Ecologica Montenegrina 17: 100-104 (2018) This journal is available online at: www.biotaxa.org/em

Microalgae in the diet of Eucypris mareotica (Crustacea, Ostracoda) in the hypersaline lake Chersonesskoye (Crimea)

ELENA V. ANUFRIIEVA*, DARIA S. BALYCHEVA, IRINA V. VDODOVICH, NICKOLAI V. SHADRIN

The A. O. Kovalevsky Institute of Marine Biological Research of RAS, 2 Nakhimov av., 299011, Sevastopol, Russia *Corresponding author: [email protected]

Received 18 April 2018 │ Accepted by V. Pešić: 14 May 2018 │ Published online 23 May 2018.

Abstract In the Crimea, there are many hypersaline lakes and lagoons, where Eucypris mareotica (Ostracoda), high halotolerant species, inhabit. Despite the wide distribution of the species and the abundance of its populations, little is known about the biology of E. mareotica, including its nutrition. Diversity of microalgae in gut of E. mareotica in Lake Chersonesskoye was studied. The crustaceans ate both phytoplankton and alga, which growth on cladophora filaments, as well as various small animals, but microalgae played a main role in their nutrition. The proportion of individuals, which had algae in intestines, ranged in a sample from 0 to 93%. In 335 analyzed individuals, 22 species of microalgae were found, which belong to 4 types, 4 classes and 11 orders. Of these, 4 species belong to the type Cyanobacteria, 3 – to Myzozoa, 4 – to Haptophyta, 11 – to Ochrophyta. The most common species was Peridinium cinctum. Given the availability of a wide variety of consumed microalgae, ostracod gut content analysis can be used to assess species diversity of microalgae in the lakes.

Key words: hypersaline waters, Ostracoda, Podocopida, feeding, microalgae, Crimea.

Introduction

Ostracoda play an important role in the food webs of different aquatic ecosystems (Brusca & Brusca 2003; Brandão et al. 2016), but this role has not been studied in extreme hypersaline waters. In Crimea, there are many hypersaline lakes and lagoons, where ostracod Eucypris mareotica (Fischer, 1855), a most halotolerant species among the ostracods in the world (Williams 1991; Li et al. 1997; Jia et al., 2015), is abundant (Dagaeva 1927; Balushkin et al. 2009; Belmonte et al. 2012; Shadrin & Anufriieva 2013). This bentho- planktonic species is widespread in Eurasia and North Africa (De Deckker 1981; Baltanás et al. 1990; Li et al. 1997; Meriç et al. 2010; Rasouli et al. 2016). Despite such wide distribution of this species and abundance of its populations, little is known about the biology of E. mareotica, including its nutrition. E. mareotica is widely used in the reconstruction of paleoenvironment conditions (Mischke et al. 2008; Li & Liu 2010); knowledge on nutrition of this species may increase the efficiency of its use as an indicator of the ecosystem state of modern lakes and paleolakes.

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The purpose of this work is to present new data and analyze the diversity of microalgae consumed by E. mareotica in the Crimean hypersaline Chersonesskoye lake.

Material and Methods

Lake Chersonesskoye (44°35'10''N, 33°23'32''E), one of 50 hypersaline lakes in Crimea, is located on Cape Chersoness, the extreme south-western point of City Sevastopol (see Fig. 1). It is a closed marine lagoon, separated from the sea by a boulder-pebble spit; through which filtration of marine water occur. The lake area is 0.05 km2, and the catchment area is 0.92 km2; the average depth is 0.38 m (Anufriieva & Shadrin 2012; Gubanov & Bobko 2012). Intensive water heating has been observed since April and reaches its maximum in August (29.5–36.0 °C); in winter, the water temperature in the lake can drop below 0 °C. The maximum salinity in the main part of the lake reached 120 g/L during the period of observations (2005– 2018), and in the southern part – up to 340 g/L (August 2009), the minimum – 35.05 g/L (February 2006). E. mareotica lives in the lake at salinity up to 290–300 g/L. The pH is usually slightly alkaline, but the maximum values due to the high intensity of photosynthesis can reach up to 10. During the period of observations in the phytoplankton of the lake, 61 species are recorded. As usually, there is an intensive development of floating green algae mats in the lake (Prazukin et al. 2008), where the bulk of ostracods and other animals concentrate (Kolesnikova et al. 2008). Quantitative samples of zooplankton were taken in different seasons (2015–2018) by filtration of at least 50–100 liters of water through a plankton net with a mesh size of 110 μm. Samples were fixed with 4% formalin and processed using the Olympus SZ-ST and LOMO MBS-9 stereo microscope, performing gut dissection and food content analysis. Species identifications were made using an Olympus BX50 compound microscope. The salinity, temperature and pH of the water were determined using a refractometer (Kelilong WZ212) and a pH meter (PHH-830).

Figure 1. The hypersaline Chersonesskoye lake in Crimea.

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Results and Discussion

Ostracods consumed both phytoplankton and epibiontic algae, which growth on cladophora filaments, as well as various small animals, but microalgae played a main role in their nutrition. The proportion of individuals, which had algae in gut content, ranged in a sample from 0 to 93%. In gut content of 335 analyzed individuals, 22 species of microalgae were found, which belong to 4 types, 4 classes and 11 orders. Of these, 4 species belong to the type Cyanobacteria, 3 – to Myzozoa, 4 – to Haptophyta, 11 – to Ochrophyta (Table 1). The most common species was Peridinium cinctum (O. F. Müller) Ehrenberg, 1832. The number of algal cells in an ostracod gut reached the high number, as an example, 153 cells for P. cinctum, 3314 cells for Microcystis pulverea (H.C. Wood) Forti, 1907 and 4140 cells for Phormidium nigroviride (Thwaites ex Gomont) Anagnostidis & Komárek, 1988, and reliably did not depend on salinity, temperature, pH. Given the availability of a wide variety of consumed microalgae, gut content analysis of ostracods can be used to assess species diversity of microalgae in the lakes.

Table 1. Microalgae in gut content of ostracod Eucypris mareotica in the hypersaline Chersonesskoye lake.

Phytoplankton Frequency of previously Type of Species occurrence in found in lake Comments habitat guts, % (Senicheva et al. 2008) Cyanobacteria Chroococcales Chroococcus minimus (Keissler) Benthic and 6.9 No – Lemmermann, 1904 epibiontic Microcystis pulverea (H.C.Wood) Forti, Benthic and 2.1 No – 1907 epibiontic Oscillatoriales Oscillatoria tenuis C.Agardh ex Gomont, Benthic and 0.9 No – 1892 epibiontic Phormidium nigroviride (Thwaites ex Benthic and 9.6 No – Gomont) Anagnostidis & Komárek, 1988 epibiontic Myzozoa Noctilucales Noctiluca scintillans (Macartney) Kofoid & 3.6 Planktonic No – Swezy, 1921 Pronoctiluca pelagica Fabre-Domergue, 0.3 Planktonic No – 1889 Peridiniales Peridinium cinctum (O.F.Müller) 18.5 Planktonic Yes – Ehrenberg, 1832 Haptophyta Coccolithales Calcidiscus leptoporus (G.Murray & 2.4 Planktonic No – V.H.Blackman) Loeblich Jr. & Tappan 1978 Coccolithus pelagicus (Wallich) J.Schiller, 0.3 Planktonic No – 1930 Oolithotus fragilis (Lohmann) Martini & 5.7 Planktonic Yes – C.Müller, 1972 Isochrysidales Emiliania huxleyi (Lohmann) W.W.Hay & May form 0.9 Planktonic Yes H.P.Mohler in Hay et al., 1967 blooms continued on the next page..

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TABLE 1. Ochrophyta Naviculales Halamphora coffeiformis (C.Agardh) Benthic and Potentially toxic 0.3 No Levkov, 2009 epibiontic species Haslea subagnita (Proshkina-Lavrenko) Benthic and 1.2 No – Makarova & Karaeva, 1985 epibiontic Benthic and Navicula sp. 0.3 Yes – epibiontic Mastogloiales Benthic and Mastogloia braunii Grunow, 1863 7.5 No – epibiontic Fragilariales Neosynedra provincialis (Grunow) Benthic and 0.3 No – D.M.Williams & Round, 1986 epibiontic Bacillariales Benthic and Nitzschia sp. 3.9 No – epibiontic Benthic and Nitzschia tenuirostris Mereschkowsky, 1902 2.1 Yes – planktonic Psammodictyon panduriforme (W.Gregory) Benthic and 0.3 No – D.G.Mann in Round et al., 1990 epibiontic Pseudo-nitzschia calliantha Lundholm, Benthic and Potentially toxic 0.6 No Moestrup & Hasle, 2003 planktonic species Tryblionella compressa (J.W.Bailey) 0.6 Planktonic No – M.Poulin, 1990 Thalassionematales Thalassionema nitzschioides (Grunow) Benthic and May form 0.3 No Mereschkowsky, 1902 planktonic blooms

Acknowledgements

This work of E.V. Anufriieva, D.S. Balycheva, and N.V. Shadrin was supported by the Russian Science Foundation (grant № 18-16-00001) and of I.V. Vdodovich by the state assignment of IMBR (№ АААА- А18-118020890074-2).

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