Ecologica Montenegrina 43: 69-75 (2021) This journal is available online at: www.biotaxa.org/em http://dx.doi.org/10.37828/em.2021.43.10

The first finding of sessile pyriforme Stiller, 1939 and sinense Song, 1991 (Ciliophora, Peritrichia) in the Black Sea

ALIE S. ABIBULAEVA* & IGOR V. DOVGAL

A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS, Sevastopol, Russia. E-mails: [email protected]*, [email protected]

Received 15 May 2021 │ Accepted by V. Pešić: 19 June 2021 │ Published online 1 July 2021.

Abstract Two species of sessile ciliates from subclass Peritrichia, Vorticella pyriforme and Zoothamnium sinense, new for Black Sea, were found in the Kruglaya Bay (the Black Sea) on algae Cystoseira crinita and Cladophora sericea. The article provides a description, systematic position and data on the distribution of the collected species.

Key words: Black Sea, Cladophora, Cystoseira, Kruglaya Bay, , Vorticella, Zoothamnium.

Introduction

Algae are a convenient substrate for various periphytic organisms including sessile ciliates. The term «periphyton» (from the Greek περιφύω - to grow in a circle, to grow) was proposed by A.L. Bening (1924, cited after Protasov, 2011). According to the classification proposed by the Czechoslovak hydrobiologist Sramek-Husek (1946, cited after Sladeckova, 1962), periphytic organisms, which inhabit aquatic plants belong to the epiphyton community. In marine hydrobiology the term was successfully used by E.B. Makkaveeva (Makkaveeva, 1979). Organisms of epiphyton can achieve of high abundance, plaing an important role in various aquatic ecosystems (Shadrin, 1990; Weissman et al., 1993; Gilbert & Schröder, 2003). In particular, the such epiphytonic organisms as peritrich ciliates are widely distributed and may be of interest in marine ecology. However, little is known about species composition of sessile ciliates from the Black Sea macrophytes, the available data mainly presented in lists (Gassowski, 1960, Konstantinenko, 2014) or in few in number publications on separate species (Dovgal et al., 2006; Pavlovskya et al., 2009; Dovgal, 2013; Dovgal & Sergeeva, 2016; Sergeeva et al., 2020). The present article deal with finds two representatives of subclass Peritrichia (Vorticella pyriforme Stiller, 1939 and Zoothamnium sinense Song, 1991) on algae Cystoseira crinita (Desf.) Bory and Cladophora sericea (Hudson) Kützing, 1843. The found species were not mentioned in the above-mentioned lists of the Black Sea ciliates and therefore are new to the sea.

Ecologica Montenegrina, 43, 2021, 69-75

FIRST FINDINGS OF TWO SESSILE CILIATES FROM THE BLACK SEA

Material and methods

The algae, Cystoseira crinita (Desf.) Bory and Cladophora sericea (Hudson) Kützing, 1843, were collected in the Kruglaya Bay (the Black Sea) in autumn 2020. A schematic map of the study area is shown in Figure 1. Kruglaya Bay is distinguished by biological and substrate diversity, as well as by variety both of sea grasses and algae vegetation (Mironova & Pankeeva, 2020).

Figure 1. Map of sampling area (September 2020).

The samples of macroalgae were collected manually by scraping at a depth from 0.1 to 2.0 meters. Samples were taken at three locations of Kruglaya Bay under the same salinity (18‰), air temperature (29 oС), and water temperature (24 oС). Fragments of the algae thalli were placed in a container filled with seawater from the sampling locations and delivered to the laboratory. Photos of the observed species were taken using the ToupCam digital microscopic camera, measurements were made using Toup View 3.7 software. The identification of ciliates was carried out according to Warren (Warren,1986), Ji et al. (Ji et al., 2006). The taxonomic position of taxa is given according to Lynn (2008). Identification of Cladophora species was carried out using keys of Afanasyev et al. (2020), while identification of Cystoseira species using keys of Zinova (1967) and Zinova & Kalugina (1974).

Results and discussion

Descriptions, taxonomy and illustrations of the collected species are given below.

Phylum: Ciliophora Doflein, 1901 Subphylum: Lynn, 1996 Class: de Puytorac et al., 1974 Subclass: Peritrichia Stein, 1859 Order: Sessilina Kahl, 1933 Family: Ehrenberg, 1838 Genus: Vorticella Linnaeus, 1767

70

ABIBULAEVA & DOVGAL

Vorticella pyriforme Stiller, 1939 (Fig. 2) Synonym: V. intermissa Nenninger, 1948

Description (after Warren, 1986 with modifications). Zooid 69–92 µm long  50–61 µm wide (45–70 µm long  30–40 µm wide after Warren, 1986). Zooid inverted bell-shaped, with constriction beneath peristomial lip. Peristomial disc is elevated slightly. Contractile vacuole is located in upper part of the body under the peristomial disk. Macronucleus is poorly visible, but according to Warren, 1986 it is C-shaped and lies transversely across the center of zooid. Pellicular striations are not visible. Stalk length ranges from 190– 212 µm (according to Warren, 1986 stalk can be up to 400 µm in length).

Figure 2. Vorticella pyriforme Stiller, 1939. A – modified from Warren, 1986, scale bar: 25 µm; B – original, in vivo, scale bar: 75 µm.

Habitat. Freshwater or marine.

Localities. First mentioned by Stiller (1939). The latter author has described this species and mentioned the location: Helgoland archipelago in the Northern Sea (Germany) (Stiller, 1939). Later on, Nenninger (1948) described a V. intermissa Nenninger, 1948 from the vicinity of Erlangen (Germany), a species which was synonymized with V. pyriforme by Warren (1986).

Substrates. Species found on green filamentous alga Cladophora sericea (Hudson) Kützing, 1843, which in turn was attached to brown alga Cystoseira crinita (Desf.) Bory. Dimensions are based on measurements of 7 samples (table 1). Distribution of ciliates over the substrate: 1 to 3 individuals per 1 mm of algae thallus.

Genus: Zoothamnium Bory de St. Vincent, 1826

Zoothamnium sinense Song, 1991 (Fig. 3,4) Synonyms: Zoothamnium commune sensu Song,1991 Z. truncatum Song, 1986 (primary homonym)

Ecologica Montenegrina, 43, 2021, 69-75 71

FIRST FINDINGS OF TWO SESSILE CILIATES FROM THE BLACK SEA

Table 1. Measurements of Vorticella pyriforme and Zoothamnium sinense.

Sample Peristomial lip Zooid in Zooid in External stalk External Сontractile number in vivo, vivo vivo in vivo stalk in vivo vacuole in vivo µm (length), (width), (length), (width), (diametr), µm µm µm µm µm Vorticella pyriforme Stiller, 1939 1 63 69 50 190 5 20 2 59 74 52 198 5 20 3 71 92 61 212 8 21 4 69 77 60 204 6 22 5 70 84 66 208 5 20 6 63 72 55 200 4 19 7 67 81 58 199 5 20 Zoothamnium sinense Song, 1991 1 34–42 32–48 25–39 256 6 10 2 36–45 35–50 28–35 245 6 12 3 35–46 36–49 25–40 270 7 10 4 34–45 35–50 29–39 272 8 11 5 36–42 38–50 30–40 300 9 13

Description. Small colony, 7 to 12 zooids, alternately branched, length of main stalk is 245–300 µm, 6–9 µm in diameter. Zooids inverted bell-shaped, about 35–50  30–40 µm in vivo. Peristomial disc is flat, occasionally slightly elevated over distinctly everted peristomial lip. At low magnification, the pellicle looks smooth. Single contractile vacuole apically positioned. Macronucleus is usually C-shaped, transversely oriented, located in oral 2/3 of body and surrounds the aboral portion of infundibulum (after Ji et al., 2006). Dimensions are based on measurements of 5 samples (table 1). Distribution of ciliates over the substrate: from 1 to 2 colonies per 1 mm of algae thallus.

Figure 3. General view of the colony Zoothamnium sinense Song, 1991 (original, in vivo), scale bar: 250 µm.

72

ABIBULAEVA & DOVGAL

Habitat. Marine, occasionally found in eutrophic waters.

Localities. Zoothamnium sinense was originally described by Song (1986) under the name Z. truncatum, but later, due to homonymy, the same author (Song 1991) proposed a replacement name Z. sinense. This species was reported from North China, attached on artificial substrate by Ji et al. (2006).

Substrates. Species found on green filamentous alga Cladophora sericea (Hudson) Kützing, 1843.

Figure 4. Zoothamnium sinense Song, 1991. A, C – original, in vivo, scale bar: 35 µm; В – modified from Ji et al., 2006, scale bar: 20 µm.

Discussion

In a review article by Gassowski (1960), the author pointed out that 177 species of ciliates were found in the Black Sea, among which are 87 peritrich ciliates, and 19 suctorians, however, information on the nature of the substrate on which these species were recorded is lacking. In article by Pavlovskya et al. (2009) reports

Ecologica Montenegrina, 43, 2021, 69-75 73

FIRST FINDINGS OF TWO SESSILE CILIATES FROM THE BLACK SEA

about 21 species of ciliates have been found in floating green algae Cladophora mats. In the Dovgal’s monograph (2013) 4 species of suctorian ciliates, which were not previously mentioned by Gassowski (1960) were registered as found at the macroalgae in the Black Sea. In addition, in the Selifonova’s (2015) thesis the collecting of Vorticella anabaena Stiller, 1940 on blue-green algae from the Black Sea was noted. Based on this, it is reasonably safe to suggest that the ciliates of the epiphyton are poorly known and invites further investigation. The fact that the species described in this article turned out to be new to the region indicates insufficient knowledge of this group in the Black Sea.

Acknowledgement

The study was conducted in the framework of the state assignments of the A.O. Kovalevsky Institute of Biology of the Southern Seas of RAS (№121040500247–0).

References

Afanasyev, D.F., Sushkova, E.G. & Kamnev A.N. (2020) Marine and brackish species of Cladophoraceae and Aegagropila, found in the Ponto-Caspian basin: the field guide. Publishing house «Pero», 76 pp. (in Russian with English summary). Dovgal, I. & Sergeeva, N. (2016) Sessile Ciliates (Ciliophora) from extreme habitats. Journal of Siberian Federal University, Biology, 9 (4), 385–397 (in Russian with English summary). Dovgal, I.V. (2013) Fauna of Ukraine: in 40 vol. Vol. 36: Ciliates – Ciliophora. Issue 1: Class Suctorea. Naukova dumka, Kiev, 271 pp. (in Russian with English summary). Dovgal, I.V., Shadrin, N.V. & Gaponova, L.P. (2006) New findings of halobiont ciliates. Vestnik zoologii, 40 (5), 462 (in Russian with English summary). Gassowski, G.M. (1960) Praktychne znachennya іnfuzorіj ta іstorіya ikh doslіdzhennya na Ukrainі. Zbirnik pratc' zoologichnogo muzeyu, Kiev, pp. 58–90 (in Ukrainian). Gilbert, J. & Schröder, T. (2003) The ciliate epibiont pygmaeum: selection for zooplankton hosts, reproduction and effect on two rotifers. Freshwater Biology, 48 (5), 878–893. Ji, D., Song, W. & Warren, A. (2006) Redescriptions of three marine peritrichous ciliates, Zoothamnium alternans Claparéde et Lachmann, 1859, Z. sinense Song, 1991 and Z. commune Kahl, 1933 (Ciliophora, Peritrichia), from North China. Acta Protozoologica, 45, 27–39. Konstantynenko, L.A. (2014) The list of the freshwater Peritrichia of the Ukraine. Visnyk of the Lviv University, Serie Biology, 64, 21–32 (in Ukrainian with English summary). Lynn, D.H. (2008) The ciliated : characterization, classification, and guide to the literature. Dordrecht: Springer, 605 pp. Makkaveeva, E.B. (1979) Bespozvonochnye zaroslej makrofitov Chernogo morya. Naukova dumka, Kiev, 228 pp. (In Russian). Mironova, N.V. & Pankeeva, T.V. (2020) Spatiotemporal сhanges in the macrophytobenthos of Kruglaya Bay (Black Sea). South of Russia: ecology, development, 15 (2), 125–139 (In Russian with English summary). Nenninger, U. (1948) Die Peritrichen der Umgebung von Erlangen mit besonderer Beriiksichtigung ihrer Wirtsspezifitat. Zoologische Jahrbücher (Systematik), 77, 169‒266. Pavlovskya, T.V., Prazukin, A.V. & Shadrin, N.V. (2009) Seasonal phenomena in Infusoria community in hypersaline lake Khersonesskoye (Crimea). Marine Ecological Journal, 2 (8), 53–63 (in Russian with English summary). Protasov, A.A. (2011) Zhizn' v gidrosfere. Ocherki po obshchej gidrobiologii. Akademperiodika, Kiev, 704 pp. (In Russian). Selifonova, J.P. (2015) Strukturno-funkcional'naya organizaciya ekosistem zalivov i buht Chernogo i Azovskogo morej (Rossijskij sector). Available from: http://dspace.vniro.ru/handle/123456789/5664 (23.06.2021) Sergeeva, N., Shadrin, N., Abibulaeva, A. & Dovgal, I. (2020) Records of sessile ciliates (Ciliophora, Peritrichia) on the green filamentous algae Cladophora sivashensis in the Sivash Bay (the Sea of Azov). Protistology, 14 (2), 89‒94.

74

ABIBULAEVA & DOVGAL

Shadrin, N.V. (1990) The influence of biotic factors on the energy balance of aquatic organisms. Bioenergetics of hydrobionts. Naukova Dumka, Kiev, pp. 109–118 (in Russian with English summary). Sladečkova, A. (1962) Limnological investigation methods for the periphyton («Aufwuchs»). The Botanical Review, 28 (2), pp. 286—350. Song, W. (1986) Descriptions of seven new species of peritrichs on Penaeus orientalis (Peritricha: Zoothamnidae: Epistylididae). Acta Zootaxonomica Sinica, 11, 225‒235 (in Chinese with English summary). Song, W. (1991) Contribution to the commensal ciliates on Penaeus orientalis. II. (Ciliophora, Peritrichida). Journal of Ocean University of Qingdao, 21, 45‒55 (in Chinese with English summary). Stiller, J. (1939) Die Peritrichenfauna der Nordsee Bei Helgoland. Archiv fur Protistenkunde, 92, 413–452. Warren, A. (1986) A revision of the genus Vorticella (Ciliophora: Peritrichida). Bulletin of the British Museum (Natural History), Zoology, 50 (1), 1–57. Weissman, P., Lonsdale, D.J. & Yen, J. (1993) The effect of peritrich ciliates on the production of Acartia hudsonica in Long Island Sound. Limnology and Oceanography, 38 (3), 613–622. Zinova, A.D. (1967) Opredelitel' zelenyh, buryh i krasnyh vodoroslej yuzhnyh morej SSSR. Nauka, Leningrad, 400 pp. (in Russian). Zinova, A.D. & Kalugina, A.A. (1974) K sistematike vidov roda Cystoseira Ag. v Chernom more. Novosti sistematiki nizshih rastenij, 11, 116–125 (in Russian).

Ecologica Montenegrina, 43, 2021, 69-75 75