Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology

Volume 42, Issue 3

ISSN 1730-413X (225–232) eISSN 1897-3191 2013

DOI: 10.2478/s13545-013-0078-7 Received: March 27, 2012 Original research paper Accepted: October 26, 2012

INTRODUCTION Some rare and interesting green algae (Chlorophyta) from subalpine Tatra lakes The Tatra Mountains are the highest and most distinct part of the large Carpathian range, which (High Tatra Mountains, Poland) stretches into several countries of Central Europe, including Poland, Slovakia, Hungary, Ukraine and Romania. The Tatra Mountains are situated in the 1,* 2 Joanna Lenarczyk , Petro Tsarenko western part of the range, on the border between Poland and Slovakia. They have an alpine character, with the highest peak called Gerlach Mt. (2663 m 1Department of Phycology, W. Szafer Institute of Botany, a.s.l.). The Polish mountains are protected within Polish Academy of Sciences, ul. Lubicz 46, 31-512 Kraków, Tatra National Park. Poland There are 113 lakes in the Polish part of the 2Department of Phycology, M.G. Kholodny Institute of mountains (Łajczak 1996), including only 28 with a Botany, National Academy of Sciences of Ukraine, surface area greater than 1 ha (Kot 2009). However, 2 Tereshchenkivska st., 01601, Kyiv, Ukraine green algae living in these lakes, including Chlorophyta and Streptophyta in the most recent taxonomic concept (Graham et al. 2009), have not been studied in detail over the last half century. The Key words: coccoid green algae, Chlorophyta, most comprehensive study on this group of algae Chlorellales, Chlorococcales, Sphaeropleales, seems to be out of date as it was published over a subalpine lake, Tatra Mountains hundred years ago. Gutwiński (1909) gave a list of about 250 species found during a 5−year investigation in more than 30 various sample stations, including many situated in lakes. Later, Szklarczyk-Gazdowa (1960) recorded about 50 Abstract species from the phytoplankton of 11 Tatra lakes. Some information about green algae in selected Tatra Five green algal taxa rarely occurring in the world were found water reservoirs was also given by Raciborski (1910), in subalpine lakes of the High Tatra Mountains in Poland. These are Actinastrum gracillimum G.M. Sm. var. elongatum (G.M. Sm.) Gutwiński (1913) and Wołoszyńska (1925). During Fott, Monoraphidium tatrae (Hindák) Hindák, Pediastrum braunii the last 50 years studies were carried out also by Wartm. in Wartm. et Schenk, Scotiella tuberculata Bourr. var. Kawecka (1966, 1970) in Morskie Oko and Wielki tuberculata and Thelesphaera olivacea (Beck-Mannag.) Fott. The taxa Staw Polski, respectively, Siemińska (1967) in are described and illustrated with light micrographs and Toporowy Staw Wyżni, Starmach (1973) in Wielki drawings. A review of their distribution in the world is presented. Staw Polski, as well as Fott et al. (1999) in Długi Staw. The studies were restricted only to selected

lakes.

Green algae are permanent components of different ecosystems, including oligotrophic * Corresponding author: [email protected]

226 | Joanna Lenarczyk, Petro Tsarenko mountain reservoirs. The lack of detailed systematic Zmarzły Staw, are situated in the eastern part of the studies focused on horizontal and vertical valley, called Czarna Dolina Gąsienicowa. The rest of distribution of algae in the Polish Tatra Mountains the lakes lie in Zielona Dolina Gąsienicowa. The two was noticed by Starmach (1957) many years ago. In parts of the valley are divided by a mountain range addition, variety, morphologic-ecological features and called Grań Kościelców, including Kościelec, which composition of algae communities in the Tatra is its highest peak (2155 m a.s.l.). reservoirs remain insufficiently studied to this time. The rarely occurring taxa were found in four A special study concerning geographical aspects of lakes, including Litworowy Staw, Wyżni Czerwony separate species and character of their distribution is Stawek, Zielony Staw (Zielona Dolina Gąsienicowa) required. In fact, of approximately 9000 green algal and Zmarzły Staw (Czarna Dolina Gąsienicowa) species occurring worldwide (Wołowski 2003), 300 (Table 1, Fig. 1). Litworowy Staw lies at the lowest were recorded from various habitats of the Polish altitude (1618 m a.s.l.) of all the studied lakes. It is Tatra Mountains (Siemińska 1962), including only 81 very shallow (maximum depth 1.1 m) and partly from stagnant waters (Hindák & Kawecka 2010). In overgrown with sedges (Carex sp.). Wyżni Czerwony the most recent study on chlorophytes and Stawek, one of the complex Czerwone Stawki lakes, streptophytes in several limnologically different Tatra is small (0.27 ha) and shallow (maximum depth 1.5 lakes, 89 taxa were found (Lenarczyk 2012). Of these, m) as well. It is surrounded by dwarf pine (Pinus 58 were recorded for the first time from the Polish mugo) and meadows. Zielony Staw is the biggest lake Tatra lakes, but none of them were the typical alpine in Zielona Dolina Gąsienicowa. Its surface is 3.84 ha, forms of algal flora found in Austria (Bourrelly 1987, with a maximum depth of 15.1 m. Its catchment has Lenzenweger 2003). The study showed that green slopes covered mainly with dwarf pine. Waters from algae occurring in the Polish Tatra lakes need to be Zielony Staw flow into Litworowy Staw through a carefully examined in the future. brook called Sucha Woda. Zmarzły Staw lies at the The aim of our study is to give description and highest altitude (1787 m a.s.l.) of the studied lakes. iconographic documentation of rarely reported Similar to Litworowy Staw and Wyżni Czerwony chlorophycean algal taxa occurring in the Polish Stawek, this lake is also small (0.28 ha) and rather Tatra lakes, together with detailed information on shallow (maximum depth 3.7 m). Zmarzły Staw is their distribution in the world. The study is a part of mainly surrounded by bare rocks. All data about an extensive revision of diversity of green algae in the position and morphometry of the studied lakes are Dolina Gąsienicowa valley. gathered in Table 1.

STUDY AREA

The study was carried out in Dolina Gąsienicowa. It is a large valley in the eastern part of the Polish Tatra Mountains, called the High Tatra Mountains. It is surrounded to the west and southwest by peaks of the West Tatras (lower part of the Tatra Mountains), including Kopa Magury (1704 m a.s.l.), Kasprowy Wierch (1987 m a.s.l.) and Beskid (2012 m a.s.l.). To the south and east this area is surrounded by peaks of the High Tatras, including Świnica (2301 m a.s.l.), Kozi Wierch (2291 m a.s.l.) and Żółta Turnia (2087 m a.s.l.). The valley is situated on granite bedrock, at an elevation ca. 1500−1800 m a.s.l., in the subalpine zone. There are 21 lakes placed in Dolina Gąsienicowa, the highest number of lakes in all the Polish Tatra valleys. The lakes differ greatly in altitude, origin, morphometry and physico-chemical parameters (Wit-Jóźwikowa & Ziemońska 1962, Fig. 1. Location of the four studied lakes in the Tatra Radwańska-Paryska & Paryski 1994, Piątek 2006). Mountains (Poland) Two of the lakes, Czarny Staw Gąsienicowy and

Some rare and interesting green algae from subalpine Tatra lakes (High Tatra Mountains, Poland)| 227

Table 1

Morphometry (according to Wit-Jóźwikowa & Ziemońska 1962), basic physico-chemical water parameters (original measurements), as well as five rare green algal taxa observed in the studied Tatra lakes; - not measured

Lake Unit Litworowy Staw Wyżni Czerwony Stawek Zielony Staw Zmarzły Staw 49°14’01” N 49°13’40” N 49°13’43” N 49°13’26” N Position 19°59’49” E 20°00’14” E 19°59’58” E 20°01’21” E Altitude a.s.l. m 1618 1695 1672 1787 Surface ha 0.48 0.27 3.84 0.28 Maximum depth m 1.1 1.5 15.1 3.7 Mean depth m 0.6 0.5 6.8 2.3 Date of observation 25th August 2011 22nd July 2011 25th August 2011 25th August 2011 23rd July 2011 Water temperature °C 14.4 - 16.8 17.8 14.8 pH 7.1 - 7.7 7.7 7.4 Conductivity μS cm-1 ca. 17 - ca. 22 ca. 16 ca. 15 Pediastrum braunii, Actinastrum Observed taxa Monoraphidium tatrae Scotiella tuberculata var. Thelesphaera olivacea gracillimum Thelesphaera olivacea tuberculata var. elongatum

M ATERIALS AND METHODS descriptions and some taxonomic notes, together with iconographic documentation of the taxa, are The material was collected during the summer of provided below. 2011 from littoral zones of the four lakes (Table 1, Fig. 1). One sample station was situated in each of Chlorellales the lakes. There were mainly Sphagnum sp. and vascular plants (Litworowy Staw) or bare rocks Actinastrum gracillimum G.M. Sm. var. (Wyżni Czerwony Stawek, Zielony Staw, Zmarzły elongatum (G.M. Sm.) Fott 1977, p. 5, figs 1h & 3f Staw) close to the sample stations. Phytoplankton samples were taken with a plankton net (mesh size 10 Basionym: Actinastrum hantzschii Lagerh. var. µm) from three of the lakes. At Zielony Staw, the elongatum G.M. Sm. (Fott 1977). fourth lake, periphyton samples (with small parts of vascular plants and water from the lake) were taken. Coenobium 4−celled. Cells 30−37 µm long, 3 µm The samples were collected into ca. 30 ml plastic wide (2 µm near the apex), strongly elongated, containers and immediately preserved with 2−4% cylindrical or slightly narrowing towards widely formaldehyde. Selected physico-chemical water rounded apex. Chloroplast parietal, not going into parameters (Table 1) were measured in the field with the apex (Fig. 2a, b). an Elmetron pH/conductivity meter CPC-401, equipped with EPS-1 electrode, Elmetron Notes. Our cells are narrower than cells in the conductivity and Nakamichi temperature sensors. original description (Fott 1977), 4−5 µm in width. The material was examined in the laboratory using a Nikon Optiphot-2 light microscope with a Nikon Sphaeropleales DS-Fi1 camera. The taxonomic study was conducted according to Fott (1966, 1977), Hindák (1977), Monoraphidium tatrae (Hindák) Hindák 1977, p. Komárek & Fott (1983), and Komárek & Jankovská 109 (2001). Basionym: Chlorolobion tatrae Hindák 1970, p. 13, fig. RESULTS 4

Five coccoid green algae (phylum Chlorophyta, Single cell 23 µm long, 7 µm wide, asymmetrical, with class Chlorophyceae, orders: Sphaeropleales, one sharp elongated apex and the other rounded, Chlorellales and Chlorococcales) which are rarely slightly curved, with one side convex and the other reported in the world were observed in the material almost straight. Chloroplast parietal, without collected from the studied lakes (Table 1). Short pyrenoid (Fig. 2c).

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228 | Joanna Lenarczyk, Petro Tsarenko

Fig. 2. a, b − Actinastrum gracillimum G.M. Sm. var. elongatum (G.M. Sm.) Fott.; c − Monoraphidium tatrae (Hindák) Hindák; d, g − Pediastrum braunii Wartm. in Wartm. & Schenk (one specimen in different views); e, f, h, i − Scotiella tuberculata Bourr. var. tuberculata (one specimen in different views); j−o − Thelesphaera olivacea (Beck-Mannag.) Fott (three specimens)

Some rare and interesting green algae from subalpine Tatra lakes (High Tatra Mountains, Poland)| 229

Notes. The alga is morphologically very similar to Cell oval, empty (without protoplast), 28 µm long Chlorolobion lunulatum Hindák (1970). The main and 19 µm wide, with 10 hyaline, smooth ribs, difference is that Ch. lunulatum possesses a pyrenoid. situated concentrically along the cell, 2−4 ribs joined Because of the absence of the pyrenoid Hindák at the cell poles (Fig. 2e, f, h, i). (1977) moved Ch. tatrae to the genus Monoraphidium Komárk.-Legner. On the basis of the morphological Notes. Mature cells of the genus Scotiella probably and ecological similarities, M. tatrae and Ch. lunulatum generate four autospores (Komárek & Fott 1983). If are supposed to belong to the same species this is true, our cells should have died before (Komárek & Fott 1983). observation as no protoplast and no cell wall crack for releasing the autospores was found. However, Pediastrum braunii Wartm. in Wartm. & Schenk some of the Scotiella species are supposed to be (Komárek & Jankovská 2001, p. 72, figs 46 a−g) resting stages of other green algae, including Chloromonas cryophila Hoham et Mullet = Ch. nivalis Basionym: Pediastrum tricornutum Borge (Chodat) Hoham & Mullet (Hoham & Mullet 1977, (Wołoszyńska 1925, p. 50, fig. 2) 1978) and Ch. pichillchae (Lagerh.) Wille (Hoham 1975). Various stages of the life cycle of Scotiella were Synonyms: P. tricornutum var. alpinum Schmidle 1896, observed by Komáromy (1978). p. 5, pl. 14, figs 2−4; P. tricornutum var. alpinum fo. punctatum Schröder 1898, p. 22, pl. 1, fig. 2 Thelesphaera olivacea (Beck-Mannag.) Fott 1976, p. 296, fig. 5 Coenobia 39−42 µm diameter, circular in outline, one complete 8−celled and another one incomplete Basionym: Tetraedron olivaceum Beck-Mannag. (Fott 16−celled, without or with small openings between 1976) cells. Marginal cells 10−11 µm long, 8−11 µm wide, trapezoid. Each of them with almost straight outer Cells single or doubled, 19−22 µm diameter sides, without any incision, but with four short (including processes), spherical or polygonal. Cell conical lobes, ended with small processes. Two of wall thick, hyaline or brown, with 5−7 short, the lobes situated close the neighboring marginal rounded processes (Fig. 2j - o). cells and in the plane of the coenobium, two others in the middle of the outer cell margin and obliquely Notes. By determining our specimens of Thelesphaera to the plane of the coenobium. Additional small we understood that its diameter, 21−31 µm (given by warts near the basis of the marginal cells also present. Fott 1976), includes the length of the processes as Inner cells 9 µm long, 9−11 µm wide, polygonal, with well. So our specimens are a bit smaller than Fott’s. lobes and processes oriented obliquely to the plane Pascher (1943) described Th. alpina as having a of the coenobium and morphologically identical to 10−12 µm diameter and up to 5 µm long processes. lobes of the marginal cells. Cell wall irregularly In fact, total dimensions of both taxa, Th. olivacea and granulated (Fig. 2d, g). Th. alpina, are very similar, including length of the processes. However, Czerwik-Marcinkowska & Notes. Parra (1979) noticed that localization of the Mrozińska (2011) observed cells of Th. alpina having processes can be variable and sometimes only tree 10−12 µm diameter and 0.5 µm long processes. The processes can be visible. It was the reason why the authors presented pictures made in TEM, so their former name of the species was P. tricornutum, derived cells are difficult to compare with our cells in LM from Latin trĕs (three) and cornŭ (horn). Wołoszyńska pictures or the specimens drawn by Pascher (1943), (1925) observed smooth cell surface. According to Fott (1976) and Lukavský (1994). Very small cells of Parra (1979) and Komárek & Jankovská (2001) the Th. alpina, with 10.5−12.5 μm diameter and forming cell wall is reticulate with irregularly disposed warts sometimes 3−7 celled pseudofilaments, were or granules. observed by Uher (2008). Details of the protoplast in Th. olivacea were neither described, nor appropriately Chlorococcales drawn (Fott 1976). In spite of this, both taxa are morphologically very close to each other. Scotiella tuberculata Bourr. var. tuberculata Reproduction in the genus Thelesphaera consists of (Komárek & Fott 1983, p. 710, pl. 199, fig. 1) production of autospores (Pascher 1943). Doubled

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230 | Joanna Lenarczyk, Petro Tsarenko cells observed in the collected materials (Fig. 2n, o) of the Slovak Tatra Mountains (Hindák 1970). should be the two autospores, which can escape Chlorolobion lunulatum, which closely resembles M. through a crack in the maternal cell wall. Some of our tatrae in form, has similar ecological requirements. cells have brown walls, not observed in Thelesphaera This is one of the reasons why Komárek & Fott by other authors (Pascher 1943, Fott 1976, Lukavský (1983) supposed that both M. tatrae and Ch. lunulatum 1994, Uher 2008, Czerwik-Marcinkowska & belong to the same species. The latter was isolated Mrozińska 2011). Pascher (1943) noticed that from calcite substratum (1400 m a.s.l.) in the Slovak specimens of Thelesphaera are similar to spores of Tatra Mountains and determined after culturing in liverworts (Hepaticae). Lukavský (1994) observed cells strain no. 1962/38 (Hindák 1970). However, the recognized by him as “cf. Thelesphaera alpina Pascher species was also observed in the Danube, a river in or propagation bodies of Hepaticeae” in the Slovakia (Hindák 1993). hypolimnion of Velké Hincovo, one of the Slovak Pediastrum braunii was regarded as an arctic-alpine Tatra lakes. However, although these cells are form by Wołoszyńska (1925). Komárek & Jankovská polyhedral, their processes are not directed to various (2001) assumed that the species had a boreo-alpine sides. It is possible that both Th. olivacea and Th. distribution. P. braunii occurs very rarely in the world. alpina belong to the same species. The genus It is known only from high mountains and both Thelesphaera requires further taxonomic studies. northern and southern circumpolar regions, where it was found exclusively in cold and clean swampy DISCUSSION localities, small water bodies and wetlands (Komárek & Jankovská 2001). The recent finding of P. braunii is Summer phytoplankton and periphyton in the first in Poland since the beginning of the 20th Litworowy Staw, Wyżni Czerwony Stawek, Zielony century. Wołoszyńska (1925) recorded it in various Staw and Zmarzły Staw (Dolina Gąsienicowa, Tatra unspecified Polish Tatra lakes. Juriš & Kováčik Mountains) were studied. The lakes are situated in (1987), who studied the phytoplankton of more than the subalpine zone and have a low trophy. Their forty Slovak Tatra lakes, found the species only in conductivity is ca. 15−22 μS cm-1, pH values range Zelené pleso Kežmarské, which lies at an altitude of from 7.1−7.7 and water temperatures are quite low 1545 m a.s.l. Other close localities of the species are (14.4−17.8°C), even during the vegetative season. situated in the Karkonosze Mountains, the second Five coccoid green algal taxa which are rarely noted highest mountain range in southern Poland, where in the world were found in these lakes: Actinastrum five climatic zones, including the subalpine and gracillimum var. elongatum, Monoraphidium tatrae, alpine, can be distinguished (Raj 2001). Schröder Pediastrum braunii, Scotiella tuberculata var. tuberculata (1898) observed P. braunii in these mountains, and Thelesphaera olivacea. The taxa were noted in including in a small pool close to a lake called Wielki different lakes, except for Th. olivacea, which was Staw and in some peat bogs situated in the found in both Wyżni Czerwony Stawek and Zmarzły borderland of Poland and the Czech Republic. The Staw. The two lakes are quite distant from each species was sought again in this area, but without other, situated in different parts of Dolina success (Kowalska 2010). P. braunii was found also in Gąsienicowa. The single findings of the remaining a dystrophic lake, Suchar Wielki, in Wigry National four taxa should not mean that their occurrences are Park (northeastern Poland) by Ryppowa (1927). restricted only to the particular lakes. It is possible Other European localities of the species are, e.g. in that they occur very rarely, making it very difficult to lakes of the Czornohora Mountains in the East find them regularly in each of the Tatra lakes. Carpathians of Ukraine (Wołoszyńska 1925), in Ötz Potentially, they could be distributed in other Tatra Tal, a valley in the Austrian Alps (Schmidle 1896), in lakes as well, and they only need to be found. Swedish Lapland (Skuja 1963), southern Greenland The taxa described above can be divided into two (Nygaard 1978), northwestern Finland (Weckström groups depending on their distribution in the world. et al. 2009) and in the British Isles (Guiry & Guiry The first group contains three species, Monoraphidium 2012). The species was also found in Taiwan tatrae, Pediastrum braunii and Thelesphaera olivacea, which (McManus & Lewis 2005) and China (Guiry & Guiry mostly occur in mountainous areas. 2012). Monoraphidium tatrae was previously observed in Details on distribution of the third species, some shallow pools in Malá Studená Dolina, which is Thelesphaera olivacea, remain scarce. As described by a valley situated in the alpine zone (ca. 2000 m a.s.l.) Fott (1976), Th. olivacea was observed on peat bogs

Some rare and interesting green algae from subalpine Tatra lakes (High Tatra Mountains, Poland)| 231 and in some pools in Pančavská louka, a subalpine that the number of poorly recognized green algae meadow in the Karkonosze Mountains (Czech living in the Tatra lakes is higher than already found. Republic). The other alpine species of the genus It will certainly increase with progress in the ongoing Thelesphaera, Th. alpina, which is morphologically very studies of these water bodies. close to Th. olivacea, was first found in Austria, including wet rocks close to Böckstein-Gastein, wet ACKNOWLEDGEMENTS places close to a peak called Ameringkogel (Packalps, Styria state) and Schleinitz, a river by Lienz, Tyrol We are grateful to the two anonymous reviewers state (Pascher 1943). Many years later the species was for valuable remarks on the manuscript and to also recorded at Lacul Stucilor, a lake in Romania Konrad Wołowski (Kraków, Poland) for helpful (Cărăuş 2002), semi-aerophytic habitats in Bratislava, advice during elaboration of the materials. This study Slovak Republic (Uher 2008), from Jaskinia was partly financed through the statutory fund of the Sąspowska, which is a cave in southern Poland Institute of Botany of the Polish Academy of (Czerwik-Marcinkowska & Mrozińska 2011) and Sciences, including a grant “Młodzi Naukowcy” in from Austria (Guiry & Guiry 2012). As mentioned 2011. above, we suppose that Th. olivacea and Th. alpina belong to the same species, owing to similar REFERENCES morphology and ecological requirements. The two other rarely occurring taxa, Actinastrum Biswas S. 1992. Phytoplankton periodicity in Ogelube Lake, gracillimum var. elongatum and Scotiella tuberculata var. Anambra State, Nigeria during 1979−1980. 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