Biodiversity and Conservation (2006) 15:3445–3457 DOI 10.1007/s10531-005-2008-5 Ó Springer 2006 -1 Red Data List of Charophytes in the Balkans JELENA BLAŽENČIĆ1,*, BRANKA STEVANOVIĆ1, ŽIVOJIN BLAŽENČIĆ2 and VLADIMIR STEVANOVIĆ1 1 Institute of Botany and Botanical Garden ‘‘Jevremovac’’, Faculty of Biology, University of Belgrade, Takovska 43, Belgrade 11000, Yugoslavia; 2Faculty of Veterinary Medicine, University of Belgrade, Belgrade, Yugoslavia; *Author for correspondence (e-mail: jblaz@eunet.yu; fax: +381-11-2769903) Received 17 August 2004; accepted in revised form 31 January 2005 Key words: Charophytes, Endemic species, Red list, Stoneworts, Threat categories Abstract. The occurrence of 47 species of all the six recent genera of charophytes recorded in the Balkans is demonstrated. Our aim was to assess their status of threat according to the 2001 IUCN threat categories and criteria, in order to establish the Red List of Charophytes distributed in the Balkan Peninsula. The List underlines the diversity of charophytes in this part of the world and provides guidelines for its conservation. Analysis of the charophytes in each category of threat has provided a general overview of their distribution, species richness, population features and possibility of survival throughout the various regions of the Balkan Peninsula. Introduction The Balkan Peninsula (SE Europe) is the richest and the most diverse region of the western Palaearctic regarding its general flora and vegetation (Stevanović 1999). It is distinguished also by a rich algal flora, of which charophytes are particularly important. This botanical luxuriance has resulted from historicalevolutionary changes of the living world and conditions of the habitat in this part of Europe, from the Tertiary, through the Ice Age, up to present day. The Peninsula abounds in different terrestrial and aquatic habitats, ranging from low-land to high-land regions, as well as those in the littoral parts of the Adriatic Sea. Generally, the Peninsula is bordered by aquatic ecosystems: the Sava and the Danube rivers in the north, the Mediterranean Sea in the south, the Black, Marmara and Aegean Seas in the east and south-east, and the Adriatic and Ionian Seas in the west. The geomorphologic, pedologic and hydrologic variety of the Balkan Peninsula provides exceptional richness in both algae and other plant groups, including a large number of endemic species. The Balkan Peninsula is characterized by numerous ‘hot-spots’, or centres of diversity, and by the important plant area (IPA), which features, in particular, the specific group of charophytes. Charophytes or stoneworts are a group of complex, macroscopic, advanced algae, of great importance for both their evolutionary and ecological significance. They are commonly a very important component of the underwater 3446 vegetation of certain, particularly oligotrophic, lakes, where they are the dominant aquatic plants forming dense underwater meadows. The stoneworts are very susceptible to nutrient enrichment, and are therefore good indicators of water quality, i.e. of clean, transparent aquatic ecosystems with strongly calcareous conditions. In the Balkan Peninsula the charophytes develop successfully in lakes, rivers, channels, ponds, puddles, springs, peat-bogs, fishponds, thermal and/or mineral waters, reservoirs and marshy meadows and so on. The fresh water habitats are always the richest in different charophyte species. There are also several species (Chara intermedia, Ch. aspera, Ch. baltica, Tolypella nidifica) that grow in brackish waters or in puddles with extremely salty water (Lamprothamnium papulosum) in a number of habitats along the Adriatic coast, although they are not fully marine species. However, most of these aquatic ecosystems are exposed to various kinds of human activities such as drying up, overgrowing, extensive tourism, agricultural measures, and wastes from industrial and urban facilities. The best preserved habitats, with rich, genuine charophyte populations, are those that are accessible only with difficulty to humans and their actions, in particular the charming glacial lakes. The floristic variety of charophytes in the Balkan Peninsula has been more or less thoroughly investigated, the extent of the research varying from country to country. This holds true also for the territory of the former Yugoslavia (which covered almost one half of the Balkan Peninsula) albeit, over the last 30 years, this group of algae has been continuously and meticulously examined (Blaženčić and Blaženčić 1988, 1995, 2003; Blaženčić et al. 1991; Bruinsma et al. 2000; Urbanc-Berčič 2003). In addition, during this period, there have been discovered new localities in which the populations of these algae are well preserved. Gathering together all the data available to us, we have compiled the first Red List of Charophytes of the Balkan Peninsula. The aim of the present work is to produce the Red List of Charophytes for the Balkans on the basis of the assessment of the threat degree by the application of new IUCN criteria (2001). This List should serve as a guideline and stimulus for further work on its improvement and revision, including the total number of charophytes and the threat category of each species. Material and methods The total number of taxa has been established on the basis of all data available to the authors, comprising our own field and herbaria investigation findings, and the numerous literature results on charophytes from all the Balkan countries. For Romania, only data relating to the locality from the flooded zone of the river Danube and the Romanian part of Dobrudja were included. There are no available data for the European part of Turkey. 3447 The stonewort species were determined according to the keys proposed by Corillion (1957, 1975), Gollerbah and Krasavina (1983), and Krause (1997), as well as on the basis of the data reported by Vilhelm (1912), Wood and Imahori (1964, 1965) and Blaženčić and Randelović (1994). Threat category assessments in this study correspond to the global 2001 IUCN Threat Categories and Criteria, which are applied to the regional level. The extent of occurrence and area of occupancy are estimated as if the species were distributed only in the Balkan Peninsula. The basic criteria for determining the threat category are the number of localities and the state of the species populations, i.e. the degree of their habitat fragmentation and/or population decline. The species were thus classified into the following categories: EX (glob) – globally extinct; CR (glob) – globally critically endangered; EX (Balk) – extinct in the Balkans; CR (Balk) – critically endangered in the Balkans; EN (Balk) – endangered in the Balkans; VU (Balk) – vulnerable in the Balkans, and LR (Balk) – lower risk in the Balkans. To assess IUCN threat categories on the regional and national (single country) scale we applied the software programme designed by Niketić (1999) for the closely related criteria and sub-criteria for the vascular flora of Serbia, presented in The Red Data Book of the Flora of Serbia – Extinct and Critically Endangered Taxa (Stevanović 1999). Results and discussion According to Krause (1997), about 400 species of charophytes are known world-wide and 54 in Europe. We assumed 62 species of charophytes in Europe taking into account the number of Krause (1997) as well as the records of particular species reported by Vilhelm (1912), Wood and Imahori (1964, 1965), Blaženčić and Randelović (1994), Kashta (1994), and Schubert and Blindow (2003). Hitherto, 47 species were recorded in the flora of the Balkan Peninsula (Table 1) which accounts for 76% of the species of charophytes recorded in Europe (62 species) or about 12% of the registered charophyte species worldwide (400 species). These data confirm the floristic richness of stoneworts in the area studied. Thus, in the aquatic ecosystems in the Balkan Peninsula, species of all recent genera of charophytes are present, viz. Chara (28 species), Nitella (10 species), Tolypella (6 species), Lamprothamnium (1 species), Lychnothamnus (1 species) and Nitellopsis (1 species). Such a floristic richness of stoneworts in the Balkan Peninsula results from their marked evolutionary ability to adapt to various aquatic environments, of climatically different zones, and determined by the different physico-chemical properties of the water. Thus, in some regions of the Balkan Peninsula, charophytes have been recorded in fresh waters (Petkov 1913; Ionescu-Teculescu 1970; Randelović et al. 1993; Koumpli-Sovantzi 1997; Bruinsma et al. 2000; Urbanc-Berčič 2003), salty waters (Blaženčić and Blaženčić 1990), 3448 Table 1. The list of Charophytes of the Balkan countriesa. Species Country SCG CRO FYRMa SLO B&H BG RO GR AL 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 17 16 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 Chara aspera Deth. ex Willd Chara baltica Bruz. Chara braunii Gm. Chara conimbrigensis G. Da C. Chara canescens Desv. & Lois Chara connivens Saltzm. Chara conniventi-fragilis Hy Chara contraria A. Br. Chara corfuensis J. Gr. ex Fil. Chara fragifera Dur. de la Mais. Chara galioides DC. Chara globularis Thuill. Chara hispida L. Chara hydropitys Reih Chara imperfecta A. Br. Chara intermedia A.Br. Chara kokeilii A. Br. Chara muscosa J. Gr. et B.-W. Chara ohridana Kostic Chara polyacantha A. Br. Chara rohlenae Vilh. Chara rudis A. Br. Chara strigosa A. Br. Chara tenuispina A. Br. Chara tomentosa L. Chara virgata Kütz. Chara visianii J. Blaz. & V. Randj. Chara vulgaris L. Lamprothamnium papulosum (Wallr). J. Gr. Lychnothamnus barbatus (Meyen) v. Leonh. Nitella capillaris (Krock) J. Gr. et B.-W. Nitella flexilis Ag. Nitella confervacea (Brèb). A. Br. Nitella gracilis Ag. Nitella hyalina (DC) Ag. Nitella mucronata A. Br. Nitella opaca Ag. Nitella syncarpa (Thuill). Kütz. Nitella tenuissima (Desv). Kütz. Nitella translucens (Pers). Ag. Nitellopsis obtusa (Desv. in Lois) J. Gr. Tolypella glomerata (Desv)v. Leonh Tolypella hispanica Nords. Tolypella intricata (Trent) v. Leonh + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + + 3449 Table 1. Continueda. Species Country SCG CRO FYRMa SLO BH BG RO GR AL 45 Tolypella nidifica (Müller) A. Br. 46 Tolypella prolifera (Ziz). v. Leonh. + 47 Tolypella salina R.Cor.. + + + + + a The abbreviations of the Balkan countries: SCG – Serbia Montenegro, CRO – Croatia, FYRMa – FYR Macedonia, SLO – Slovenia, B H – Bosnia Herzegovina, BG – Bulgaria, RO – Romania, GR – Greece, AL – Albania. brackish (Zavodnik 1968; Urbanc-Berčič 2003) and mineral waters (Vouk 1919; Tortić-Njegovan 1956; Blaženčić 1984). The localities in which these algae were recorded range from lowland (Blaženčić et al. 1995) to montane and high mountain regions (Vilhelm 1912; Vodeničarov 1963; Blaženčić et al. 1990; Bruinsma et al. 2000). Glacial lakes are particularly interesting, given that stoneworts are dominant in these lakes that confer physiognomic character to aquatic vegetation (Blaženčić and Blaženčić 1988, 1995). Recently, interest in charophytes in the Balkan Peninsula has been intensified, notably in Slovenia (Bruinsma et al. 2000; Urbanc-Berčič 2003), Albania (Kashta 1994, Rakaj and Kashta 1999), Greece (Raabe and Koumpli-Sovantzi 2000, 2002; Raus and Raabe 2002) and Macedonia (Trajanovska 2002; Trajanovska et al. 2004). For each of the 47 charophyte species recorded in the Balkan Peninsula, the threat category, and the criteria and sub-criteria for its vulnerability have been established (Table 2). The present Red List of Charophytes inhabiting the Balkan Peninsula reveals that more than 80% of these algae are to some degree endangered. About 19% of charophyte species belong to globally threatened taxa that are at the same time Balkan endemics or rare species occurring either in a few localities in Europe or throughout the world. Figure 1 reveals the percentage occurrence of all established threat categories of stonewort species recorded in the Balkans. These data clearly indicate that more than 60% of the total number of stonewort species are either critically endangered (36, 1%) or endangered (27, 6%). It should be noted, however, that in the Balkans currently only seven species of stoneworts have a lower risk status (Table 2). About one third of the total number of charophytes present in the Balkan Peninsula are rare and critically endangered species, given that they occur in only a few localities or are present in reduced populations, mainly due to altered environmental conditions. Among these are four endemic species: Chara rohlenae, Ch. visianii, Ch. corfuensis and Ch. ohridana (Figure 2). Today, the existence of Ch. rohlenae is doubtful, given that for more than 70 years there have been no new (confirmed) records. The other three endemic species 3450 Table 2. IUCN Threat categories and criteria of the Charophytes distributed in the Balkans. 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 Species Category Chara rohlenae Chara visianii Chara corfuensis Chara ohridana Chara conniventi-fragilis Chara conimbrigensis Chara muscosa Tolypella salina Chara kokeilii Chara imperfecta Tolypella nidifica Chara galioides Tolypella hispanica Chara baltica Nitella translucens Chara hydropytis Chara strigosa Chara fragifera Nitella hyalina Chara intermedia Chara polyacantha Nitella confervacea Tolypella glomerata Tolypella prolifera Chara connivens Nitella gracilis Lychnothamnus barbarus Lamprothamnium papulosum Chara rudis Tolypella intricata Chara tenuispina Nitella syncarpa Nitella tenuissima Chara canescens Chara tomentosa Nitella capillaris Chara hispida Nitella mucronata Nitella flexilis Nitellopsis obtusa Nitella opaca Chara braunii Chara contraria Chara globularis Chara aspera Chara virgata Chara vulgaris EX (glob) (?) CR (glob) CR (glob) CR (glob) CR (glob) CR (glob) CR (glob) CR (glob) CR (glob) EX (Balk) (?) CR (Balk) CR (Balk) CR (Balk) CR (Balk) CR (Balk) CR (Balk) CR (Balk) CR (Balk) CR (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) EN (Balk) VU (Balk) VU (Balk) VU (Balk) VU (Balk) VU (Balk) VU (Balk) VU (Balk) VU (Balk) LR (Balk) LR (Balk) LR (Balk) LR (Balk) LR (Balk) LR (Balk) LR (Balk) Criteria B1-A1e B1-A1e B1-A1e B1-A1e B1 B1 B1 B1 B1-B2a-e B1 B1 B1-B2c B1-B2a-c B3b B3b B3b B3b B3b B1 B1 B1 B1 B1 B1 B1 B2b-c B2c B2c B2c B2c B1 B1 B1 B1 D2 D2 D2 D2 1nt 1nt 2nt 2nt 2nt 2nt 1c 3451 Figure 1. Percentage of IUCN threat categories of charophytes recorded in the Balkans. Figure 2. Distribution of four endemic Charophytes in the Balkan Peninsula. 3452 were recorded in one or a few localities only. Thus, Ch. visianii was found in the Krka river in the vicinity of the Skradin cascades in Croatia (Blaženčić and Randelović 1994), Ch. corfuensis in Baćinska Lakes in Croatia and also on Corfu in Greece (Blaženčić and Blaženčić 2002, 2003), and Ch. ohridana on the Ohrid Lake in Macedonia (Krause 1997; Blaženčić 2004) and in the ponds along the banks of the Dojran Lake, also in Macedonia where the populations are very small and highly endangered due to drying up (Blaženčić and Blaženčić 1997, 1999). Some species of charophytes that are present in a small number of localities, such as the critically endangered Ch. kokeilii and Ch. strigosa (Figure 3). The species Ch. conimbrigensis and Ch. conniventi-fragilis, which occur along the bank of the Dojran Lake in Macedonia (Blaženčić and Blaženčić 1997, 1999), and Ch. muscosa in Lake Vražje on Mount Durmitor in Montenegro (Blaženčić and Blaženčić 2002), are designated critically endangered, given that their presence in the Balkans was established in these localities only (Figure 3). Further, the species Ch. galioides, Tolypella hispanica and T. salina were Figure 3. Distribution of some endangered Charophyte species recorded in only one or a few localities in the Balkans. 3453 recorded at only one locality in Greece, the former two on NW Peloponesus (Raabe and Koumpli-Sovantzi 2000, 2002), and T. salina in the surroundings of Athens (U. Raabe, personal communication). The species Ch. baltica,recorded in a brackish lake Fiesta in Slovenia, also belongs to this category (Firbas and Al-Sabti 1995). In the Balkans, the species Tolypella nidifica, Ch. strigosa and Ch. kokeilii occur in small populations because their habitats have been destroyed, resulting in the rapid decline and even disappearance of some of these populations. Thus, Tolypella nidifica, which was previously recorded in several localities in Croatia, now inhabits, with certainty, only the river Zrmanja between Obrovac and its mouth into the Adriatic Sea (Blaženčić et al. 1998). The species Ch. kokeilii is rare, in general, in Europe (Krause 1997) – even inGermany it is treated as an extinct species (Weyer and Raabe 1999). Due to their ecological requirements, charophytes are an extremely endangered algal group, given that their habitats are fragmented or even destroyed to a greater or lesser extent either physically (by draining) or due to the change in physical–chemical characteristics (primarily by eutrophication processes). In fact, most members of the charophyte genera distributed in the Balkan Peninsula belong to some category of threat (critically endangered, endangered or vulnerable). Nevertheless, some species, notably those of the genus Chara that are widely distributed (Chara vulgaris, Ch. contraria), are more adaptive to unfavourable conditions and are able to survive them for shorter or longer periods of time. However, out of 28 species of the genus Chara recorded in the Balkan Peninsula, 2 species are considered extinct, and as many as 17 belong to the category of critically endangered or endangered (globally or in the Balkans), since they have been recorded in only a few localities or their populations are reduced. It should be noted that the members of all other genera of charophytes are also much endangered, their habitats being disturbed (fragmented) and population reduced or restricted, and therefore require strict protective measures. By comparing Red Lists of Charophytes of different European countries, it is noticeable that the same species belong to the category of critically endangered and endangered, both in Europe in general and in the Balkans. Furthermore, the number of species that belong to the low risk category in the Balkans, such as N. opaca, Ch. contraria, Ch. aspera, Ch. virgata, are classified as endangered in Germany, whereas Ch. brauni is ranked as vulnerable in Sweden and even as critically endangered in Germany (Schmidt et al. 1996; Blindow 2000). Data on the occurrence and abundance of charophytes, as well as on their distribution, are constantly accumulating and subject to revision (Bruinsma et al. 2000; Raabe and Koumpli-Sovantzi 2000, 2002; Raus and Raabe 2002; Talevska and Trajanovska 2002; Trajanovska 2002; Trajanovski et al. 2002; Urbanc-Berčič 2003). Therefore it may be concluded that the charophyte flora of the Balkan Peninsula is still insufficiently well known and that its entire richness has not yet been recognized. 3454 The occurrence and numbers of charophytes vary with the change in ecological conditions in their habitats. Thus, the presence of these algae has been observed to fluctuate in the ponds around the Dojran Lake in Macedonia (Blaženčić and Blaženčić 1997, 1999), in the fishponds of Vojvodina in Serbia (Blaženčić and Blaženčić 1995), and in a number of rivers and channels (Janković and Janković 1987; Blaženčić 1995). In contrast, regions abounding in large lakes or lake complexes are characterized by richness and diversity in charophyte genera and species. Such is Lake Skadar with 24 recorded species belonging to 4 genera (Chara, Nitella, Tolypella and Nitellopsis), Lake Ohrid with 15 species belonging to 3 genera (Chara, Nitella, Tolypella), the Baćinska Lakes with 12 species and the Krka river with 9 species belonging to 4 genera (Chara, Nitella, Nitellopsis and Lychnothamnus), as well as the glacial lakes of Mount Durmitor with 10 species belonging to two genera (Chara and Nitella). Besides, 14 species belonging to 5 genera (Chara, Nitella, Nitellopsis, Tolypella and Lamprothamnium) were recorded in the lower watercourse and on the mouth of the Neretva river in the Adriatic Sea. Therefore, all these sites may be considered as ‘hot-spots’ and potential centres of diversity of charophytes in the Balkan Peninsula (Figure 4). The populations of charophytes in the flooded areas of lowland rivers in the southern part of the Pannonian Plain are severely affected by the adverse effects of pollution because of the waste water influxes loaded with organic Figure 4. Potential centres of diversity of Charophytes in the Balkan peninsula. 3455 substances from industrial and urban facilities, as well as from arable lands on which chemical fertilizers and herbicides are used. The survival of these algae is also jeopardized in drying up wetlands (the Negotin Marsh) as well as in aquatic ecosystems of tourist centres (lakes in Mount Durmitor), aquatic habitats along the shores of sea resorts, etc. Bearing all these facts in mind, it is necessary to start with the protection of these regions since, by conserving the habitats, the existence of charophytes will be assured. This will contribute to the overall preservation of natural resources in the Balkan Peninsula as a part of Europe famed for its exceptional diversity. 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