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19 July 2023

Biodiversity of Marine Interstitial Ciliates in the Intertidal Zone of the White Sea: A Dataset from the Chernaya River Estuary, Kandalaksha Gulf

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and
1
Faculty of Biology, Shenzhen MSU-BIT University, 1 International University Park Road, Shenzhen 518172, China
2
Department of General Ecology and Hydrobiology, Lomonosov Moscow State University, 1 Leninskiye Gory, 119899 Moscow, Russia
3
Department of Microbiology, Epidemiology and Infectious Diseases, Penza State University, Krasnaya Street 40, 440026 Penza, Russia
*
Author to whom correspondence should be addressed.
Diversity2023, 15(7), 873;https://doi.org/10.3390/d15070873
This article belongs to the Special Issue Biodiversity of Invertebrates
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Abstract

(1) Background: An estuary is a zone in which sea and river waters mix. It is a specific area with a very non-stable environment and salinity gradient. However, little is known about the diversity of ciliate communities in estuarine benthic ecosystems in the Arctic. The aim of this paper is to describe the diversity of intertidal ciliates in the Chernaya river estuary (Kandalaksha Gulf, White Sea), which is characterized by a pronounced salinity gradient (0–22‰), on the basis of a recently published dataset. (2) Methods: We conducted our own investigations during the summer periods of 1998–2000. Material was collected at five permanent stations along the salinity gradient (0–22%) of the estuary. For each observation, the coordinates of the sampling sites, the number of individuals observed and the sampling date were recorded. The total effort comprised 35 sampling days, with five sampling sites at each date. (3) Results: The dataset contains 4270 unique occurrences of 119 ciliates taxa (109 species, 8 unidentified species of the genus level and 2 unidentified species on the family level). The total number of specimens represented is 64,475. (4) Conclusions: The largest classes in terms of species diversity are Hypotrichea (27 species), Gymnostomatea (26 species), Oligohymenophorea (17 species) and Karyorelictea (16 species).
Dataset: https://doi.org/10.15468/ccku5d.
Dataset License: Creative Commons Attribution (CC-BY) 4.0 License.

1. Summary

Ciliates are unicellular protists with a high level of diversity and wide distribution [1]. Intertidal sediments are characterized by a high species abundance and richness of ciliates, with up to 2500 cells/mL [2,3,4]. Hamels et al. [5] detected 53 species from a volume of 0.2 mL of intertidal sediment. Burkovsky and Mazei [6,7] reported 125 ciliate species from an area of one square meter of intertidal sediment during a long-term study. With their high abundance and species richness, interstitial ciliates are suitable for evaluating the distribution patterns of protists and the major factors regulating their dispersal on different spatial scales [8,9,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24]. Previous studies have reported high levels of diversity of interstitial ciliates and other protists in the White Sea [25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41].
High environmental variability and a critical salinity level (3–8‰) cause peculiarities in ciliate community composition and complexity in brackish waters when compared with other biotopes [42,43,44,45,46,47,48,49,50,51,52,53,54]. Herein, we describe intertidal ciliate fauna in a non-stable environment with a pronounced salinity gradient (0–22‰) based on a recently published dataset.

2. Data Description

2.1. Dataset Description

In the dataset (Table 1), each observation includes basic information: the date of observation, coordinates (latitude/longitude), observer name, identifier name and publications (if available). The coordinates were determined using satellite images.
Table 1. Description of the data in the dataset.
The dataset contains 4270 unique occurrences of 119 ciliates taxa (species, genera and families) from the Chernaya River estuary (Kandalaksha Bay, White Sea). The dataset is based on field studies by Yuri A. Mazei and Igor V. Burkovsky which were performed in the period 1998–2000 [29,36].

2.2. Figures, Tables and Schemes

The dataset contains 4270 unique occurrences of 119 ciliates taxa (109 species, 8 genera and 2 families) from the Chernaya River estuary (Kandalaksha Bay, White Sea). The total number of specimens represented is 64,475. Hypotrichea (27 species), Gymnostomatea (26), Oligohymenophorea (17) and Karyorelictea (16) are the largest classes in terms of species richness. Karyorelictea (24,868) and Oligohymenophorea (19,260) are the largest classes in terms of abundance. Class Litostomatea were represented by only one species and one individual (Table 2).
Table 2. Species diversity of ciliate classes from the dataset.
Twenty species presented in the database have corrected names compared to the original studies [29,36,48]: Biholosticha discocephalus (Kahl, 1932) Berger, 2003, Anigsteinia clarissimum Kahl, 1928, Anigsteinia salinarum (Florentin, 1899) Kahl, 1932, Enchelyodon sulcatus Kahl, 1930, Holosticha gibba (Müller, 1786) Wrzesniowski, 1877, Kentrophoros fasciolatus Sauerbrey, 1928, Kentrophoros latus Raikov, 1962, Kentrophoros uninucleatus (Raikov, 1962) Raikov, 1962, Pleuronema coronatum Kent, 1881, Pleuronema crissum Dujardin, 1841, Protogastrostyla pulchra (Pereyaslawzewa, 1886) Gong, Kim, Kim, Min, Roberts, Warren & Choi, 2007, Limnostrombidium viride (Stein, 1867) Krainer, 1995, Tracheloraphis oligostriata Raikov, 1962, Prototrachelocerca caudata (Dragesco & Raikov, 1966) Foissner, 1986, Trachelocerca incaudata Kahl, 1933, Apotrachelocerca arenicola (Kahl, 1933), Trachelostyla pediculiformis (Cohn, 1866) Borror, 1972, Trichotaxis multinucleatus Burkovsky, 1970, Uroleptus caudatus (Stokes, 1886) Bardele, 1981, Uronema marinum Dujardin, 1841 and Urosoma caudatum (Ehrenberg, 1833) Berger, 1999.
In the marine zone (station 1, see Figure 1), the highest species richness was observed. As it moves towards the river mouth, we detected decreases in the abundance and richness of most stenohaline marine species and corresponding increases in marine euryhaline and brackish water (oligohaline) species. We did not find species of freshwater origin in the estuary.
Figure 1. Sampling sites in the White Sea. (a,b) The white stars on the satellite images showing the location of Chernaya River estuary. The basis for the maps (a,b) was https://www.google.com/maps/ (accessed on 5 June 2023). (c) A scheme of the locations of stations 1–5 in the estuary; numbers in the figure showing exact sampling sites at each station. The basis for the map (c) was https://360earthview.com/ (accessed on 5 June 2023).
For the entire period of observation, there were 45 families and 34,191 individuals recorded at station 1, 44 families and 15,223 individuals at station 2, 42 families and 7707 individuals at station 3, 39 families and 4003 individuals at station 4 and 34 families and 3351 individuals at station 5.
Each year, between 21 and 65 taxa were detected in one sample at station 1, between 15 and 46 taxa were detected at station 2, between 7 and 36 taxa were detected at station 3, between 6 and 27 taxa were detected at station 4 and between 8 and 30 taxa were detected at station 5.
The following taxa were found the most often in the most marine part of the estuary at Station 1: Apotrachelocerca arenicola, Cardiostomatella vermiformis, Coleps tesselatus, Didinium balbiani, Diophrys scutum, Discocephalus rotatorius, Geleia fossata, Histobalantium majus, Histobalantium marinum, Lacrymaria affinis, Limnostrombidium viride, Pleuronema marina, Prorodon, Remanella margaritifera, Trachelocerca incaudata, Urostrongylum caudatum and Uronema marinum. Moreover, Apotrachelocerca renicola, Histobalantium marinum, Remanella margaritifera, Trachelocerca incaudata and Uronema marinum were found in each sample the entire period of observation (Table 3).
Table 3. Abundance (individuals per square centimeter) and number of unique occurrences of most common ciliate species from the dataset.
The most common taxa found at Station 2 were Cardiostomatella vermiformis, Cyclidium fuscum, Didinium balbiani, Enchelyodon, Limnostrombidium viride, Histobalantium marinum, Prorodon, Remanella margaritifera, Sonderia vorax, Trachelocerca incaudata, Trachelocercidae, Tracheloraphis kahli, Trachelostyla caudata, Urostrongylum caudatum and Uronema marinum.
The most common taxa found at Station 3 were Cardiostomatella vermiformis, Coleps tesselatus, Cyclidium fuscum, Didinium balbiani, Enchelyodon, Histobalantium marinum, Pleuronema crassum, Prorodon, Sonderia vorax, Trachelocercidae, Trachelostyla caudata and Uronema marinum.
The most common taxa found at Station 4 were Anigsteinia clarissimum, Cyclidium fuscum, Enchelyodon, Glaucoma pyriformis, Lacrymaria affinis, Lacrymaria cohnii, Lacrymaria coronata, Oxytrichidae, Paraprorodon morgani, Pleuronema crassum, Prorodon and Uronema marinum.
The most common taxa found at Station 5 were Anigsteinia clarissimum, Cyclidium fuscum, Cyrtohymena marina, Enchelyodon, Lacrymaria affinis, Lacrymaria cohnii, Lacrymaria conifera, Lacrymaria coronata, Oxytrichidae, Paraprorodon morgani, Pleuronema crassum, Prorodon, Uronema marinum and Urosoma caudatum.
The following taxa were found at all stations for the entire period of observation: Apotrachelocerca arenicola, Aspidisca fusca Kahl, 1928, Anigsteinia clarissimum, Cardiostomatella vermiformis, Condylostoma curva Burkovsky, 1970, Cyclidium fuscum, Didinium balbiani, Diophrys scutum, Enchelyodon, Enchelyodon sulcatus Kahl, 1930, Euplotes trisulcatus Kahl, 1932, Frontonia fusca Quennerstedt, 1869, Frontonia marisalbi Burkovsky, 1970, Frontonia tchibisovae, Helicostoma notatum Kahl, 1931, Histobalantium marinum, Lacrymaria affinis, Lacrymaria caudata Kahl, 1933, Lacrymaria cohnii, Lacrymaria conifera, Lacrymaria coronata Claparède & Lachmann, 1859, Lacrymaria marina Meunier, 1907, Limnostrombidium viride, Mesodinium pulex (Claparède & Lachmann, 1859) Stein, 1867, Oxytrichidae, Paraprorodon morgani, Pleuronema coronatum Kent, 1881, Pleuronema crassum, Pleuronema marina, Prorodon, Sonderia vorax, Strombidium sulcatum Claparède & Lachmann, 1859, Trachelocercidae, Trachelostyla caudata, Trachelostyla pediculiformis (Cohn, 1866) Borror, 1972, Uroleptus caudatus (Stokes, 1886) Bardele, 1981, Uronema marinum, Uronychia transfuga (Müller, 1776) Stein, 1859 and Urostrongylum caudatum.
Ciliate species richness was slightly different in different years: 78 taxa in 1998, 79 taxa in 1999 and 94 taxa in 2000. As salinity decreases, the number of species decreases as well. General data on species richness at different stations in 1998, 1999 and 2000 are presented in Figure 2.
Figure 2. Number of taxa at different stations in all years.

3. Methods

The investigations were conducted during the summer periods of 1998–2000 periods in the Chernaya river estuary (the Kandalaksha Bay, the White Sea). Material was collected at five permanent stations. The stations were located at the middle horizon of the intertidal zone along the estuary on the borders, dividing relatively homogenous zones (Figure 1). The distance from the shore to a station differed at different stations due to the topography characteristics. Thus, at station 1 it was 60 m, at station 2 it was 10 m, at station 3 it was 5 m, at station 4 it was 12 m and at station 5 it was 2 m. The sampling was carried out in intervals of 5–7 days. The total effort comprised 14 sampling days in 1998, 5 sampling days in 1999 and 16 sampling days in 2000.
Each sample was a series of 15 subsamples (1 cm2 in square, 3 cm in height, which resulted in a 45 cm3 total sample) collected from a strictly fixed square 50 × 50 cm. A random sampling, corresponding to 1/15 of the total sample (3 cm3), was examined (i.e., under one mean statistical square centimeter). Fifteen simultaneously taken subsamples allowed one to grade the possible spatial heterogeneity and to receive as much information as possible about the species biodiversity. The ciliates were extracted from the sediment by washing, according to the Uhlig method [55], one hour after sampling. The quantitative counting of ciliates was performed on live individuals under the stereomicroscope BIOMED-9 (Russia) at a magnification of ×32–56. The ciliates were identified on silver-impregnated slides [56], according to Carey [57]. All individuals found were identified at species, genus or family levels. Most of the species were morphologically described in our previous publications [58,59,60,61].
Environmental factors (water temperature, salinity and pH) were measured at each station. The interstitial water temperature was measured using an ordinary thermometer (graduated to 0.1 °C), and salinity and pH were measured with a conductivity meter and pH meter, correspondingly (HANNA Instruments, Belgium).
The results of measuring different environmental parameters (Table 4) show that the Chernaya river estuary is a very spatially heterogeneous and temporally unstable environment. The spatial heterogeneity of the biotope is, first of all, connected with the mosaic distribution of mineral and organic sediments in the intertidal zone, which also determines other important environmental characteristics (pH, Eh and the granulometric composition of sediment). Temporal instability is conditioned by tidal rhythms and the unsteadiness of the river flow. More detailed information about environmental parameters for particular sampling points are provided in Table S1.
Table 4. Environmental parameters of samples from five stations.
All calculations were made with the use of MS Excel and PAST 4.11 packages.

Supplementary Materials

The following are available online at https://www.mdpi.com/article/10.3390/d15070873/s1, Table S1: Environmental parameters for particular sampling points in the Chernaya river estuary.

Author Contributions

Conceptualization, I.V.B. and Y.A.M.; methodology, I.V.B. and Y.A.M.; software, D.A.S.; validation, X.L., A.S.E. and D.A.S.; formal analysis, A.S.E.; investigation, I.V.B. and Y.A.M.; resources, I.V.B. and Y.A.M.; data curation, Y.A.M.; writing—original draft preparation, X.L. and A.S.E.; writing—review and editing, X.L., A.S.E., I.V.B., D.A.S. and Y.A.M.; visualization, A.S.E.; supervision, Y.A.M.; project administration, Y.A.M.; funding acquisition, Y.A.M. All authors have read and agreed to the published version of the manuscript.

Funding

The work was supported by the Russian Science Foundation (19-14-00102).

Institutional Review Board Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

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