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
Protozoan communities in estuaries are formed under the influence of a complex of factors. Among them salinity is of the greatest importance (Mazei et al., 2002). Moreover, great environmental variability
and critical salinity level (3-8 %c) cause lower community complexity in estuaries as compared with communities in other biotopes (Khlebovitch, 1974; Safianov, 1987; Burkovsky and Stoljarov, 1995; Burkovsky and Mazei, 2001). However, species richness may achieve high levels due to complex interactions
© 2005 by Russia, Protistology
between active and passive species diversity and environmental factors.
The aim of this study is to describe species composition 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 ofbenthic ciliates of the White Sea.
Material and Methods
Investigations were conducted during 1998-2000 summer periods in the Chernaya river estuary (the Kandalaksha Bay, the White Sea). Material was collected at 5 permanent stations. The stations were located at the middle horizon of the intertidal zone along the estuary (Fig. 1). A detailed hydrological and hydrochemical characteristic of the stations was given in a previous article (Burkovsky and Mazei, 2001).
Each station was a strictly fixed sampling area 50 x 50 cm, where recordings of the ciliate abundance were performed. Extraction and quantitative counting of ciliates were performed on live individuals (Carey,
1991). The ciliates were identified on the Shatton-Lwoff silver-impregnated preparations (Foissner, 1991), according to Carey (1991).
Most of the species names are given following Carey (1991). The main results of recent revisions of Trache-locercidae, Kentrophoros and Metopus were also taken into account (see Azovsky and Mazei, 2003). The following species of Trachelocercidae already redescribed are given below in accordance with the newly rebuilt system and the synonymy arisen: Trachelocerca sagitta (Syn.: Tracheloraphis striata Raikov 1962), Trachelocerca incaudata (Syn.: Tracheloraphis incaudatus (Kahl 1933) Dragesco 1960), Tracheloraphis longicollis (Syn.: Trachelonema longicollis Dragesco 1960), Tracheloraphis oligostriata (Syn.: Trachelonemaoligostriata Raikov 1962).
To distinguish species groups with similar distribution along the estuary, the cluster analysis by complete linkage method on the basis of a matrix of Czsekanovsky similarity indices was performed. Calculations were conducted with the help of STATISTICA software package. To construct curves of dependence between the number of samples taken and the number of species observed, original software rendered by Dr. A.I. Azovsky (Moscow M.V. Lomonosov State University) was used.
Results and Discussion
Species composition of the estuarine community
Altogether, in the studied zones of the Chernaya river estuary 123 species of ciliates were found: st. 1 -
Fig. 1. A scheme of location of stations 1-5 in the estuary. Thick line - coastline, thin line - zero of depth.
100, st. 2 - 94, st. 3 - 87, st. 4 - 72, st. 5 - 59 species. As salinity decreases, the number ofspecies falls significantly. During one summer season only some of the species characteristic of a given biotope can be encountered, since many ciliates (about a half at every station) do not always get into the samples because of their low abundance.
From the total ciliate species diversity, species groups according to salinity gradient are distinguished with the aid of cluster analysis (Fig. 2). In different seasons 6-7 clusters are marked at the same similarity level. The trends of species' relative abundance changes along the estuary are represented in Fig. 3. Clusters 1 and 1a include marine stenohaline species occurring at the stations 1 and 2; clusters 2 and 3 are composed of marine euryhaline organisms from the stations 2 and 3 accordingly; clusters 4, 4a and 4b consist of brackish water ciliates, forming community at the stations 4 and 5. Quantitative data about all estuarine ciliates are given in table 1, where species are grouped in accordance to belonging to clusters reflecting their spatial distribution along the salinity gradient.
On the other hand, estuarine ciliate species may be grouped depending on the role played by ciliates in the community: 1) basic structure-forming species with distinct preferences in terms of distribution along the estuary, 2) species widely distributed along the estuary and appearing at different stations in different years, 3) rare ciliates sporadically occurring in the community (Table 1).
Annually, 23 dominating and 37 subdominating species compose the basis of the ciliate community in the estuary, which constitutes almost a half of the total species richness. These species occur constantly in samples and form the community "nucleus". In Fig. 4 distribution patterns of mass species (relatively constant structural components of the community) are given. The share of each of them at least at one of the 5 stations is about 5% of total biomass. However, their relative
Fig. 2. Results of the cluster analysis of the species based on species distribution similarity according to salinity gradient. 1-4b - clusters. A - 1998, B - 1999, C - 2000.
contribution into total abundance and biomass fluctuates from year to year and throughout the season (it is reflected in the corresponding indices of coefficient of variation - CV). As a rule, the most mass and typical for a given area species have the most stable abundance. Low values of CV indicate a higher correspondence of given conditions to the ciliates' environmental requirements, whereas high values, lower correspondence, thus characterising the preferendum zone for this or that species in the whole complex of natural factors.
Another part of the community is represented by accidental or very rare species (cryptic diversity -Fenchel et al., 1997), sporadically occurring at different stations during different seasons. At the same time, some of these species may contribute a significant part (up to 2%) into the total community biomass. However, in different seasons they may develop at extremely distant stations depending on abiotic and/or coenotic factors. Another part of the cryptic diversity consists of species with stable preferences in terms of location
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 ofconditions 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 3.55.8% of the total White Sea species richness constitute "active" diversity in a given microhabitat at a particular point in time.
In addition, in Fig. 5 relations between number of samples taken and number of species registered are represented. It is obvious that at all stations asymptotic level of species richness curve (i.e. species saturation) is observed. All curves are approximated by linear regression model in log-transformed data. Asymptotic value of species richness curve is proved by negative residuals occurring in the tail in the residuals vs. number of samples curve. In table
2 data representing the dependence between the set of samples taken and the number of species recorded is given. For revealing 90 % of total species richness it is necessary to take: a) 6-9 samples at a station in a given season, b) 13-19 samples at a station during three years, c) 23 samples at all stations in a given season and d) 41 samples at all stations during three years. In the marine part of the estuary species saturation comes faster than in the riverine one. On the other hand, increasing the number of the seasons investigated yields a greater (up to 1.3 times) species number at a given station. Increasing the number of stations within the estuary leads to the rise of species number up to 1.7 times. This indicates that spatial heterogeneity of the biotope causes a greater increase in species richness than temporal one.
Fig. 3. Distribution of ciliates' clusters in the estuary.
Total species list of the benthic ciliates of the White Sea
Total species list of the benthic ciliates of the White Sea was compiled on the basis of our long-term observations in the Velikaya Salma Strait and Chernaya river estuary (Burkovsky, 1970a, 1970b, 1970c, 1976, 1984,
1992), as well as literature sources (Fokin, 2001).
Altogether 273 ciliate species from 94 genera are listed; 261 of them are registered in our investigations: ^
Philym Ciliophora Doflein 1901
Subphylum Postciliodesmatophora Gerassimova et Seravin 1976
1) Taxonomic scheme according to Lynn and Small (2000); symbol * - species not registered in our investigations.
Class Karyorelictea Corliss 1974 Order Prostomatida Small et Lynn 1985 Family Kentrophoridae Jankowski 1980 Genus Kentrophoros Sauerbrey 1928 K. fasciolatus (Sauerbrey 1928) Dragesco 1960 K. gracilis Raikov 1963 K. grandis Dragesco 1954 K. latum Raikov 1962 K. uninucleatum Raikov 1962 Genus Tracheloraphis Dragesco 1960 T. bimicronucleatus (Raikov 1969) Carey 1991 T. discolor Raikov 1962 T. dogeili Raikov, 1957 T. drachi (Dragesco 1953) Dragesco 1960 T. hyalinum Dragesco 1960 T. kahli Raikov 1962
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 1a - 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, 4a 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
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
Table 1. (Continuation).
Stations
Species 1 2 3 4 5
% CV % CV % CV % CV % CV
Dileptus tronquideus Dileptus monilatus Spirostomum intermedium Stentor polymorphus Oxytrich bifaria Spathidium simplex 0.02 0.001 0.001 0.001 0.001 0.001 374 400 400 400 400 400
Notes: CV - 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-co 1996 (Syn. Trachelonema longicollis Dragesco 1960) T. margaritata Kahl 1930 T. oligostriata Foissner et Dragesco 1960 (Syn. Trachelonema oligostriata Raikov 1962)
T. phoenicopterus (Cohn 1866) Dragesco 1960 T. prenanti Dragesco 1960 T. teissieri Dragesco 1960 T. vermiformis Raikov 1962 Genus Trachelonema Dragesco 1960 T. grassei Dragesco 1960 T. lanceolata Raikov 1962 Family Trachelocercidae Kent 1881 Genus Trachelocerca Ehrenberg 1833 T. coluber Kahl 1933
T. incaudata (Kahl 1933) Foissner 1996 (Syn. Tracheloraphis incaudatus Kahl 1933)
T. minor Gruber 1887 *T. schulzei Dragesco 1954 T. sagitta (Muller 1786) Foissner et Dragesco 1996 (Syn. Tracheloraphis striata Raikov 1962)
T. tenuicollis Quennerstedt 1867 Order Loxodida Jankovski 1980 Family Cryptopharyngidae Jankowski 1980 Genus Cryptopharynx Kahl 1930
C. setigerus Kahl 1928 Family Loxodidae Butchli 1889 Genus Remanella Kahl 1933 R. brunnea Kahl 1933 R. granulosa (Kahl 1933) Dragesco, 1960 R. margaritifera (Kahl 1933) Dragesco, 1960 R. multinucleata Kahl 1930 R. rugosa (Kahl 1933) Dragesco 1960 R. unicorpusculata (Kahl 1933) Dragesco 1965 Order Protoheterotrichida Nouzarede 1977 Family Geleiidae Kahl 1933 Genus Geleia Kahl 1933
G. decolor (Kahl 1933) Dragesco 1960
G. fossata (Kahl 1933) Dragesco 1960
G. hyalina Dragesco 1960
G. major Dragesco 1960
G. murmanica Raikov 1962
G. nigriceps (Kahl 1933) Dragesco 1960
G. orbis Faure-Fremiet 1950
G. simplex Faure-Fremiet 1951 Incertae sedis in Class Karyorelictea Genus Ciliofaurea Dragesco 1960
C. arenicola Dragesco 1953 Class Heterotrichea Stein 1859 Order Heterotrichida Stein 1859 Family Blepharismidae Jankovsky in Small et Lynn 1985
Genus Anigstenia Perty 1849 A. clarissimum (Anigstein 1912) Isquith 1968 A. salinarum Florentin 1899 Family Climacostomidae Repak 1972 Genus Climacostomum Stein 1867
C. virens (Ehrenberg 1933) Kahl 1930-5 Family Condylostomatidae Kahl in Doflein et Reichenow 1929
Genus Condylostoma Bory St Vincent 1826
C. arenarium Spiegel 1926
C. curva Burkovsky 1970
C. patens Dujardin 1841
C. remanei (Spiegel 1928) Kahl 1930-5
C. rugosa Kahl 1930-5 Family Peritromidae Stein, 1867 Genus Peritromus Stein 1862 P. faurei Kahl 1930-5 Family Spirostomidae Stein 1867 Genus Spirostomum Ehrenberg 1833 S. intermedium Kahl 1930-5 S. teres Claparede et Lachmann 1859 Genus Gruberia Kahl 1932
G. lanceolata (Gruber 1884) Kahl 1930-5
G. uninucleata Kahl 1930-5 Family Stentoridae Carus 1863 Genus Stentor Oken 1815 S. polymorphus (Muller 1773) Ehrenberg 1830 Subphylum Intramacronucleata Lynn 1996 Class Spirotrichea Butschli 1889 Subclass Hypotrichia Stein 1859 Order Euplotida Small et Lynn 1985 Family Discocephalidae Jankowski 1979
Fig. 4. Distribution of the dominant ciliate species along the estuary.
Genus Discocephalus Ehrenberg 1831
D. ehrenbergi Dragesco 1960
D. minimus Dragesco 1968
D. rotatorius Ehrenberg 1831 Genus Psammocephalus Wicklow 1982 P. borrori Wicklow 1982 P. faurei (Dragesco 1963) Wicklow 1982 Family Aspidiscidae Ehrenberg 1838
Genus Aspidisca Ehrenberg 1838 A. dentata Kahl 1928 A. fusca Kahl 1928 A. irinae Burkovsky 1970 A. lyncaster (Mzller 1773) Ehrenberg 1830 A. major (Madsen 1931) Kahl 1932 A. psammobiotica Burkovsky 1970 A. sedigita Quennerstedt 1867
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 Genus Onychaspis Stein 1859
*O. polystyla Stein 1859 Family Certesiidae Borror et Hill 1995 Genus Certesia Fabre-Domergue 1885
C. quadrinucleata Fabre-Domergue 1885 Family Euplotidae Ehrenberg 1838 Genus Euplotes Ehrenberg 1830 E. baleatus (Dujardin 1841) Kahl 1932 E. balticus (Kahl 1935) Dragesco 1966
E. bisulcatus Kahl 1932 E. crassus (Dujardin 1841) Kahl 1932 E. cristatus Kahl 1932
E. elegans Kahl 1932
E. moebiusi Kahl 1932
E. trisulcatus Kahl 1932
E. zenkewitchi Burkovsky 1970 Family Gastrocirrhidae Faure-Fremiet 1961 Genus Euplotidium Noland 1937
E. psammophilus (Vacelet 1961) Borror 1972
Family Uronychiidae Jankowski 1979 Genus Diophrys Dujardin 1841 D. appendiculata (Ehrenberg 1838) Kahl 1932
D. irmgard Mansfeld 1923
D. kahli Dragesco 1963
D. scutum Dujardin 1841 Genus Paradiophrys Foissner 1996
P. histix (Buddenbrock 1920) Foissner 1996 Genus Uronychia Stein 1859 U. setigera Calkinsi 1902 U. transfuga (MMler 1786) Stein 1859 Subclass Stichotrichia Small et Lynn 1985 Order Stichotrichida Faure-Fremiet 1961 Family Amphisiellidae Jankowski 1979 Genus Amphisiella Gourett et Roeser 1888 A. milnei Kahl 1935 Genus Gastrostyla Englemann 1862
G. pulchra Perejaslawzewa 1886 Genus Psammomitra Borror 1972 P. brevicaudata (Kahl 1933) Borror 1972 Family Epiclintidae Wicklow et Borror 1990 Genus Epiclintes Stein 1862
E. felis (Muller 1786) Carey et Tatchell 1983 Family Kahliellidae Tuffrau, 1979
Genus Kahliella (Horvath 1932) Corliss 1960 K. costata (Kahl 1932) Corliss 1960 Genus Paraurostyla Borror 1972 P. gibba (Kahl 1932) Borror 1972 P. dispar (Kahl 1932) Borror 1972 Family Keronidae Dujardin 1840 Genus Keronopsis Penard 1922 K. multinucleatus Maupas 1883 K. ovalis Kahl 1932 K. rubra (Ehrenberg 1838) Kahl 1932 Genus Paraholosticha Kahl 1932 P. polychaeta Borror 1966 Family Spirofilidae von Gelei 1929 Genus Urostrongylum Kahl 1935 U. caudatum Kahl 1935 Order Sporadotrichina Faure-Fremiet 1961 Family Oxytrichidae Ehrenberg 1838 Genus Opisthotricha Kent 1880-2 O. ovata Kahl 1935 Genus Oxytricha Bory St. Vincent 1826 O. bifaria Stokes 1887 O. discifera Kahl 1932 O. marina Kahl 1932 O. ovalis Kahl 1932 Genus Urosoma Kowalewski 1882 U. caudata Stokes 1887 Family Trachelostylidae Small et Lynn 1985 Genus Trachelostyla Kahl 1932 T. caudata (Kahl 1932) Maeda et Garey 1984 T. pediculiformis (Kahl 1932) Maeda et Carey 1984 Order Urostylida Jankowski 1979
Family Urostylidae BMschli 1889 Genus Holosticha Wrzesnioski 1887 H. diademata (Rees 1884) Kahl 1932 H. discocephalus Kahl 1932 H. kessleri (Wrzesnioski 1877) Kahl 1932 H. fasciola Kahl 1932 H. extensa Kahl 1932
H. manca Kahl 1932
H. simplicis Wang et Nie 1932 Genus Trichotaxis Stokes 1891 T. multinucleatus Burkovsky 1970 Genus Urostyla Ehrenberg 1830 U. marina Kahl 1930 Genus Uroleptopsis Kahl 1932 U. viridis (Perejaslawzewa 1885) Kahl 1932 Genus Uroleptus Ehrenberg 1831 U. caudatus (Claparede et Lachmann 1858) Kahl 1932
Subclass Oligotrichia Bttschli 1887 Order Stombidiida Petz et Foissner 1992 Family Strombidiidae Faure-Fremiet 1970 Genus Strombidium Claparede et Lachmann 1858 S. calkinsi Faure-Fremiet 1932 S. coronatum (Leegard 1915) Kahl 1932 S. conicum (Lohmann 1908) Wulff 1919 S. latum Kahl 1932
*S. longipes (Meunier 1910) Kahl 1932 S. sauerbreyae (Sauerbrey 1928) Kahl 1932 S. sulcatum Claparede et Lachmann 1858 S. typicum (Lankester 1874) BMschli 1889 S. viridae Stein 1867 Insertae sedis in Class Spirotrichea Order Armophorida Jankowksi 1964 Family Caenomorphidae Poche 1913 Genus Caenomorpha Perty 1852
C. capucina Kahl 1930-5 Family Metopidae Kahl 1927 Genus Metopus Claparede et Lachmann 1858 *M. contortus (Quennerstedt 1867) Kahl 1932 M. halophila Kahl 1925 M. pellitus (Kahl 1932) Carey 1994 M. setosus Kahl 1927 Class Litostomatea Small et Lynn 1981 Subclass Haptoria Corliss 1974 Order Cyclotrichida Jankowski 1980 Family Mesodiniidae Jankowski 1980 Genus Askenasia Blochmann 1895 A. stellaris (Leegaad 1920) Kahl 1930 Genus Mesodinium Stein 1862 M. acarus Stein,1862
M. pulex (Claparede et Lachmann 1858) Kahl 1930 M. pulex var. pupula Kahl 1933 Order Haptorida Corliss 1974 Family Didiniidae Poche 1913 Genus Cyclotrichium Meunier 1910
C. cyclokaryon Meunier 1910
C. sphaericum Faure-Fremiet 1924 Genus Didinium Stein 1859
D. balbiani Kahl 1933 Family Helicoprorodontidae Small et Lynn 1985 Genus Helicoprorodon Faure-Fremiet 1950
H. gigas (Kahl 1933) Faure-Fremiet 1950
H. minutus Bock 1952
H. multinucleatum Dragesco 1960 Family Lacrymariidae de Fromentel 1876 Genus Lacrymaria Bory 1826 L. acuta Kahl 1933 L. affinis Docr 1952 L. caudata (Kahl 1933) Dragesco 1960 L. cohni Kent 1880-2 L. conifera Burkovsky 1970 L. coronata Claparede et Lachmann 1858 L. kahli (Dragesco 1954) Dragesco 1960 L. lagenula Claparede et Lachmann 1858 L. marina Kahl 1927 L. metabolica Burger 1908 L. minima Kahl 1928 L. multinucleata Dragesco 1960 L. ovata Burkovsky 1970 L. salinarum Kahl 1928 Family Spathidiidae Kahl in Doflein et Reichenow 1929
Genus Perispira Stein 1859 P. stephosoma Stokes 1886 Genus Spathidium Dujardin 1841 S. curvatum Kahl 1928 S. fossicola Kahl 1933 S. procerum Kahl 1930 S. simplex (Pennard 1922) Kahl 1930 Family Tracheliidae Ehrenberg 1838 Genus Dileptus Dujardin 1840
D. marinus Kahl 1933
D. monilatus (Stokes 1886) Kahl 1931
D. tronquideus Dragesco 1960 Family Trachelophyllidae Kent 1882
Genus Chaenea Quennerstedt 1867 Ch. elongata Kahl 1926 Ch. robusta Kahl 1930 Ch. psammophila Dragesco 1960 Genus Enchelyodon Claparede et Lachmann 1859
E. sulcatus Kahl 1930 Genus Lagynophrya Kahl 1930
L. halophila Kahl 1930 L. maxima Burkovsky 1970 Genus Trachelophyllum Claparede et Lachmann
1859
T. apiculatum (Perty 1852) Claparede et Lachmann 1859
Order Pleurostomatida Schewiakoff 1896 Family Amphileptidae BMschli 1889
Genus Amphileptus Ehrenberg 1830 A. filum Gruder 1888 Genus Litonotus Wrzesnioski 1870 L. anguilla Kahl 1930 L. fusidens Kahl 1926
*L. fasciola (MMler 1786) Wrzesniowski 1870 L. lamella (Ehrenberg 1838) Schewiakoff 1896 L. pictus Kahl 1931 L. salmica Burkovsky 1970 Genus Loxophyllum Dujardin 1841 L. asetosum Burkovsky 1970 L. fasciolatum Kahl 1933 L. helus Stokes 1884
L. levigatum (Sauerdrey 1928) Dragesco 1960 L. lanceolatum (Dragesco 1954) Dragesco 1960 L. multiplicatum Kahl 1931 L. multiverrucosum (Kahl 1933) Carey 1994 L. niemeccense (Stein 1859) Kahl 1931 L. schewiakoffi Burkovsky 1970 L. setigerum Quennerstedt 1868 L. soliforme Faure-Fremiet 1951 L. trinucleatum Manfeld 1924 L. undulatum Sauerbrey 1928 L. uninucleatum Kahl 1930 L. variabilis Dragesco 1954 L. vermiforme Sauerbrey 1928 L. verrucosum (Stokes 1893) Dragesco 1965 Class Phyllopharyngea de Puytorac et al. 1974 Subclass Phyllopharyngia de Puytorac et al. 1974 Order Chlamydodontida Deroux 1976 Family Chilodonellidae Deroux 1970 Genus Chilodonella Strand 1928 Ch. psammophila Dragesco 1960 Ch. uncinata (Ehrenberg 1835) Kahl 1931 Family Chlamydodontidae Stein 1859 Genus Chlamydodon Ehrenberg 1835 Ch. cyclops Entz 1884 Ch. major (Kahl 1931) Carey 1994 Ch. mnemosine Ehrenberg 1835 Ch. obliquus Kahl 1931 Ch. triquetrus (MMler 1886) Dragesco 1960 Order Dysteriida Deroux 1976 Family Dysteriidae Claparede et Lachmann 1858 Genus Dysteria Huxley 1857
D. monostyla (Ehrenberg 1838) Kahl 1931 Genus Trochilia Dujardin 1841 *T. sigmoides Dujardin 1841 Class Nassophorea Small et Lynn 1981 Order Synhymeniida de Puytorac et al. 1974 Family Scaphidiodontidae Deroux 1978 Genus Chilodontopsis Blochmann 1895 Ch. vorax (Stokes 1886) Kahl 1931 Ch. elongata (Kahl 1933) Dragesco 1960 Ch. simplex Ozaki et Yagiu 1941 Order Microthoracida Jankowski 1967
Family Microthoracidae Wrzesniowski 1870 Genus Leptopharynx Mermod 1914 L. torpens Kahl 1931 Genus Microthorax Englemann 1892 M. sulcatus Englemann 1862 Class Colpodea Small et Lynn 1981 Order Cyrtolophosidida Foissner 1978 Family Woodruffiidae von Gelei 1954 Genus Woodruffia Kahl 1931 W. rostrata Kahl 1931 Class Prostomatida Schewiakoff 1896 Order Prorodontida Corliss 1974 Family Colepidae Ehrenberg 1838 Genus Coleps Nitzsch 1827 C. hirtus Nitzsch 1817 C. pulcher Spiegel 1926 C. similis Kahl 1933 C. spiralis Noland 1937 C. tesselatus Kahl 1930 Genus Plagiopogon Stein 1859 P. loricatus Kahl 1933 Family Holophryidae Perty 1852 Genus Holophrya Ehrenberg 1831
H. biconica Sauerbrey 1928 Family Placidae Small et Lynn 1985 Genus Spathidiopsis Fabre-Domergue 1889 S. dogieli (Burkovsky 1970) Corliss 1979 S. striatus (Cohn 1866) Corliss 1979 S. sulcatus (Mansfeld 1923) Corliss 1979 Family Prorodontidae Kent 1880-2 Genus Prorodon Ehrenberg 1833 P. binucleatus Dragesco 1965 *P. discolor Ehrenberg 1831 P. dubius Kahl 1930 P. lemani Dragesco 1965 P. marinus Claparede et Lachmann 1858 P. morgani Kahl 1930 P. teres Ehrenberg 1838 Genus Pseudoprorodon Blochmann 1886 P. arenicola Kahl 1933 P. mononucleatus Bock 1952 Class Plagyopylea Small et Lynn 1985 Order Plagiopylida Small et Lynn 1985 Family Plagiopylidae Schewiakoff 1896 Genus Plagiopyla Stein 1860 P. marina Kahl 1933 P. ovata Kahl 1931 Family Sonderiidae Small et Lynn 1985 Genus Sonderia Kahl 1928 S. vorax Kahl 1928 Class Oligohymenophorea de Puytorac et al. 1974 Subclass Peniculia Faure-Fremiet in Corliss 1956 Order Peniculida Faure-Fremiet in Corliss 1956 Family Frontoniidae Kahl 1926 Genus Frontonia Ehrenberg 1838
F. arenaria Kahl 1933
F. elongata Burkovsky 1970
F. fusca Quennerstedt 1869 *F. leucas Ehrenberg 1833
F. marina Fabre-Domergue 1891
F. maris-albi Burkovsky 1970
F. microstomata Kahl 1931
F. tchibisovae Burkovsky 1970 Family Parameciidae Dujardin 1840 Genus Paramecium Muller 1773 P. calkinsi Woodruff 1921 *P. duboscqui Chatton et Brachon 1933 *P. nephridiatum Gelei 1925 *P. woodruffi Wenrich 1928 Subclass Scuticociliatia Small 1967 Order Philasterida Small 1967 Family Cinetochilidae Perty 1852 Genus Cinetochilium Perty 1852 C. margaritaceum Perty 1852 C. marinum Kahl 1931 Family Cohnilembidae Kahl 1933 Genus Cohnilembus Kahl 1933 C. pusillus (Quennerstedt 1869) Kahl 1931 Family Loxocephalidae Jankowski 1964 Genus Cardiostomatella Corliss 1960 C. vermiforme (Kahl 1928) Corliss 1960 Family Philasteridae Kahl 1931 Genus Helicostoma Cohn 1866
H. buddenbrocki Kahl 1931
H. notatum Kahl 1931
H. oblogum Cohn 1866 Family Uronematidae Thompson 1964 Genus Uronema Dujardin 1841 U. marinum Dujardin 1841 Order Pleuronematida Faure-Fremiet in Corliss 1956 Family Cyclidiiidae Ehrenberg 1838 Genus Cristigera Roux 1899 C. minuta Kahl 1928 C. setosa Kahl 1928 Genus Cyclidium Muller 1786 C. candens Kahl 1928 C. fuscum Kahl 1928 C. marinum Borror 1963 C. velliferum Kahl 1933 Family Histibalantiidae de Puytorac et Corliss in Corliss 1979
Genus Histiobalantium Stokes 1886
H. majus Kahl 1931
H. marinum Kahl 1933 Family Pleuronematidae Kent 1880-2 Genus Pleuronema Dujardin 1836 *P. chrysalis (Muller 1786) Perty 1852 P. coronata Kent 1880-2 P. crassa Dujardin 1836 P. marina Dujardin 1841
P. setigera Calkins 1902 P. simplex Dragesco 1960 Subclass Hymenostomatia Delage et Herouard 1896 Order Hymenostomatida Delage et Herouard 1896 Family Glaucomidae Corliss 1971 Genus Glaucoma Ehrenberg 1830
G. pyriformis (Ehrenberg 1838) Maupas 1883 Family Ophryoglenidae Kent 1880-2 Genus Ophryoglena Ehrenberg 1831 O. macrostoma Kahl 1928 O. marina Burkovsky 1970 Insertae sedis in Phylum Ciliophora Family Coelosomidiidae Corliss 1961 Genus Coelosomides Strand 1928 C. vermiformis Burkovsky 1970 Genus Paraspathidium Noland 1937 P. fuscum (Kahl 1928) Dragesco 1960 P. obliquum Dragesco 1960
Total species richness recorded in the White Sea (273 species) is much lower than in such relatively well-studied seas as the Caspian (351 species, Agamaliev, 1983; Alekperov and Asadullaeva, 1996), the Baltic (318 species, Agamaliev, 1983) and the Black Sea (about 450 species, Azovsky and Mazei, 2003). This fact may be considered as surprising, taking into account the long history of ciliatological studies at the White Sea. However, an overwhelming majority of investigations was conducted in a restricted geographical region (in the Kandalaksha Bay), where scientific centres are concentrated. At the same time, it has been noted that differences between regions within seas may be significant, exploration of new regions yielding a great increase in the total species number (Azovsky and Mazei, 2003).
Species/genera (S/G) ratio for the White Sea fauna as a whole is 2.91. It is rather low as compared with other relatively well-studied seas (Caspian - 3.36; Black - 3.24; Baltic - 2.89; North Atlantic - 3.33; Azovsky and Mazei, 2003), indicating that less congeners constitute the White Sea fauna. The largest genera are Loxophyllum (17 species), Lacrymaria (15), Tracheloraphis (13), Euplotes (9), Strombidium (9), Geleia (8), Aspidisca (8), Frontonia (8). They form 31.5% of the total species richness of the region and only 8.4% of the genera richness. On the other hand, there are 43 single-species genera (15.6% of species richness and 45.3% of genera richness).
Acknowledgements
The work was supported by the Russian Foundation for Basic Research, grants № 02-04-48002 and № 0404-48338.
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Address for correspondence: Yuri A. Mazei. Department of Ecology, Penza State Pedagogical University, Penza, 440026, Russia. E-mail: [email protected]
Editorial responsibility: Sergei Fokin