ridge 0.45-0.56 ^m in length. There is the narrow marginal rim of 0.04-0.06 ^m width at the end of plate scales.
The dimensions and shape of observed scales agreed well with the original description by M.
Fig. 1. Electron microscopy of centrohelid species (SEM) : a, b, c—Acanthocystis lyra (b — first and third type of spine scales; c — first type of spine scales); d, e, f — A. trifurca; g — A.pectinata; h, i, j — A.penardi (i — plate scale; j — apex of the long type of spine scales). Scale bars: d, h — 10 pm; a, c, e — 5 pm; b, f, g, I, j — 2 pm.
Dürrschmidt in 1987 from Sri Lanka (Dürrschmidt, 1987a). Differs from A. takahashii by the presence of radial ribs on plate scales.
The scales of eight cells from sample 9 (Table 2) were observed.
Previous reports were from freshwaters of the European part of Russia (Leonov and Plotnikov, 2009; Leonov, 2009, 2010, 2012; Zlatogursky, 2014a) and the Far East of Russia (Zlatogursky, 2014a), Nigeria (Wujek et al., 2007), USA (Wujek, 2006), Sri Lanka, Japan, Canada (Dürrschmidt, 1987a).
Acanthocystis trifurca Nicholls, 1983 (Fig. 1, d—f).
Spine and plate scales from a single cell occupied an area 20 ^m in diameter, represented by one type of spine scales and plate scales. Spine scales straight or slightly curved, 3.4—10.2 ^m in length. The cylindrical hollow shaft of spine scales is 0.12—0.21 ^m in diameter, slightly tapers to the tip, and with 3 tapering teeth at the end. The rounded and flat base of spine scales is 0.45—1.0 ^m in diameter. Plate scales are roundish or pear-shaped, 2.3—3.0x1.4— 2.2 ^m, with a narrow marginal rim and central thickening of 0.43—0.73 ^m in length.
This species was originally described by K.H. Nicholls in 1980 from Canada using an electron microscope (Nicholls, 1983). Morphology of scales we observed was very similar to the type material; however, we did not observe a marginal rim.
This species was often identified as A. myriospina Penard, 1890. This confusion arose because M. Dürrschmidt in 1985 described this species using electron microscope, and her diagnosis was similar to A. trifurca, which she reduced to a synonym. K.H. Nicholls redescribed A. myriospina two years earlier, in 1983, and he pointed to the abruptly cut apex of spine scales. He also used light microscope, and correlated the dimensions of living cells with the description made by E. Penard. That is why we accepted the description of K.H. Nichols.
Scales of one cell from sample 2 and several cells from samples 3 and 9 (Table 2) were observed.
Previous reports of this species were from fresh waters of the European part of Russia ([as A. myriospina] Leonov and Plotnikov, 2009; Leonov, 2010, 2012; Leonov and Mylnikov, 2012; Ermolenko and Plotnikov, 2013; Plotnikov and Ermolenko, 2015), Crimea ([as A. myriospina] Mikrjukov, 1999), Ukraine ([as A. myriospina] Gaponova, 2009), Mongolia ([as A. myriospina] Kosolapova and Mylnikov, 2015), Switzerland
([as A. trifurca] Zlatogursky, 2014a), USA ([as A. myriospina] Wujek, 2006), Canada ([as A. trifurca] Nicholls, 1983), Nigeria ([as A. myriospina] Wujek et al., 2011), India ([as A. myriospina] Wujek and Saha, 2006), Chile ([as A. myriospina] Dürrschmidt, 1985), Australia ([as A. myriospina] Croome, 1986); from brackish inland waters of the European part of Russia ([as A. myriospina] Leonov and Plotnikov, 2009); from marine waters of the Black Sea ([as A. myriospina] Leonov, 2010, 2012).
Acanthocystis turfacea Carter, 1863 (Fig. 2, d—h).
Spine and plate scales from a single cell occupied an area 15.2—102.6 ^m in diameter. There are 2 types of spine scales. First type — short scales, 4.03—11.6 ^m in length. Distal part has 2 long (1.45—4.6 ^m), widely divergent furcae with 3 marginal teeth on the tip. Second type — long spine scales, 12.81—35.6 ^m in length, with 2 short furcae (0.4—1.6 ^m in length) at the distal part of the scales with 4 marginal teeth. The base of each type of spine scales is roundish, 0.95—2.58 ^m in diameter. Shafts of spine scales are 0.34—0.77 ^m in diameter.
We observed 2 so-called subspecies, "gigas" and "viridis", mentioned by Leonov, (2012), but never officially described. Morphology and dimensions of subspecies agreed well with those given by Leonov (2012). These "subspecies" differ from each other by their size. We observed scale groups with diameters 69.5 to 102.6 ^m (for gigas) and 15.2 to 28.4 ^m (for viridis); spine scales 9.4—35.6 ^m in length (for gigas) and 4.03—14.06 ^m in length (for viridis); plate scales 2.5—7.9X2.0—4.85 ^m (for gigas) and 2.5—3.9x2.0—2.5 ^m (for viridis).
Scales of three cells from sample 4 and a few scales from samples 3 and 8 of "subspecies" gigas, and eleven cells from sample 2 and a few cells from sample 7 of "subspecies" viridis (Table 2) were observed.
Previous records of A. turfacea were from fresh waters of the European part of Russia (Mikrjukov, 1993a, 1999; Leonov and Plotnikov, 2009; Leonov, 2010, 2012; Leonov and Mylnikov, 2012; Ermolenko and Plotnikov, 2013; Plotnikov and Ermolenko, 2015), Ukraine (Gaponova, 2009), Switzerland (Zlatogursky, 2014a), Netherlands (Siemensma, 1981), Nigeria (Wujek et al., 2007), India (Wujek and Saha, 2006), USA (Wujek, 2005, 2006, 2015), Canada (Nicholls, 1983), Chile (Dürrschmidt, 1985), Australia (Croome, 1986); from marine waters ofthe White Sea (Leonov, 2010, 2012), the Baltic Sea (Vors, 1992), and Antarctica (Croome et al., 1987).
Fig. 2. Electron microscopy of centrohelid species (SEM): a, b, c — Acanthocystisaff. takahashii; d, e, f—A. turfacea "gigas" (f — long type of spine scales); g, h — A. turfacea "viridis" (h — short type of spine scales); i, j — Polyplacocystis ambigua. Scale bars: a, d, g, i — 10 pm; e, f, j — 5 pm; b, c, h — 2 pm.
Family Raphidiophryidae Febvre-Chevalier et Febvre, 1984
Genus Polyplacocystis Mikrjukov, 1996
Polyplacocystis ambigua (Penard, 1904) Mikrjukov, 1996 [basionym: Raphidiophrys ambigua Penard, 1904] (Fig. 2, i, j).
Spine and plate scales from a single cell occupied an area 47.3 pm in diameter. Scales of 3 types were present: first type — fusiform scales 9.8—11.1x0.8— 1.6 pm; second type — elliptical scales with narrow margins 7.6—8.4x2.4—3.6 pm; third type — broad elliptic scales, with rounded margins 4.7—5.8x2.5— 3.2 pm. The external surface of scales had reticular structure. All types of scales had well marked marginal rims 0.25—0.43 pm in diameter.
Scales of only one cell from sample 14 (Table 2) were observed.
Previous records were from fresh waters of the European part of Russia (Leonov and Plotnikov, 2009; Leonov, 2010, 2012; Leonov and Mylnikov, 2012; Ermolenko and Plotnikov, 2013; Plotnikov and Ermolenko, 2015), Ukraine (Gaponova, 2009), Mongolia (Kosolapova and Mylnikov, 2015), The Netherlands (Siemensma, 1981; Siemensma and Roijackers, 1988b), USA (Wujek, 2006), Canada, Chile, New Zealand, Sri Lanka (Nicholls and Dürrshmidt, 1985).
Polyplacocystis symmetrica (Penard, 1904) Mikryukov, 1996 (Fig. 3, a, b).
Elongate elliptical scales (5.1—9.6x2.0—3.1 pm) from a single cell occupied an area about 42 pm in diameter. The external surface of scales had reticular structure and marginal rim was 0.18—0.39 pm in width.
Scales of only one cell from sample 9 (Table 2) were observed.
Previous records were from freshwaters of the European part of Russia (Leonov, 2010, 2012), The Netherlands (Siemensma, 1981; Siemensma and Roijackers, 1988b), Greenland (Ikävalko et al., 1996), and Canada (Nicholls and Dürrschmidt, 1985).
Order Pterocystida Cavalier-Smith, 2012 Family Choanocystidae Cavalier-Smith et von der Heyden,2007
Genus Choanocystis Penard, 1904
Choanocystis symna Zlatogursky, 2014 (Fig. 3, c—e).
Spine and plate scales from a single cell occupied an area 19.9—24.8 pm in diameter. Spine scales are 3.4—11.3 pm in length, slightly curved to the base of the scale. The shaft of spine scale is 0.3—0.4 pm in diameter, smoothly tapers to distal part with 4—5 teeth. The heart-shaped base is 1.4—1.9 pm in diameter, with the marginal rim at the inner side. Smooth dumbbell-shaped plate scales are 3.8-4.7x1.9-2.4 pm.
Scales of three cells from sample 1 (Table 2) were observed.
The morphology and dimensions of scales are similar to those originally described from the European part of Russia by V.V. Zlatogursky (Zlatogursky, 2014b). Only spine scales in the observed material were slightly larger than in the type material (3.9-6.7 pm).
Family Pterocystidae Cavalier-Smith et von der Heyden, 2007
Genus Pterocystis Siemensma et Roijackers, 1988
Pterocystis paliformis (Dürrschmidt, 1987) Siemensma, 1991 (fig. 3, i).
Spine scales are 3.0-3.6x1.4-1.8 pm in length. Shaft of spine scales is 0.04-0.10 pm in diameter with a roundish tip. Lateral wings connected with basal wings and formed shovel-shaped structure. There is a narrow rim at the margin of the wings and a small protrusion at the proximal part of the shaft. Ovoid or elliptical plate scales are of 1.4-2.3x0.9-1.5 pm, with central ridge, 0.82-1.41 pm in length and 0.03-1.41 pm in width.
The morphology and dimensions of the observed scales are very similar to those originally described by M. Dürrschmidt from Chile (Dürrschmidt, 1987b), except for the longer spine scales (up to 4.5 pm).
Several scales from sample 13 (Table 2) were observed.
This is the first record for this species from Russia. Previous records were from fresh waters of Chile, New Zealand (Dürrschmidt, 1987b; Prokina and Mylnikov, 2017), USA (Wujek, 2003a, 2005, 2006); from the Baltic Sea (Vors, 1992).
Pterocystis pinnata (Nicholls, 1983) Siemensma et Roijackers, 1988 (Fig. 4, a-c).
Cell coverings were represented by spine scales and plate scales. One type of spine scales is 4.1-6.4 pm long, curved at the proximal part. There are lateral wings at the both sides of the shaft, narrowed to the distal end. The distance between the widest
Fig. 3. Electron microscopy of centrohelid species (a—h — SEM; i — TEM): a, b — Polyplacocystis symmetrica; c, d, e — Choanocystissymna; f, g, h — Heterophrys-like organisms; i — Pterocystispaliformis (spine scales). Scale bars: a, c, f — 10 цт; b, g — 5 цт; d, e, h, i — 2 цт.
parts of lateral wings is 1.6—2.4 pm. Scoop-shaped base with a broad marginal rim curved at the right angle to shaft and lateral wings.
Elliptical plate scales 2.1—2.9x 1.4—1.6 pm with large central ridge of 1.15—1.19x0.13—0.17 pm.
Morphology and dimensions are very similar to those described by the other authors (Dürrschmidt, 1987b; Leonov, 2009), except for the lateral wing of spine scales, which goes to 1/2 of the length of the shift according to the description by F.J. Siemensma and M.M. Roijackers (Siemensma and Roijackers, 1988a).
The scales of three cells from sample 2 and one cell from sample 8 (table 2) were observed.
Previous reports were from freshwaters of the European part of Russia (Leonov, 2009; Leonov and Plotnikov, 2009), Sweden (Siemensma and Roijackers, 1988a), Nigeria (Wujek and Ogundipe, 2002), Canada (Nicholls, 1983), USA (Wujek et al., 2003b), Chile, and New Zealand (Dürrschmidt, 1987b).
Pterocystis striata (Nicholls, 1983) Siemensma et Roijackers, 1988 [basionym: Acanthocystis striata (Nicholls, 1983)] (Fig. 4, d, e).
Spine scales with shafts are 2.0—2.8 pm long and 0.14—0.20 pm in diameter, expand from the base and end with a rounded apex. The proximal part of shaft stretched out into oval membrane 1.7—2.5* 1.6—1.9 pm, with 30—34 radial ribs. The base of shaft with the small protrusion.
This species was described as Acanthocystis striata by K.H. Nicholls in 1983 from Canada. In 1988 F.J. Siemensma and R.M.M. Roijackers transferred this species to the genus Pterocysris (Siemensma and Roijackers, 1988a).
Only a few scales from sample 12 (table 2) were observed.
This is first record for Russia. Previous records were from fresh waters of Germany, Chile, New Zealand (Dürrschmidt, 1987b), USA (Wujek, 2003a, 2005), Canada (Nicholls, 1983), Nigeria (Wujek et al., 2007), and Tasmania (Croome, 1986).
Pterocystis tropica (Dürrschmidt, 1987) Sie-mensma et Roijackers, 1988 (Fig. 4, f—h).
Spine and plate scales from a single cell occupied an area 7.7—23.1 pm in diameter. Spine scales are 1.9—6.9 pm in length, with hollow shaft, 0.07—0.20 pm in diameter, tapers to the apex. There are proximally rectangular lateral wings with the
marginal rim located on the both sides of the shaft. The shaft curved at the base and with lateral wings forming bucket-like structure. The inner surface of spine scales with 7—9 parallel unequal ribs. Elliptical or oviform plate scales are of 1.9—2.8x 1.2—1.8 pm, with median protrusions 0.41—1.28 pm in length.
Morphology and dimensions of the observed scales are close to subspecies A. tropica ssp. paucist-riata described by M. Dürrschmidt from Chile (Dürrschmidt, 1987b), which lateral and basal wings have less number of radial ribs and plate scales without radial ribs. Later K.A. Mikrjukov placed this subspecies to Pterocystis tropica (Mikrjukov, 2002).
Scales of four cells from sample 10, nine cells from sample 11, and a few scales from samples 1, 8, and 13 (Table 2) were observed.
This is the first record from Russia. Previous records were from fresh waters of Germany, Sri Lanka, Chile (Dürrschmidt, 1987b), Nigeria (Wujek et al., 2007, 2011), India (Wujek, Saha, 2006), USA (Wujek, 2015).
Genus Raineriophrys (Mikrjukov, 2001) Mikrjukov, 2002
Raineriophrys echinata (Rainer, 1968) Mikrjukov, 2000 (Fig. 4, i).
Spine scales with hollow shafts, 10.5—23.6 pm in length, and 0.40—0.56 pm in diameter, curved at the proximal part and pointed at distal part. Thare are lateral wings with a few teeth along the length of shaft. Lateral wings connected by a membrane with a heart-shaped base 1.5—2.2 pm in diameter.
A few scales from sample 5 (Table 2) were observed.
Previous records were from fresh waters of Russia (Leonov and Plotnikov, 2009; Leonov, 2009, 2010, 2012; Leonov and Mylnikov, 2012), Ukraine (Gaponova, 2009), and The Netherlands (Siemensma, 1981; Siemensma and Roijackers, 1988a).
Raineriophrys kilianii (Dürrschmidt, 1987) Mikrjukov 2001 (fig. 4, j, k).
Spine and plate scales from a single cell occupied an area 17.5 pm in diameter. Spine scales are 7.4— 10.6 pm in length, strongly curved and tapering to truncated apex. Hollow shaft with 2 narrow wavy lateral wings extending to 2/3 of the shaft length. Bases of the wings are bucket-shaped, 1.2—3.9 pm in width. Ovoid plate scales are patternless, 3.6-4.4x2.4-2.7 pm.
Fig. 4. Electron microscopy of centrohelid species (SEM): a, b, c — Pterocystispinnata (b — spine scale; c — plate scale); d, e — P. striata (spine scales); f, g, h — P. tropica (g — plate scale; h — base of spine scale); i — Raineriophrys echinata; j, k — R. kilianii. Scale bars: a, f, j — 10 5 ^m; b — 5 ^m; c, g, h, i, k — 2 ^m; d, e — 1 ^m.
This species was originally described by M. Dürrschmidt from Chile (Dürrschmidt, 1987b). Our observations are very similar to this description, except for larger size of scale groups on the whole-mounts (25—40 ^m). F.J. Siemensma and M.M. Roijackers, on the contrary, described very small areas — 14 ^m (Siemensma and Roijackers, 1988a). M.M. Leonov described a pointed apex of the spine scales (Leonov, 2012). In addition, some authors (Croome, 1987; Dürrschmidt, 1987b; Mikrjukov, 2002; Leonov, 2012) described central ridge on the plate scales.
Scales of only one cell from sample 2 (Table 2) were observed.
Previous records were from fresh waters of the European part of Russia (Leonov, 2012; Leonov and Mylnikov, 2012), Germany, Chile (Dürrschmidt, 1987b), The Netherlands, Sweden (Siemensma and Roijackers, 1988a), Tasmania (Croome, 1987), USA (Wujek, 2003a); from marine waters of the White Sea (Leonov, 2012).
Centroplasthelida incertae sedis Genus Raphidiophrys Archer, 1867
Raphidiophrys intermedia Penard, 1904 (Fig. 5, a—c).
Cell coverings were represented by one type of scales with complex structure. Scales are 4.6— 9.2x2.5—4.9 ^m, elongated to elliptical, rarely triangular or three-lobed. The margins of scales wrapped from the inside to the outer side, forming a rather wide rim (0.28—0.56 ^m in width) with 38—64 radial ribs.
Scales of five cells from sample 7 (Table 2) were observed.
Previous records were from fresh waters of the European part of Russia (Leonov and Plotnikov, 2009; Leonov, 2009, 2010, 2012), Sweden, Holland (Siemensma, 1981; Siemensma and Roijackers, 1988b), India (Wujek and Saha, 2006), Nigeria (Wujek and Ogundipe, 2002; Wujek et al., 2007, 2011), Tasmania (Croome, 1987), USA (Wujek, 2003a, 2003b, 2005, 2006), Canada, Chile, New Zealand, Malaysia (Nicholls and Dürrschmidt, 1985).
Raphidiophrys minuta Nicholls, 1985 (Fig. 5d).
Roundish to oval plate scales 2.40-6.54x1.80-4.95 ^m, with radial ribs, without a marginal rim. Several scales from sample 13 (Table 2) were observed. This is the first record for Russia.
Previous reports were from Canada (Nicholls and Dürrschmidt, 1985), Nigeria (Wujek et al., 2011), Australia (Croome, 1986).
Heterophrys-like organisms (Fig. 3, f—h).
Numerous radially oriented spicules from a single cell 5.0—8.3 pm in length occupied an area 11.3—34.1 ^ in diameter. The width of spicules ranges from 0.05 to 0.10 j^m, being nearly the same along the entire length, tapering to pointed tips. Spicules are slightly flattened and smoothly spirally twisted.
Morphology and dimensions of the observed cells are similar to Marophrys marina (Hertwig et Lesser, 1874) Cavalier-Smith et von der Heyden, 2007 (Mikijukov and Croome, 1998; Plotnikov and Ermolenko, 2015), but differs by slightly flattened and smoothly spirally twisted spicules. In addition, K.A. Mikrjukov described Marophrys marina with non-tapering spicules, with the length equal to the cell diameter (Mikrjukov, 2001).
Spicules of eight cells from sample 6 and three cells from sample 9 (Table 2) were observed.
Discussion
We observed 18 species of centrohelid heliozoans, 15 of which belong to five genera from four families; two species from one genus have an uncertain systematic position; and some belong to unidentified Heterophrys-like organisms (Table 2). The greatest number of species belongs to the families Acanthocystidae and Pterocystidae (6 species in each family). Two species belong to the family Raphydiophryidae, one to Choanocystidae.
Morphology of the observed scales is similar to those given by the other authors. However, we detected some slight differences in the size and the shape. The lengths of spine scales of Acanthocystis pectinata, A. penardi and Pterocystis paliformis were smaller than those reported earlier (Dürrschmidt, 1985, 1987b; Siemensma and Roijackers, 1988a; Leonov and Plotnikov, 2009; Leonov, 2009, 2012). The observed spine scales of Choanocystis symna were slightly longer in comparison to the original description (Zlatogursky, 2014b). We did not observe marginal rim at the base of spine scales of Acanthocystis trifurca, mentioned in the description of K.H. Nicholls (Nicholls, 1983). We observed curved apexes of spine scales in Pterocystis kilianii, while Leonov (2012) described pointed apexes. The
Fig. 5. Electron microscopy of centrohelid species (a-c — SEM; d — TEM): a, b, c — Raphidiophrys intermedia; d — R. minuta. Scale bars: a — 20 pm; b — 5 pm; c, d — 2 pm.
size of the observed plate scales of Acanthocystis pectinata was slightly larger than that described by the other authors (Nicholls, 1983; Siemensma and Roijackers, 1988a). We observed plate scales of Pterocystis kilianii without axial thickening, while many authors reported it (Croome et al., 1987; Dürrschmidt, 1987b; Mikrjukov, 2001; Leonov, 2012). All observed insignificant variability in size and shape of the scales could be due to the intraspecific variability. Thus, we supplemented and refined descriptions of many observed species.
The most frequently occurred species in the studied samples were Pterocystis tropica and Acanthocystis turfacea (found in 5 samples) and Acanthocystis penardi (4 samples). Twelve species (Acanthocystis lyra, A. pectinata, A. aff. takahashii, Polyplacocystis ambigua, P. symmetrica, Choanocystis symna, Pterocystis paliformis, P. pterocantha, Raineriophrys echinata, R. kilianii, Raphidiophrys intermedia and R. minuta) were rare, found only in one sample.
Most species are cosmopolitans. Two species, which distribution is not sufficiently studied, were recently described from the European part of Russia — Acanthocystis lyra and Choanocystis symna (Zlatogursky, 2014b; Gerasimova and Plotnikov, 2016). Many species were previously found in marine and saline continental waters: Acanthocystis myriospina, A. penardi, A. turfacea, Pterocystis paliformis, P. pinnata and Raineriophrys kilianii
(Croome et al., 1987; Siemensma and Roijackers, 1988a; Vors, 1992; Mikrjukov, 1999; Leonov, 2010, 2012), and thus might be considered as euryhaline.
Three species (Pterocystis paliformis, P. striata, P. tropica) were reported in Russia for the first time. We found eight species in the Arkhangelsk Region (Acanthocystis trifurca, A. penardi, A. turfacea, Choanocystis symna, P. pinnata, P. tropica, Raineriophrys echinata, R. kilianii), all of which being the first records for the region. We found eight species from the Vologda Region (Acantho-cystis lyra, A. trifurca, A. aff. takahashii, A. turfacea, Polyplacocystis symmetrica, Pterocystis pinnata, P. tropica, Raphidiophrys intermedia), six of them being new for this region, and two were previously reported — Acanthocystis trifurca and A. turfacea (Leonov, 2012). We found seven species from the Republic of Karelia (Acanthocystis pectinata, A. penardi, Polyplacocystis ambigua, Pterocystis paliformis, P. striata, P. tropica, Raphidiophrys minuta), four of them being new for this region, and three species were previously reported — Acanthocystis pectinata, A. penardi, Polyplacocystis ambigua (Leonov, 2012; Leonov and Mylnikov, 2012; Zlatogursky, 2014a, 2014b). Only Pterocystis tropica was found in all three investigated regions.
The species diversity of centrohelid heliozoans in the mires of the Arkhangelsk Region and the Vologda Region were the closest (the Sorensen similarity index 0.58), each having 9 species. The
species composition in the Republic of Karelia has small resemblance with the other two (only two species were common, Acanthocystis penardi and Pterocystis tropica).
From 1 to 7 species were found in the individual mire massifs (2.1 on average). The greatest number of species was found in the Nizinnoe mire (7 species) and Schichengskoe mire (6 species). It is worth noting that the same mire massifs were characterised by the large species richness of another group of protists, heterotrophic flagellates (Prokina et al., 2016, 2017b).
The studied mire water bodies differed both in typology, genesis, and physical-chemical parameters of water (Table 1). From 2 to 9 species were found in the mire water bodies (4.1 on average).
The least richness was observed in the laggs and the hollows in the ombrotrophic mires, having 2 species each. At that, only these mire water bodies had Raphidiophrys intermedia (in lagg) and Raineriophrys echinata (in hollow). The low species richness in these ombrotrophic mire water bodies could be due to the oligotrophic character of the phytocoenoses in general, as well as hydrochemical water characteristics, being strongly affected by the Sphagnum mosses (projective cover reaching 90-95%), and the low pH values of 4.2-5.5, lack of flowage, small depths, and fast warming, and also significant plankton development (Philippov, 2014; Zaytseva et al., 2016; Stroynov and Phillippov, 2017). Only three centrohelid species were found in the mire lake Krugloe (Acanthocystis pectinata and Polyplacocystis ambigua were found only here).
The greatest number of centrohelids (15 species) was registered in the water bodies of minerotrophic mires. Five species were found in the mire streams (Acanthocystis lyraand A. turfacea "gigas" only here); seven species were found in the space bet-ween the hummocks (Choanocystis symna and Raineriophrys kilianii only here); nine species were found in the flarks of the aapa mires (Acanthocystis aff. takahashii, Polyplacocystis symmetrica, Pterocystis paliformis, P. striata and Raphidiophrys minuta only here). These habitats are characterized by lower pH values (5.1-6.6), poor flowage, open water zones, and eutrophic phytocoenoses. As a rule, in the minerotrophic mire water bodies, centrohelid heliozoans tend to be present in the bottom detrital matter rather than in the water column. In general, the minerotrophic mire water bodies appear to have the most favourable environmental conditions, compared to ombrotrophic ones.
The present study promotes the current knowledge of the centrohelid heliozoans species richness in the water bodies of northern mires. To date, 24 centrohelid heliozoans species were reported for the mires of the northern part of the European Russia (Leonov, 2012; Leonov and Mylnikov, 2012; current paper). The data obtained in the present study challenge the assertion by M.M. Leonov (Leonov, 2012) that northern mires have the lesser centrohelid heliozoa diversity compared with the mires of the forest steppe zone of the Central Russian Upland. Further investigations and analysis of the other types of mires and mire water bodies will help to reveal new species for the mire ecosystems, but also will gain some insight into the role of centrohelid heliozoans in the mire water bodies ecosystem structure and functioning.
Acknowledgments
This work was supported by the Russian Foundation for Basic Research (grant 14-04-32258 mol_a, grant 17-04-00565, grant 13-05-00837, grant 1529-02518 ofi_m). We are grateful to O .V. Galanina, A.A. Przhiboro, S.A. Kutenkov, and V.A. Philippov for their help in the field study, and to A.P. Mylnikov and D.V. Tikhonenkov for the discussions of the present paper and valuable suggestions.
References
Burki F., Kaplan M., Tikhonenkov D.V., Zlatogursky V. et al. 2016. Untangling the early diversification of eukaryotes: a phylogenomic study of the evolutionary origins of Centrohelida, Haptophyta and Cryptista. Proc. Royal. Soc. B. 283, (1823), 20152802.
Cavalier- Smith T.and von der Heyden S. 2007. Molecular phylogeny, scale evolution and taxonomy of Centrohelid heliozoa. Mol. Phyl. Evol. 44, 1186-1203.
Croome R.L. 1986. Observations ofthe heliozoan genera Acanthocystis and Raphidocystis from Australia. Arch. Protistenkd. 131, 189-199.
Croome R.L. 1987. Observations of heliozoan genera Acanthocystis, Raphidiophrys, Clathrulina, and Pompholyxophrys from Australian freshwaters. Arch. Protistenkd. 133, 237-243.
Croome R.L., van den Hoff J. and Burton H.R. 1987. Observations of the Heliozoean gene-
ra Pinasiophora and Acanthocystis (Heliozoea, Sarcodina, Protozoa) from Ellis Fjord, Antarctica. Polar Biol. 8, 23-28.
Dürrschmidt M. 1985. Electron microscopic observations on scales of species of the genus Acanthocystis (Centrohelidia, Heliozoa) from Chile. I. Arch. Protistenkd. 129, 55-87.
Dürrschmidt M. 1987a. An electron microscopical study of freshwater Heliozoa (genus Acanthocystis, Centrohelidia) from Chile, New Zealand, Malaysia and Sri-Lanka. II. Arch. Protistenkd. 133, 21-48.
Dürrschmidt M. 1987b. An electron microscopical study on freshwater heliozoan (genus Acanthocystis, Centrohelidia) from Chile, New Zealand, Malaysia and Sri Lanka. III. Arch. Protistenkd. 133, 49-80.
Dürrschmidt M. and Patterson D.J. 1987. On the organization of the Heliozoa Raphidiophrys ambigua Penard and R. pallida Sculze. Ann. Sci. Nat. 8, 135-155.
Ermolenko E.A. and Plotnikov A.O. 2013. Ecology of centrohelid heliozoa in the Southern Urals reservoirs. Vestnik OGU. 10, 118-121 (in Russian with English summary).
Gaponova L.P. 2009. Centrohelid heliozoa (Centrohelea Cavalier-Smith, 1993) Kievskogo and Chernigovskogo Polissya. PhD thesis. Kiev (in Ukrainian).
Gerasimova E.A. and Plotnikov A.O. 2016. New freshwater species of Centrohelids Acanthocystis lyra sp. nov. and Acanthocystis siemensmae sp. nov. (Haptista, Heliozoa, Centrohelea) from the South Urals, Russia. Acta Protozool. 55, 231-237.
Ikävalko J., Thomsen H.A. and Caestens M. 1996. A preliminary study of NE Greenland shallow meltwater ponds with particular emphasis of loricate and scale-covered forms (Choanoflagellida, Chrysophyceae sensu lato, Synurophyceae, Heliozoa), including the descriptions of Epipyxis thamno-ides sp. nov. and Pseudokephyrion poculiforme sp. nov. (Chrysophyceae). Arch. Protistenkd. 147, 29-42.
Kosolapova N.G. and Mylnikov A.P. 2015. First record of Centrohelid heliozoans (Centrohelida) in Mongolia. Inland Water Biology. 8 (3), 232-235.
Leonov M.M. 2009. Heliozoan fauna of water-bodies and watercourses of the Central Russian Upland forest-steppe. Inland Water Biology. 2 (1), 6-12.
Leonov M.M. 2010. Heliozoans (Heliozoa,
Sarcodina, Protista) of fresh and marine water of the European part of Russia: species composition, morphology, and description. Inland Water Biology. 3 (4), 344-355.
Leonov M.M. 2012. Species diversity and morphology of Heliozoa of waterbodies and watercourses in European part of Russia. PhD thesis. Borok (in Russian).
Leonov M.M. and Mylnikov A.P. 2012. Centro-heliozoa from Southern Karelia. Zool. Zh. 91, 515-523 (in Russian with English summary).
Leonov M.M. and Plotnikov A.O. 2009. Species composition, morphology, and distribution of Centrohelid Heliozoa from Central Chernozemic Area and the South Urals. Zool. Zh. 88, 1-11 (in Russian with English summary).
Mikrjukov K.A. 1993a. Observations on Centro-heliozoa (Sarcodina, Protozoa) of the Volga basin. Zoosystematica Rossica (St.Petersburg). 2, 201-209.
Mikrjukov K.A. 1993b. On centrohelid and rotosphaerid Heliozoa from the environs of the Vörtsjärv limnological station in Estonia. Proc. Estonian Acad. Sci. Biol. 42, 154-160.
Mikrjukov K.A. 1999. Interesting findings of heliozoan (Protista) in Black Sea and Crimea: data on the similarity of sea and freshwater fauna of these organisms. Rus. J. Zool. 3, 240-249.
Mikrjukov K.A. 2002. Centrohelid heliozoans (Centroheliozoa). KMK Sci. Press, Moscow (in Russian with English summary).
Mikrjukov K.A. 2001. Heliozoa as a component of marine microbenthos: a study of heliozoa of the White Sea. Ophelia. 54, 51-73.
Mikrjukov K.A. and Croome R.L. 1998. Observations of heliozoans in Ice-covered ponds on Mount Buffalo. The Victorian Naturalist. 115, 239-241.
Moestrup 0. and Thomsen H.A. 1980. Preparations of shadow cast whole mounts. In: Handbook of Phycological Methods. Cambridge Univ. Press, Cambridge. p. 385-390.
Nicholls K.H. 1983. Little-known and new heliozoeans: the centrohelid genus Acanthocystis, including descriptions of nine new species. Can. J. Zool. 61, 1369-1386.
Nicholls K.H. and Dürrschmidt M. 1985. Scale structure and taxonomy of some species of Raphidocystis, Raphidiophrys and Pompholyxophrys (Heliozoea) including descriptions of six new taxa. Can. J. Zool. 63, 1944-1961.
Philippov D.A. 2014. Hydrochemical characteristics of mire water tracks (by the example of Shichengskoe raised bog, Vologda Region). Water: chemistry and ecology. 7, 10—17 (in Russian with English summary).
Plotnikov A.O. and Ermolenko E.A. 2015. Centrohelid heliozoan (Chromista, Hacrobia) of Southern Cis-Ural Region. Biol. Bull. 42, 683-695.
Prokina K.I. and Mylnikov A.P. 2017. Centro-heliozoa of different types freshwater water bodies of South Patagonia and Tierra del Fuego, Chile. Inland Water Biology (in press).
Prokina K.I., Mylnikov A.P. and Zelalem W. 2017a. First data on heterotrophic flagellates and heliozoans of Ethiopia. Zool. Zhur. 96 (2), 127-143 (in Russian with English summary).
Prokina K.I., Mylnikov A.P., Galanina O.V. and Philippov D.A. 2017b. First data on heterotrophic flagellates in the mires of Arkhangelsk Oblast', Russia. Zool. Zhur. 96 (5), 499-510 (in Russian with English summary).
Prokina K.I., Philippov D.A. and Mylnikov A.P. 2016. On heterotrophic flagellates of raised bogs Sphagnum hollows in the North of European Russia. In: Proceed. VI Intern. Meet. Biology of Sphagnum. St.Petersburg, Khanty-Mansiysk. July 28 — August 11, 2016. Tomsk, Tomsk State Univ. Publ. pp. 56—58 (in Russian with English summary).
Rainer H. 1968. Urtiere, Protozoa, Wurzelfüßler, Rhizopoda, Sonnentierchen, Heliozoa. In: Die Tierwelt Deutschlands. (Ed. Dahl F.) Т. 56.
Siemensma F.J. 1981. De Nederlandse Zonne-diertjes (Actinopoda, Heliozoa). Wetenschappelijke Mededelingen. (Koninklijke Nederlandse Natuur-historische Vereniging). Zeist, Koninklijke Nederlandse Natuurhistorische Vereniging. 149, 1—118 (in Dutch).
Siemensma F.J. and Roijackers M.M. 1988a. A study of new and little-known acanthocystid heliozoans, and a proposed devision of the genus Acanthocystis (Actinopoda, Heliozoea). Arch. Protistenkd. 135, 197-212.
Siemensma F.J. and Roijackers M.M. 1988b. The genus Raphidiophrys (Actinopoda, Heliozoea): scale morphology and species distinctions. Arch. Protistenkd. 136, 237-248.
Stroynov Ya.V. and Philippov D.A. 2017. Bacterio- and virioplankton in water bodies of a raised bog (Vologda oblast, Russia). Inland Water Biology. 10, 37-43.
Vors N. 1992. Heterotrophic amoebae, flagella-
tes and heliozoa from the Tvärminne area, Gulf of Finland, in 1988-1990. Ophelia. 36, 1-109.
Wailes G.H. 1925. III. Some new or rare Protozoa from British Columbia. J. Nat. History. 16, 40-48.
Wujek D.E. 2003a. Freshwater scaled heterotrophic protistans from four Gulf States, including descriptions of two new species. J. Alabama Acad. Sci. 74, 164-180.
Wujek D.E. 2003b. Freshwater heliozoan (Protista, Heliozoa) from Indiana. Proc. Indian Acad. Sci. 112, 169-174.
Wujek D.E. 2005. Identification, ecology, and distribution of scale bearing amoeba, ciliates, flagellates and heliozoan from the Carolinas. J. North Carolina Acad. Sci. 121, 1-16.
Wujek D.E. 2006. Freshwater heliozoa from Florida. Florida Sci. 69, 177-191.
Wujek D.E. 2015. Freshwater silica-scaled heterotrophic Protista: Heliozoan, Thaumatomonad Flagellates, Amoebae, and Bicosoecids, from the Lake Itasca Region, Minnasota. J. Minnesota Acad. Sci. 78, 1-14.
Wujek D.E. and Ogundipe O.T. 2002. Heliozoa from Nigeria. Trop. Freshw. Biol. 11, 1-9.
Wujek D.E. and Saha L.C. 2006. Freshwater scaled Heterotrophic Flagellates and Heliozoa from India including a description of a new species of Choanocystis. J. Bombay Nat. Hist. Soc. 103, 71-81.
Wujek D.E., Dziedzic R.M., Kadiri M.O., Adesalu T.A. and Nwankwo D.I. 2007. Identification, ecology, and distribution of heliozoa, scaled flagellates and scaled ciliates from Western Nigeria. Trop. Freshw. Biol. 16, 1-15.
Wujek D.E., Kadiri M.O. and Dziebzic R.M. 2011. Freshwater scaled chrysophytes, heliozoan and thaumatomonad flagellates from Edo State, Nigeria. African J. Aquatic Sci. 6, 207-212.
Zaytseva V.L., Philippov D.A. and Lobunicheva V.L. 2016. Zooplankton ofraised bogs hollows in the central part of the Vologda Region. Vestnik Sankt-Petersburgskogo universiteta. Ser. 3. Biologiya. 2, 4-17 (in Russian with English summary).
Zlatogursky V.V. 2014a. Diversity and evolution cover structure of centrohelid heliozoans (Protista: Centrohelida). PhD thesis. St. Petersburg (in Russian).
Zlatogursky V.V. 2014b. Two new species of centrohelid heliozoans: Acanthocystis costata sp. nov. and Choanocystis symna sp. nov. Acta Protozool. 53, 313-324.
Address for correspondence: Kristina I. Prokina. I.D. Papanin Institute for Biology of Inland Waters of Russian Academy of Sciences, 109, Borok, Nekouzskiy destrict, Yaroslavskaya Oblast', 142742, Russia; e-mail: [email protected]
