Protistology 4 (2), 107 120 (2005) Protistology
Species composition of benthic ciliate community in the Chernaya River estuary (Kandalaksha Bay, White Sea) with a total checklist of the White Sea benthic ciliate fauna
Yuri A. Mazei1 and Igor V. Burkovsky2
1 Department of Ecology, Penza State Pedagogical University, Penza, Russia 2 Department of Hydrobiology, Biological Faculty, Moscow State University, Moscow, Russia
Summary
During the period of 1998 2000, 123 psammophilous ciliate species were found in the White Sea estuary. Community consists of marine stenohaline species occurring in the marine part of the estuary, marine euryhaline ciliates represented both in the marine and the freshened zone and brackish water organisms dominating in the riverine part of the estuary. On the other hand, community is composed of basic structure forming species (the community "nucleus"), constantly prevailing in a certain estuarine zone, and accidental, or very rare species (cryptic diversity), sporadically occurring at different stations during different seasons. The total list of the White Sea benthic ciliate fauna contains 273 species from 94 genera, recorded in the Kandalaksha Bay. Only 3.5 5.8% of the total White Sea species richness constitute "active" diversity in a given microhabitat at a particular point in time. Relations between the number of samples taken and the number of species registered testify to species saturation at all stations. Spatial heterogeneity of the biotope causes a greater increase in species richness than temporal one.
Key words: benthic interstitial ciliates, estuary, White Sea ciliate fauna, community structure
Introduction and critical salinity level (3 8 ‰) cause lower community complexity in estuaries as compared with Protozoan communities in estuaries are formed communities in other biotopes (Khlebovitch, 1974; under the influence of a complex of factors. Among Safianov, 1987; Burkovsky and Stoljarov, 1995; them salinity is of the greatest importance (Mazei et Burkovsky and Mazei, 2001). However, species richness al., 2002). Moreover, great environmental variability may achieve high levels due to complex interactions
© 2005 by Russia, Protistology 108 · Yuri A. Mazei and Igor V. Burkovsky between active and passive species diversity and envi ronmental factors. The aim of this study is to describe species com position of psammophilous ciliate community in terms of their distribution along the salinity gradient in the estuary and their role in the community organisation. In addition, we present a total species list of benthic ciliates of the White Sea.
Material and Methods Investigations were conducted during 1998 2000 summer periods in the Chernaya river estuary (the Fig. 1. A scheme of location of stations 1 5 in the Kandalaksha Bay, the White Sea). Material was estuary. Thick line coastline, thin line zero of collected at 5 permanent stations. The stations were depth. located at the middle horizon of the intertidal zone along the estuary (Fig. 1). A detailed hydrological and 100, st. 2 94, st. 3 87, st. 4 72, st. 5 59 species. As hydrochemical characteristic of the stations was given salinity decreases, the number of species falls significantly. in a previous article (Burkovsky and Mazei, 2001). During one summer season only some of the species Each station was a strictly fixed sampling area 50 x characteristic of a given biotope can be encountered, 50 cm, where recordings of the ciliate abundance were since many ciliates (about a half at every station) do performed. Extraction and quantitative counting of not always get into the samples because of their low ciliates were performed on live individuals (Carey, abundance. 1991). The ciliates were identified on the Shatton Lwoff From the total ciliate species diversity, species silver impregnated preparations (Foissner, 1991), groups according to salinity gradient are distinguished according to Carey (1991). with the aid of cluster analysis (Fig. 2). In different Most of the species names are given following Carey seasons 6 7 clusters are marked at the same similarity (1991). The main results of recent revisions of Trache level. The trends of species' relative abundance changes locercidae, Kentrophoros and Metopus were also taken along the estuary are represented in Fig. 3. Clusters 1 into account (see Azovsky and Mazei, 2003). The and 1a include marine stenohaline species occurring at following species of Trachelocercidae already redes the stations 1 and 2; clusters 2 and 3 are composed of cribed are given below in accordance with the newly marine euryhaline organisms from the stations 2 and 3 rebuilt system and the synonymy arisen: Trachelocerca accordingly; clusters 4, 4а and 4b consist of brackish sagitta (Syn.: Tracheloraphis striata Raikov 1962), water ciliates, forming community at the stations 4 and Trachelocerca incaudata (Syn.: Tracheloraphis incaudatus 5. Quantitative data about all estuarine ciliates are given (Kahl 1933) Dragesco 1960), Tracheloraphis longicollis in table 1, where species are grouped in accordance to (Syn.: Trachelonema longicollis Dragesco 1960), Tra belonging to clusters reflecting their spatial distribution cheloraphis oligostriata (Syn.: Trachelonema oligostriata along the salinity gradient. Raikov 1962). On the other hand, estuarine ciliate species may be To distinguish species groups with similar distribu grouped depending on the role played by ciliates in the tion along the estuary, the cluster analysis by complete community: 1) basic structure forming species with linkage method on the basis of a matrix of Czsekanovsky distinct preferences in terms of distribution along the similarity indices was performed. Calculations were estuary, 2) species widely distributed along the estuary conducted with the help of STATISTICA software and appearing at different stations in different years, package. To construct curves of dependence between 3) rare ciliates sporadically occurring in the community the number of samples taken and the number of species (Table 1). observed, original software rendered by Dr. A.I. Azovsky Annually, 23 dominating and 37 subdominating (Moscow M.V. Lomonosov State University) was used. species compose the basis of the ciliate community in the estuary, which constitutes almost a half of the total Results and Discussion species richness. These species occur constantly in samples and form the community "nucleus". In Fig. 4 distribution patterns of mass species (relatively constant SPECIES COMPOSITION OF THE ESTUARINE COMMUNITY structural components of the community) are given. Altogether, in the studied zones of the Chernaya The share of each of them at least at one of the 5 stations river estuary 123 species of ciliates were found: st. 1 is about 5% of total biomass. However, their relative Protistology · 109
within the estuary, but they are very infrequent (Table 1). It has been proposed that the microbial diversity of a habitat may be defined as the number of microbial niches filled at a particular point in time (Finlay et al., 1997). Therefore in a given ecosystem only a limited number of microbial niches is available at any moment in time (Finlay and Esteban, 1998). So, ciliate species diversity may be divided into "active" and "passive" diversity, i.e. species that have found their niches and are engaged in population growth, and those that are waiting for the arrival of conditions suitable for growth and reproduction (Petz and Foissner, 1988; Fenchel et al., 1997; Finlay, 1998). In the estuary during the three summer periods only 60 species (about 50% of the total species richness) may be distinguished as "active" diversity (Table 1). Moreover, a single sample contains 20 60 species (concrete level depends on salinity regime and seasonal succession stage (Burkovsky and Mazei, 2001; Mazei and Bur kovsky, 2002; Mazei et al., 2002), i.e. on the number of ecological niches available). Among them only 10 16 species dominate and may be considered as an "active" component of the community. So we may conclude that only 3.5 5.8% of the total White Sea species richness constitute "active" diversity in a given microhabitat at a particular point in time. Fig. 2. Results of the cluster analysis of the species based on In addition, in Fig. 5 relations between species distribution similarity according to salinity gradient. 1 number of samples taken and number of species 4b clusters. A 1998, B 1999, C 2000. registered are represented. It is obvious that at all stations asymptotic level of species richness contribution into total abundance and biomass fluctuates curve (i.e. species saturation) is observed. All curves are from year to year and throughout the season (it is approximated by linear regression model in log reflected in the corresponding indices of coefficient of transformed data. Asymptotic value of species richness variation CV). As a rule, the most mass and typical curve is proved by negative residuals occurring in the for a given area species have the most stable abundance. tail in the residuals vs. number of samples curve. In table Low values of CV indicate a higher correspondence of 2 data representing the dependence between the set of given conditions to the ciliates' environmental requi samples taken and the number of species recorded is rements, whereas high values, lower correspondence, given. For revealing 90 % of total species richness it is thus characterising the preferendum zone for this or necessary to take: a) 6 9 samples at a station in a given that species in the whole complex of natural factors. season, b) 13 19 samples at a station during three years, Another part of the community is represented by c) 23 samples at all stations in a given season and d) 41 accidental or very rare species (cryptic diversity samples at all stations during three years. In the marine Fenchel et al., 1997), sporadically occurring at different part of the estuary species saturation comes faster than stations during different seasons. At the same time, in the riverine one. On the other hand, increasing the some of these species may contribute a significant part number of the seasons investigated yields a greater (up (up to 2%) into the total community biomass. However, to 1.3 times) species number at a given station. Increasing in different seasons they may develop at extremely the number of stations within the estuary leads to the distant stations depending on abiotic and/or coenotic rise of species number up to 1.7 times. This indicates factors. Another part of the cryptic diversity consists of that spatial heterogeneity of the biotope causes a greater species with stable preferences in terms of location increase in species richness than temporal one. 110 · Yuri A. Mazei and Igor V. Burkovsky
Fig. 3. Distribution of ciliates' clusters in the estuary.
TOTAL SPECIES LIST OF THE BENTHIC CILIATES OF THE Class Karyorelictea Corliss 1974 WHITE SEA Order Prostomatida Small et Lynn 1985 Family Kentrophoridae Jankowski 1980 Total species list of the benthic ciliates of the White Genus Kentrophoros Sauerbrey 1928 Sea was compiled on the basis of our long term obser K. fasciolatus (Sauerbrey 1928) Dragesco 1960 vations in the Velikaya Salma Strait and Chernaya river K. gracilis Raikov 1963 estuary (Burkovsky, 1970a, 1970b, 1970c, 1976, 1984, K. grandis Dragesco 1954 1992), as well as literature sources (Fokin, 2001). K. latum Raikov 1962 Altogether 273 ciliate species from 94 genera are K. uninucleatum Raikov 1962 1) listed; 261 of them are registered in our investigations: Genus Tracheloraphis Dragesco 1960 T. bimicronucleatus (Raikov 1969) Carey 1991 Philym Ciliophora Doflein 1901 T. discolor Raikov 1962 Subphylum Postciliodesmatophora Gerassimova et T. dogeili Raikov, 1957 Seravin 1976 T. drachi (Dragesco 1953) Dragesco 1960 1) Taxonomic scheme according to Lynn and Small T. hyalinum Dragesco 1960 (2000); symbol * species not registered in our investigations. T. kahli Raikov 1962 Protistology · 111
Table 1. Relative abundance (% of the total biomass) and variation coefficients (%) of the psammophilous ciliates in the estuary (average data on 1998 2000 years).
Stations Species 1 2 3 4 5 % CV % CV % CV % CV % CV Basic structure forming species with distinct preferences in terms of distribution along the estuary cluster 1 – station 1 and cluster 1а – stations 1 2 Coleps tesselatus 5.0 55 0.3 196 1.1 97 0.2 164 Histiobalantium majus 3.3 86 0.4 126 0.04 374 0.1 374 Gastrostyla pulchra 2.3 114 1.0 161 0.3 269 Trachelocerca incaudata 19.1 61 7.2 96 1.6 214 Histiobalantium marinum 15.3 68 9.5 62 3.6 139 2.7 230 0.9 170 Remanella granulose 0.11 191 Kentrophoros uninucleatus 0.06 176 Holosticha discocephalus 0.43 273 0.004 374 Oxytricha discifera 0.27 111 0.03 271 Pleuronema marina 1.38 57 0.22 161 Trichotaxis multimicronucleatus 0.40 138 0.16 262 0.03 374 Kentrophoros fasciolatum 0.30 93 0.26 138 0.003 374 Discocephalus rotatorius 1.12 90 0.34 172 0.05 270 Geleia fossata 1.55 78 0.22 231 0.01 374 Remanella rugosa 0.46 94 0.09 139 0.11 374 Frontonia elongata 0.21 148 0.24 137 0.05 374 Cinetochilum margaritaceum 0.20 178 0.02 179 0.01 270 0.01 374 Paradiophrys histrix 0.22 158 0.04 227 0.02 305 0.02 374 Enchelyodon sulcatum 1.90 92 0.90 129 0.60 190 0.80 231 0.10 374 Trachelocerca saggita 1.25 58 0.32 135 1.38 102 0.30 224 0.02 374 Strombidium sulcatum 0.70 201 0.68 238 0.26 197 0.20 254 0.02 374 cluster 2 – station 2 Remanella margaritifera 12.4 96 27.1 73 0.5 185 0.1 321 Trachelocercidae gen.sp. 2.5 70 9.2 79 1.2 88 1.7 192 0.1 254 Tracheloraphis kahli 1.0 89 5.5 94 0.5 169 Frontonia microstoma 0.05 256 3.0 181 0.7 238 0.5 180 Tracheloraphis phoenicopterus 0.8 77 1.3 120 0.2 322 Tracheloraphis oligostriata 0.3 79 1.5 127 0.02 374 0.06 374 Urostrongylum caudatum 0.9 92 1.6 88 0.3 252 0.1 254 0.1 214 Tracheloraphis dogieli 0.25 180 Anigsteinia salinarium 0.01 270 0.7 244 0.2 240 0.2 224 Frontonia fusca 0.01 224 0.14 200 0.05 299 0.05 374 0.05 374 Chilodonella uncinata 0.004 256 0.03 118 cluster 3 – station 3 Cardiostomatella vermiforme 11.6 63 13.1 65 33.1 116 3.3 275 0.9 289 Frontonia tchibisovae 0.4 149 0.4 341 10.3 128 7.4 211 0.6 176 Sonderia vorax 0.1 148 0.7 82 3.1 131 4.5 192 0.4 157 Diophrys scutum 0.8 68 0.4 153 8.3 171 0.4 252 1.4 237 Spathidium procerum 0.4 180 3.3 72 0.9 214 1.0 224 Uronychia transfuga 0.10 160 0.17 210 0.24 142 0.14 239 0.12 224 clusters 4, 4а and 4b stations 4 and 5 Pleuronema crassa 0.01 387 0.2 189 4.6 62 9.7 77 15.5 69 Prorodon morgani 0.8 251 0.5 303 4.7 139 8.6 174 13.8 133 Prorodon sp. 0.3 162 1.4 87 3.6 128 9.1 162 6.5 157 Cyclidium fuscum 0.1 151 0.4 107 1.2 116 8.3 73 8.0 54 Enchelydae gen.sp. 0.4 102 1.5 98 1.1 109 9.5 89 8.8 64 Oxytrichidae gen.sp. 0.4 97 0.3 162 0.7 189 3.9 121 6.2 88 Anigsteinia clarissimum 0.3 117 0.4 163 1.6 150 4.5 149 5.0 107 Urosoma caudate 0.3 199 3.1 181 4.4 118 Helicostoma notata 0.2 204 0.2 195 0.3 234 1.9 234 3.5 148 Uronema marina 0.43 105 0.25 137 0.57 105 0.78 136 1.65 66 Pleuronema coronata 0.67 95 0.43 121 0.32 147 0.90 233 1.73 154 Thrachelostyla caudata 0.51 84 0.74 105 1.00 121 0.95 241 1.49 188 Lacrymaria affinis 0.50 101 0.23 88 0.15 173 1.61 198 0.83 167 Lacrymaria cohni 0.08 156 0.03 262 0.01 224 0.69 224 0.81 84 Lacrymaria coronata 0.12 201 0.13 153 0.31 174 0.54 178 0.65 110 Uroleptus caudatus 0.13 106 0.02 224 0.19 185 0.06 374 0.48 299 Condylostoma curva 0.02 149 0.05 314 0.56 161 1.44 340 0.22 254 Glaucoma pyriformis 0.01 322 0.53 188 0.96 117 0.82 158
112 · Yuri A. Mazei and Igor V. Burkovsky
Table 1. (Continuation). Stations Species 1 2 3 4 5 % CV % CV % CV % CV % CV Paraurostyla dispar 0.01 374 1.50 208 1.60 196 1.49 119 Oxytricha marina 0.02 188 0.3 116 0.9 125 1.4 142 Spirostomum teres 1.25 174 0.85 188 1.79 137 Caenomorpha capucina 0.18 201 0.04 303 Metopus setosus 0.19 139 0.11 374 Species widely distributed along the estuary and appearing at different stations in different years Chlamydodon triquetrus 0.09 224 0.07 105 0.09 374 Euplotes balteatus 0.01 148 0.09 101 0.05 124 Loxophyllum verrucosum 0.03 148 0.04 91 0.02 137 Condylostoma remanei 0.12 282 0.16 168 0.22 283 0.11 254 Diophrys appendiculata 0.18 104 0.05 269 0.04 289 0.15 263 Euplotes moebiusi 0.05 132 0.05 289 0.03 226 0.28 238 Holosticha diademata 0.04 170 0.01 214 0.13 130 0.06 199 Loxophyllum laevigatum 0.01 387 0.01 374 0.06 374 0.35 374 Oxytricha ovalis 0.05 298 0.03 254 0.04 270 0.04 374 Paraspatidium fuscum 0.60 119 0.41 374 0.05 374 0.45 374 Placus striatus 0.07 175 0.03 374 0.03 374 Plagiopyla ovata 0.04 164 0.01 270 0.003 374 0.03 199 Tracheloraphis margaritata 0.10 126 0.05 374 0.04 224 0.71 245 Enchelyodon sp. 2.37 61 1.07 102 0.35 128 0.70 197 2.27 332 Trachelostyla pediculiforme 0.60 132 0.33 130 0.21 130 0.10 151 0.47 161 Euplotes trisulcatus 0.04 116 0.05 178 0.01 204 0.09 225 0.01 254 Mesodinium pulex 0.12 128 0.05 102 0.02 219 0.03 207 0.53 161 Aspidisca fusca 0.05 153 0.04 131 0.06 139 0.01 254 0.18 120 Aspidisca steini 0.02 225 0.03 114 0.01 149 0.04 224 0.01 374 Didinium balbiani 0.81 104 0.31 172 0.47 118 0.35 187 1.31 202 Frontonia marisalbi 0.66 133 1.10 162 0.47 228 0.14 374 0.59 224 Lacrymaria marina 0.11 102 0.18 172 0.16 245 0.13 332 0.07 177 Lacrymaria caudate 0.005 374 0.08 252 0.15 169 0.32 187 0.16 203 Lacrymaria conifera 0.11 69 0.11 121 0.06 135 0.15 118 0.39 97 Lacrymaria acuta 0.04 254 0.03 299 0.03 128 0.16 200 Strombidium sp. 0.001 400 0.29 157 0.05 374 0.69 235 Rare species sporadically occurring in the community Lacrymaria kahli 0.02 207 Lacrymaria lagenula 0.02 235 Lacrymaria multinucleata 0.08 117 Lagynophrya halophila 0.02 172 Lagynophrya maxima 0.003 374 Litonotus filium 0.003 231 Euplotes sp. 0.02 82 Geleia sp. 0.05 162 Chaenea vorax 0.03 236 Helicoprorodon sp. 0.02 250 Loxophillum variabilis 0.003 231 Epiclintes felis 0.08 285 0.03 374 Aspidisca psammobiotica 0.02 159 0.01 254 Kentrophoros latum 0.04 124 0.05 374 Lacrymaria ovata 0.01 325 0.003 374 Litonotus pictus 0.003 273 0.003 374 Remanella brunnea 0.04 374 0.01 374 Holosticha kessleri 0.18 64 0.01 209 0.02 177 Tracheloraphis drachi 0.17 43 0.07 224 Ophryoglena marina 0.004 400 0.03 270 Loxophyllum asetosum 0.01 199 Pseudopropodon sp. 0.11 181 Holosticha extensa 0.004 374 Condylostoma rugosa 0.01 374 Loxophillum lanceolatum 0.01 270 Coleps pulcher 0.03 149 Thuricola sp. 0.002 374 Chilodonella psammophila 0.04 219 0.3 265 0.03 374 Chilodontopsis simplex 0.10 289 Coleps hirtus 0.41 182
Protistology · 113
Table 1. (Continuation). Stations Species 1 2 3 4 5 % CV % CV % CV % CV % CV Dileptus tronquideus 0.02 374 Dileptus monilatus 0.001 400 Spirostomum intermedium 0.001 400 Stentor polymorphus 0.001 400 Oxytrich bifaria 0.001 400 Spathidium simplex 0.001 400
Notes: СV – variation coefficients, %. Relative abundances of the dominant species (constituting more than 2% of the total community biomass) are marked in bold print.
T. longicollis (Dragesco 1960) Foissner et Drages G. nigriceps (Kahl 1933) Dragesco 1960 co 1996 (Syn. Trachelonema longicollis Dragesco 1960) G. orbis Faure Fremiet 1950 T. margaritata Kahl 1930 G. simplex Faure Fremiet 1951 T. oligostriata Foissner et Dragesco 1960 (Syn. Incertae sedis in Class Karyorelictea Trachelonema oligostriata Raikov 1962) Genus Ciliofaurea Dragesco 1960 T. phoenicopterus (Cohn 1866) Dragesco 1960 C. arenicola Dragesco 1953 T. prenanti Dragesco 1960 Class Heterotrichea Stein 1859 T. teissieri Dragesco 1960 Order Heterotrichida Stein 1859 T. vermiformis Raikov 1962 Family Blepharismidae Jankovsky in Small et Lynn Genus Trachelonema Dragesco 1960 1985 T. grassei Dragesco 1960 Genus Anigstenia Perty 1849 T. lanceolata Raikov 1962 A. clarissimum (Anigstein 1912) Isquith 1968 Family Trachelocercidae Kent 1881 A. salinarum Florentin 1899 Genus Trachelоcerca Ehrenberg 1833 Family Climacostomidae Repak 1972 T. coluber Kahl 1933 Genus Climacostomum Stein 1867 T. incaudata (Kahl 1933) Foissner 1996 (Syn. C. virens (Ehrenberg 1933) Kahl 1930 5 Tracheloraphis incaudatus Kahl 1933) Family Condylostomatidae Kahl in Doflein et T. minor Gruber 1887 Reichenow 1929 *T. schulzei Dragesco 1954 Genus Condylostoma Bory St Vincent 1826 T. sagitta (Mzller 1786) Foissner et Dragesco C. arenarium Spiegel 1926 1996 (Syn. Tracheloraphis striata Raikov 1962) C. curva Burkovsky 1970 T. tenuicollis Quennerstedt 1867 C. patens Dujardin 1841 Order Loxodida Jankovski 1980 C. remanei (Spiegel 1928) Kahl 1930 5 Family Cryptopharyngidae Jankowski 1980 C. rugosa Kahl 1930 5 Genus Cryptopharynx Kahl 1930 Family Peritromidae Stein, 1867 C. setigerus Kahl 1928 Genus Peritromus Stein 1862 Family Loxodidae Butchli 1889 P. faurei Kahl 1930 5 Genus Remanella Kahl 1933 Family Spirostomidae Stein 1867 R. brunnea Kahl 1933 Genus Spirostomum Ehrenberg 1833 R. granulosa (Kahl 1933) Dragesco, 1960 S. intermedium Kahl 1930 5 R. margaritifera (Kahl 1933) Dragesco, 1960 S. teres Claparede et Lachmann 1859 R. multinucleata Kahl 1930 Genus Gruberia Kahl 1932 R. rugosa (Kahl 1933) Dragesco 1960 G. lanceolata (Gruber 1884) Kahl 1930 5 R. unicorpusculata (Kahl 1933) Dragesco 1965 G. uninucleata Kahl 1930 5 Order Protoheterotrichida Nouzarede 1977 Family Stentoridae Carus 1863 Family Geleiidae Kahl 1933 Genus Stentor Oken 1815 Genus Geleia Kahl 1933 S. polymorphus (Mzller 1773) Ehrenberg 1830 G. decolor (Kahl 1933) Dragesco 1960 Subphylum Intramacronucleata Lynn 1996 G. fossata (Kahl 1933) Dragesco 1960 Class Spirotrichea Butschli 1889 G. hyalina Dragesco 1960 Subclass Hypotrichia Stein 1859 G. major Dragesco 1960 Order Euplotida Small et Lynn 1985 G. murmanica Raikov 1962 Family Discocephalidae Jankowski 1979 114 · Yuri A. Mazei and Igor V. Burkovsky
Fig. 4. Distribution of the dominant ciliate species along the estuary.
Genus Discocephalus Ehrenberg 1831 Genus Aspidisca Ehrenberg 1838 D. ehrenbergi Dragesco 1960 A. dentata Kahl 1928 D. minimus Dragesco 1968 A. fusca Kahl 1928 D. rotatorius Ehrenberg 1831 A. irinae Burkovsky 1970 Genus Psammocephalus Wicklow 1982 A. lyncaster (Mzller 1773) Ehrenberg 1830 P. borrori Wicklow 1982 A. major (Madsen 1931) Kahl 1932 P. faurei (Dragesco 1963) Wicklow 1982 A. psammobiotica Burkovsky 1970 Family Aspidiscidae Ehrenberg 1838 A. sedigita Quennerstedt 1867 Protistology · 115
Fig. 5. Relationship between the number of samples taken (N) and the number of species recorded (S). A st. 1 5, 1998 2000 years, B st. 1, 2000, C st. 2, 2000, D st. 3, 2000, E st. 4, 2000, F st. 5, 2000.
A. steini Buddenbrock 1920 E. bisulcatus Kahl 1932 Genus Onychaspis Stein 1859 E. crassus (Dujardin 1841) Kahl 1932 *O. polystyla Stein 1859 E. cristatus Kahl 1932 Family Certesiidae Borror et Hill 1995 E. elegans Kahl 1932 Genus Certesia Fabre Domergue 1885 E. moebiusi Kahl 1932 C. quadrinucleata Fabre Domergue 1885 E. trisulcatus Kahl 1932 Family Euplotidae Ehrenberg 1838 E. zenkewitchi Burkovsky 1970 Genus Euplotes Ehrenberg 1830 Family Gastrocirrhidae Faure Fremiet 1961 E. baleatus (Dujardin 1841) Kahl 1932 Genus Euplotidium Noland 1937 E. balticus (Kahl 1935) Dragesco 1966 E. psammophilus (Vacelet 1961) Borror 1972 116 · Yuri A. Mazei and Igor V. Burkovsky
Family Uronychiidae Jankowski 1979 Family Urostylidae Bztschli 1889 Genus Diophrys Dujardin 1841 Genus Holosticha Wrzesnioski 1887 D. appendiculata (Ehrenberg 1838) Kahl 1932 H. diademata (Rees 1884) Kahl 1932 D. irmgard Mansfeld 1923 H. discocephalus Kahl 1932 D. kahli Dragesco 1963 H. kessleri (Wrzesnioski 1877) Kahl 1932 D. scutum Dujardin 1841 H. fasciola Kahl 1932 Genus Paradiophrys Foissner 1996 H. extensa Kahl 1932 P. histix (Buddenbrock 1920) Foissner 1996 H. manca Kahl 1932 Genus Uronychia Stein 1859 H. simplicis Wang et Nie 1932 U. setigera Calkinsi 1902 Genus Trichotaxis Stokes 1891 U. transfuga (Mzller 1786) Stein 1859 T. multinucleatus Burkovsky 1970 Subclass Stichotrichia Small et Lynn 1985 Genus Urostyla Ehrenberg 1830 Order Stichotrichida Faure Fremiet 1961 U. marina Kahl 1930 Family Amphisiellidae Jankowski 1979 Genus Uroleptopsis Kahl 1932 Genus Amphisiella Gourett et Roeser 1888 U. viridis (Perejaslawzewa 1885) Kahl 1932 A. milnei Kahl 1935 Genus Uroleptus Ehrenberg 1831 Genus Gastrostyla Englemann 1862 U. caudatus (Claparede et Lachmann 1858) G. pulchra Perejaslawzewa 1886 Kahl 1932 Genus Psammomitra Borror 1972 Subclass Oligotrichia Bztschli 1887 P. brevicaudata (Kahl 1933) Borror 1972 Order Stombidiida Petz et Foissner 1992 Family Epiclintidae Wicklow et Borror 1990 Family Strombidiidae Faure Fremiet 1970 Genus Epiclintes Stein 1862 Genus Strombidium Claparede et Lachmann 1858 E. felis (Muller 1786) Carey et Tatchell 1983 S. calkinsi Faure Fremiet 1932 Family Kahliellidae Tuffrau, 1979 S. coronatum (Leegard 1915) Kahl 1932 Genus Kahliella (Horvath 1932) Corliss 1960 S. conicum (Lohmann 1908) Wulff 1919 K. costata (Kahl 1932) Corliss 1960 S. latum Kahl 1932 Genus Paraurostyla Borror 1972 *S. longipes (Meunier 1910) Kahl 1932 P. gibba (Kahl 1932) Borror 1972 S. sauerbreyae (Sauerbrey 1928) Kahl 1932 P. dispar (Kahl 1932) Borror 1972 S. sulcatum Claparede et Lachmann 1858 Family Keronidae Dujardin 1840 S. typicum (Lankester 1874) Bztschli 1889 Genus Keronopsis Penard 1922 S. viridae Stein 1867 K. multinucleatus Maupas 1883 Insertae sedis in Class Spirotrichea K. ovalis Kahl 1932 Order Armophorida Jankowksi 1964 K. rubra (Ehrenberg 1838) Kahl 1932 Family Caenomorphidae Poche 1913 Genus Paraholosticha Kahl 1932 Genus Caenomorpha Perty 1852 P. polychaeta Borror 1966 C. capucina Kahl 1930 5 Family Spirofilidae von Gelei 1929 Family Metopidae Kahl 1927 Genus Urostrongylum Kahl 1935 Genus Metopus Claparede et Lachmann 1858 U. caudatum Kahl 1935 *M. contortus (Quennerstedt 1867) Kahl 1932 Order Sporadotrichina Faure Fremiet 1961 M. halophila Kahl 1925 Family Oxytrichidae Ehrenberg 1838 M. pellitus (Kahl 1932) Carey 1994 Genus Opisthotricha Kent 1880 2 M. setosus Kahl 1927 O. ovata Kahl 1935 Class Litostomatea Small et Lynn 1981 Genus Oxytricha Bory St. Vincent 1826 Subclass Haptoria Corliss 1974 O. bifaria Stokes 1887 Order Cyclotrichida Jankowski 1980 O. discifera Kahl 1932 Family Mesodiniidae Jankowski 1980 O. marina Kahl 1932 Genus Askenasia Blochmann 1895 O. ovalis Kahl 1932 A. stellaris (Leegaad 1920) Kahl 1930 Genus Urosoma Kowalewski 1882 Genus Mesodinium Stein 1862 U. caudata Stokes 1887 M. acarus Stein,1862 Family Trachelostylidae Small et Lynn 1985 M. pulex (Claparede et Lachmann 1858) Kahl 1930 Genus Trachelostyla Kahl 1932 M. pulex var. pupula Kahl 1933 T. caudata (Kahl 1932) Maeda et Garey 1984 Order Haptorida Corliss 1974 T. pediculiformis (Kahl 1932) Maeda et Carey 1984 Family Didiniidae Poche 1913 Order Urostylida Jankowski 1979 Genus Cyclotrichium Meunier 1910 Protistology · 117
C. cyclokaryon Meunier 1910 Genus Amphileptus Ehrenberg 1830 C. sphaericum Faure Fremiet 1924 A. filum Gruder 1888 Genus Didinium Stein 1859 Genus Litonotus Wrzesnioski 1870 D. balbiani Kahl 1933 L. anguilla Kahl 1930 Family Helicoprorodontidae Small et Lynn 1985 L. fusidens Kahl 1926 Genus Helicoprorodon Faure Fremiet 1950 *L. fasciola (Mzller 1786) Wrzesniowski 1870 H. gigas (Kahl 1933) Faure Fremiet 1950 L. lamella (Ehrenberg 1838) Schewiakoff 1896 H. minutus Bock 1952 L. pictus Kahl 1931 H. multinucleatum Dragesco 1960 L. salmica Burkovsky 1970 Family Lacrymariidae de Fromentel 1876 Genus Loxophyllum Dujardin 1841 Genus Lacrymaria Bory 1826 L. asetosum Burkovsky 1970 L. acuta Kahl 1933 L. fasciolatum Kahl 1933 L. affinis Docr 1952 L. helus Stokes 1884 L. caudata (Kahl 1933) Dragesco 1960 L. levigatum (Sauerdrey 1928) Dragesco 1960 L. cohni Kent 1880 2 L. lanceolatum (Dragesco 1954) Dragesco 1960 L. conifera Burkovsky 1970 L. multiplicatum Kahl 1931 L. coronata Claparede et Lachmann 1858 L. multiverrucosum (Kahl 1933) Carey 1994 L. kahli (Dragesco 1954) Dragesco 1960 L. niemeccense (Stein 1859) Kahl 1931 L. lagenula Claparede et Lachmann 1858 L. schewiakoffi Burkovsky 1970 L. marina Kahl 1927 L. setigerum Quennerstedt 1868 L. metabolica Burger 1908 L. soliforme Faure Fremiet 1951 L. minima Kahl 1928 L. trinucleatum Manfeld 1924 L. multinucleata Dragesco 1960 L. undulatum Sauerbrey 1928 L. ovata Burkovsky 1970 L. uninucleatum Kahl 1930 L. salinarum Kahl 1928 L. variabilis Dragesco 1954 Family Spathidiidae Kahl in Doflein et Reichenow L. vermiforme Sauerbrey 1928 1929 L. verrucosum (Stokes 1893) Dragesco 1965 Genus Perispira Stein 1859 Class Phyllopharyngea de Puytorac et al. 1974 P. stephosoma Stokes 1886 Subclass Phyllopharyngia de Puytorac et al. 1974 Genus Spathidium Dujardin 1841 Order Chlamydodontida Deroux 1976 S. curvatum Kahl 1928 Family Chilodonellidae Deroux 1970 S. fossicola Kahl 1933 Genus Chilodonella Strand 1928 S. procerum Kahl 1930 Ch. psammophila Dragesco 1960 S. simplex (Pennard 1922) Kahl 1930 Ch. uncinata (Ehrenberg 1835) Kahl 1931 Family Tracheliidae Ehrenberg 1838 Family Chlamydodontidae Stein 1859 Genus Dileptus Dujardin 1840 Genus Chlamydodon Ehrenberg 1835 D. marinus Kahl 1933 Ch. cyclops Entz 1884 D. monilatus (Stokes 1886) Kahl 1931 Ch. major (Kahl 1931) Carey 1994 D. tronquideus Dragesco 1960 Ch. mnemosine Ehrenberg 1835 Family Trachelophyllidae Kent 1882 Ch. obliquus Kahl 1931 Genus Chaenea Quennerstedt 1867 Ch. triquetrus (Mzller 1886) Dragesco 1960 Ch. elongata Kahl 1926 Order Dysteriida Deroux 1976 Ch. robusta Kahl 1930 Family Dysteriidae Claparede et Lachmann 1858 Ch. psammophila Dragesco 1960 Genus Dysteria Huxley 1857 Genus Enchelyodon Claparede et Lachmann 1859 D. monostyla (Ehrenberg 1838) Kahl 1931 E. sulcatus Kahl 1930 Genus Trochilia Dujardin 1841 Genus Lagynophrya Kahl 1930 *T. sigmoides Dujardin 1841 L. halophila Kahl 1930 Class Nassophorea Small et Lynn 1981 L. maxima Burkovsky 1970 Order Synhymeniida de Puytorac et al. 1974 Genus Trachelophyllum Claparede et Lachmann Family Scaphidiodontidae Deroux 1978 1859 Genus Chilodontopsis Blochmann 1895 T. apiculatum (Perty 1852) Claparede et Lach Ch. vorax (Stokes 1886) Kahl 1931 mann 1859 Ch. elongata (Kahl 1933) Dragesco 1960 Order Pleurostomatida Schewiakoff 1896 Ch. simplex Ozaki et Yagiu 1941 Family Amphileptidae Bztschli 1889 Order Microthoracida Jankowski 1967 118 · Yuri A. Mazei and Igor V. Burkovsky
Family Microthoracidae Wrzesniowski 1870 F. arenaria Kahl 1933 Genus Leptopharynx Mermod 1914 F. elongata Burkovsky 1970 L. torpens Kahl 1931 F. fusca Quennerstedt 1869 Genus Microthorax Englemann 1892 *F. leucas Ehrenberg 1833 M. sulcatus Englemann 1862 F. marina Fabre Domergue 1891 Class Colpodea Small et Lynn 1981 F. maris albi Burkovsky 1970 Order Cyrtolophosidida Foissner 1978 F. microstomata Kahl 1931 Family Woodruffiidae von Gelei 1954 F. tchibisovae Burkovsky 1970 Genus Woodruffia Kahl 1931 Family Parameciidae Dujardin 1840 W. rostrata Kahl 1931 Genus Paramecium Muller 1773 Class Prostomatida Schewiakoff 1896 P. calkinsi Woodruff 1921 Order Prorodontida Corliss 1974 *P. duboscqui Chatton et Brachon 1933 Family Colepidae Ehrenberg 1838 *P. nephridiatum Gelei 1925 Genus Coleps Nitzsch 1827 *P. woodruffi Wenrich 1928 C. hirtus Nitzsch 1817 Subclass Scuticociliatia Small 1967 C. pulcher Spiegel 1926 Order Philasterida Small 1967 C. similis Kahl 1933 Family Cinetochilidae Perty 1852 C. spiralis Noland 1937 Genus Cinetochilium Perty 1852 C. tesselatus Kahl 1930 C. margaritaceum Perty 1852 Genus Plagiopogon Stein 1859 C. marinum Kahl 1931 P. loricatus Kahl 1933 Family Cohnilembidae Kahl 1933 Family Holophryidae Perty 1852 Genus Cohnilembus Kahl 1933 Genus Holophrya Ehrenberg 1831 C. pusillus (Quennerstedt 1869) Kahl 1931 H. biconica Sauerbrey 1928 Family Loxocephalidae Jankowski 1964 Family Placidae Small et Lynn 1985 Genus Cardiostomatella Corliss 1960 Genus Spathidiopsis Fabre Domergue 1889 C. vermiforme (Kahl 1928) Corliss 1960 S. dogieli (Burkovsky 1970) Corliss 1979 Family Philasteridae Kahl 1931 S. striatus (Cohn 1866) Corliss 1979 Genus Helicostoma Cohn 1866 S. sulcatus (Mansfeld 1923) Corliss 1979 H. buddenbrocki Kahl 1931 Family Prorodontidae Kent 1880 2 H. notatum Kahl 1931 Genus Prorodon Ehrenberg 1833 H. oblogum Cohn 1866 P. binucleatus Dragesco 1965 Family Uronematidae Thompson 1964 *P. discolor Ehrenberg 1831 Genus Uronema Dujardin 1841 P. dubius Kahl 1930 U. marinum Dujardin 1841 P. lemani Dragesco 1965 Order Pleuronematida Faure Fremiet in Corliss 1956 P. marinus Claparede et Lachmann 1858 Family Cyclidiiidae Ehrenberg 1838 P. morgani Kahl 1930 Genus Cristigera Roux 1899 P. teres Ehrenberg 1838 C. minuta Kahl 1928 Genus Pseudoprorodon Blochmann 1886 C. setosa Kahl 1928 P. arenicola Kahl 1933 Genus Cyclidium Muller 1786 P. mononucleatus Bock 1952 C. candens Kahl 1928 Class Plagyopylea Small et Lynn 1985 C. fuscum Kahl 1928 Order Plagiopylida Small et Lynn 1985 C. marinum Borror 1963 Family Plagiopylidae Schewiakoff 1896 C. velliferum Kahl 1933 Genus Plagiopyla Stein 1860 Family Histibalantiidae de Puytorac et Corliss in P. marina Kahl 1933 Corliss 1979 P. ovata Kahl 1931 Genus Histiobalantium Stokes 1886 Family Sonderiidae Small et Lynn 1985 H. majus Kahl 1931 Genus Sonderia Kahl 1928 H. marinum Kahl 1933 S. vorax Kahl 1928 Family Pleuronematidae Kent 1880 2 Class Oligohymenophorea de Puytorac et al. 1974 Genus Pleuronema Dujardin 1836 Subclass Peniculia Faure Fremiet in Corliss 1956 *P. chrysalis (Muller 1786) Perty 1852 Order Peniculida Faure Fremiet in Corliss 1956 P. coronata Kent 1880 2 Family Frontoniidae Kahl 1926 P. crassa Dujardin 1836 Genus Frontonia Ehrenberg 1838 P. marina Dujardin 1841 Protistology · 119
P. setigera Calkins 1902 References P. simplex Dragesco 1960 Subclass Hymenostomatia Delage et Herouard 1896 Agamaliev F.G. 1983. Ciliates of the Caspian Sea: Order Hymenostomatida Delage et Herouard 1896 Systematics, ecology, zoogeography. Nauka, Leningrad. Family Glaucomidae Corliss 1971 (in Russian). Genus Glaucoma Ehrenberg 1830 Alekperov I. H. and Asadullaeva E.S. 1996. New G. pyriformis (Ehrenberg 1838) Maupas 1883 and rare ciliates of Absheron coast of the Caspian Sea. Family Ophryoglenidae Kent 1880 2 Zool. Zh. 75, 5, 763 769 (in Russian with English sum Genus Ophryoglena Ehrenberg 1831 mary). O. macrostoma Kahl 1928 Azovsky A.I. and Mazei Yu.A. 2003. Conspectus O. marina Burkovsky 1970 of the Black Sea fauna of the benthic ciliates. Protistology. Insertae sedis in Phylum Ciliophora 3, 2, 72 91. Family Coelosomidiidae Corliss 1961 Burkovsky I.V. 1970a. The ciliates of the meso Genus Coelosomides Strand 1928 psammon of the Kandalaksha Gulf (White Sea). I. Acta C. vermiformis Burkovsky 1970 Protozool. 7, 475 489 (in Russian with English Genus Paraspathidium Noland 1937 summary). P. fuscum (Kahl 1928) Dragesco 1960 Burkovsky I.V. 1970b. The ciliates of the meso P. obliquum Dragesco 1960 psammon of the Kandalaksha Gulf (White Sea). II. Acta Protozool. 8, 47 65 (in Russian with English Total species richness recorded in the White Sea summary). (273 species) is much lower than in such relatively well Burkovsky I.V. 1970c. The ciliates of sandy littoral studied seas as the Caspian (351 species, Agamaliev, and sublittoral of the Kandalaksha Gulf (White Sea) 1983; Alekperov and Asadullaeva, 1996), the Baltic (318 and analysis of the data of benthic ciliate fauna other species, Agamaliev, 1983) and the Black Sea (about 450 seas. Acta Protozool. 8, 183 201 (in Russian with species, Azovsky and Mazei, 2003). This fact may be English summary). considered as surprising, taking into account the long Burkovsky I.V. 1976. The ciliates of freshened parts history of ciliatological studies at the White Sea. of the White Sea. Zool. Zh. 55, 2, 287 289 (in Russian However, an overwhelming majority of investigations with English summary). was conducted in a restricted geographical region (in Burkovsky I.V. 1984. The ecology of free living the Kandalaksha Bay), where scientific centres are ciliates. Moscow State Univ. Press, Moscow (in Russian). concentrated. At the same time, it has been noted that Burkovsky I.V. 1992. Structural and functional differences between regions within seas may be organisation and stability of marine benthic communities. significant, exploration of new regions yielding a great Moscow State Univ. Press, Moscow (in Russian). increase in the total species number (Azovsky and Burkovsky I.V. and Mazei Yu.A. 2001. Ciliate Mazei, 2003). community structure in the zone of mixing sea and river Species/genera (S/G) ratio for the White Sea fauna waters. Entomol. Rev. 81, Suppl. 1, 7 16. as a whole is 2.91. It is rather low as compared with Burkovsky I.V. and Stolyarov A.P. 1995. Characte other relatively well studied seas (Caspian 3.36; Black ristic features of the structural organization of macro 3.24; Baltic 2.89; North Atlantic 3.33; Azovsky benthos in a biotope with a pronounced salinity gradient. and Mazei, 2003), indicating that less congeners Zool. Zh. 74, 2, 32 46 (in Russian with English sum constitute the White Sea fauna. The largest genera are mary). Loxophyllum (17 species), Lacrymaria (15), Trachelo Carey P. 1991. Marine interstitial ciliates. An illu raphis (13), Euplotes (9), Strombidium (9), Geleia (8), strated key. Brit. Mus. Nat. Hist. London. Aspidisca (8), Frontonia (8). They form 31.5% of the Fenchel T., Esteban G.F. and Finlay B. 1997. Local total species richness of the region and only 8.4% of versus global diversity of microorganisms: cryptic the genera richness. On the other hand, there are 43 diversity of ciliated protozoa. Oikos. 80, 220 225. single species genera (15.6% of species richness and Finlay B.J. 1998. The global diversity of protozoa 45.3% of genera richness). and other small species. Int. J. Parasitol. 28, 29 48. Finlay B.J. and Esteban G.F. 1998. Planktonic ciliate species diversity as an integral component of ecosystem function in a freshwater pond. Protist. 149, ACKNOWLEDGEMENTS 155 165. The work was supported by the Russian Foundation Finlay B.J, Maberly S.C. and Cooper J.I. 1997. for Basic Research, grants № 02 04 48002 and № 04 Microbial diversity and ecosystem function. Oikos. 80, 04 48338. 209 213. 120· Yuri A. Mazei and Igor V. Burkovsky
Foissner W. 1991. Basic light and scanning electron structure in the White Sea estuary. Dev. Curr. Biol. 122, microscopic methods for taxonomic studies of ciliated 2, 183 189 (in Russian with English summary). Protozoa. Eur. J. Protistol. 27, 4, 210 223. Mazei Yu.A., Burkovsky I.V. and Stolyarov A.P. Fokin S. 2001. Species list of free living invertebrates 2002. Salinity as a factor of ciliate community forming of Eurasian seas and adjacent deep water parts of the (colonization experiments). Zool. Zh. 81, 4, 387 393 Arctic. In: Investigations of the sea fauna. 51 (59). Zool. (in Russian with English summary). Inst RAS, Saint Petersburg. pp. 21 28. Petz W. and Foissner W. 1988. Spatial separation Khlebovitch V.V. 1974. Critical salinity of biological of terrestrial ciliates and testaceans (Protozoa): a processes. Nauka, Leningrad (in Russian). contribution to soil ciliatostasis. Acta Protozool. 27, 3/ Lynn D.H. and Small E.B. 2000. Phylum Ciliophora. 4, 249 258. In: An illustrated guide to the Protozoa, 2nd ed. (Eds. Safianov G.A. 1987. The estuaries. Mysl', Moscow Lee J.J., Leedale G.F. and Bradbury Ph.). Society of (in Russian). Protozoologists, Lawrence. pp. 371 656. Mazei Yu.A. and Burkovsky I.V. 2002. Spatial and temporal changes of psammophilous ciliate community
Address for correspondence: Yuri A. Mazei. Department of Ecology, Penza State Pedagogical University, Penza, 440026, Russia. E mail: [email protected]
Editorial responsibility: Sergei Fokin