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ACTA ZOOLOGICA BULGARICAActa zool. bulg., 66 (3), 2014: 347-358

Zoogeography and FaunisticsResearch Article

IntroductionProtozoa are ubiquitous; they are present in an ac-tive state in all aquatic or moist environments, while their cysts are present everywhere in the biosphere, ready to give rise to active populations. Protozoans play an important role in many natural communi-ties, although they are often overlooked (Taylor, SanderS 2001).

The taxon Protozoa is attributed to Georg August Goldfuss, who proposed the term in 1818 to embrace the ‘infusoria’, some bryozoans, and vari-ous other small animal-like creatures; however, it was not until the mid-19th century that the term was first used to refer exclusively to single-celled organisms (Finlay, eSTeban 1998). In the revised six-kingdom system, 34 out of the 57 living phyla consist entirely or largely of unicellular species (Cavalier-SmiTh 2004). Freshwater protozoans are found in 16 of the 34 protist phyla (Finlay, eSTeban 1998).

Taxonomic status of Protozoa has always been subject to various revisions. Although Protozoa was considered to be a single phylum of eukaryotic animals in early classifications, modern treatments distribute them among many phyla or higher taxa (Taylor, SanderS 2001). WhiTTaker (1969) grouped them within the kingdom of protists with other uni-

cellular eukaryotes. Cavalier-SmiTh (1981, 1983) marked them as individual kingdom. The same author made several revisions within the kingdom afterwards (Cavalier-SmiTh 2004), and even seg-regated some groups (i.e. Foraminifera, Radiolaria, Heliozoa, Ciliophora) from the kingdom Protozoa and included them into the kingdom Chromista (Cavalier-SmiTh 2009). By all means, it is difficult to find generally accepted classification of protists (ParFrey et al. 2006). In the revised classification of eukaryotes, adl et al. (2012) offered the division of eukaryotes into five supergroups (Amoebozoa, Opisthoconta, Excavata, SAR, Archaeplastida), while taxa with unclear status were classified into Incertae sedis Eukaryiota. The representatives of heterotrophic protists belong to the supergroups Amoebozoa, Excavata and SAR.

For the purpose of this paper, we define the term Protozoa as those unicellular or colonial eukaryotes that are heterotrophic. Furthermore, we will restrict ourselves to a discussion of free-living, phagotroph-ic forms in freshwater.

Most probably, due to small dimensions of bodies as well as difficulties with identifications, the fauna of freshwater protists has not been re-

Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia

Aleksandar M. Ostojić*, Ivana D. Radojević, Milica P. Rakić

Institute of Biology and Ecology, Faculty of Science, University of Kragujevac, 34000 Kragujevac, Serbia; *E-mail: ostojic@kg.ac.rs

Abstract: This paper presents a checklist of freshwater free-living species of unicellular heterotrophic protists in the territory of Serbia. The list was made based on published papers and field research of the authors. A total of 161 taxa were recorded: 160 taxa of three supergroups, Amebozoa, SAR and Excavata, and one taxon from Incertae sedis Eukaryota. Most of the taxa are generally widespread. Several new species of Difflugiidae, unknown to science, were discovered from Vlasina peat bog and the Danube River.

Key words: Protists, Amebozoa, SAR, Excavata, Serbia

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searched intensively, especially in relation to vari-ous groups of multicellular animals. The estimates of the number of the species described on our planet vary. For the kingdom Animalia, 1 552 319 species were described in 40 phyla, according to a new evo-lutionary classification (Zhang 2011). mora et al. (2011) estimated the total number of species of eu-karyotes based on mathematical and statistical mod-els. Their approach predicted ~7.77 million species of animals, ~298 000 species of plants, ~611 000 species of fungi, ~36 400 species of protozoa, and ~27 500 species of chromists; in total the approach predicted that ~8.74 million species of eukaryotes exist on Earth.

According to balian et al. (2008) 2392 spe-cies of freshwater protists has been described so far, while the number of described species of freshwater Metazoa is 125 531.

The situation in Serbia is similar. The research on freshwater zooplankton in the territory of Sebia started at the beginning of the 2th century and pri-marily reffered to the fauna of Rotifera, Cladocera and Copepoda (OstOjić 2010). The fauna of the free-living freshwater protists was sporadically re-searched and a great number of results was presented at local conferences and published in the proceed-ings. Therefore, little is known about the diversity and distribution of those protists in the territory of Serbia. Since, apart from the several papers of Anđelija Živković, no other authors dedicated their research to this group, the existing data are very poor. According to Kalafatić (1995), 236 species of Testacea from 28 families were recorded in the terri-tory of former Yugoslavia (Serbia and Montenegro). However, this number includes some unpublished data by A. Živković, which makes the number of species indicated in the published papers smaller.

The objective of this paper is to summarise all the data regarding the number of recorded taxa of free-living freshwater protists in Serbia.

Material and MethodsThe present checklist was compiled using published

records and original data, mostly from the recent field work of the authors (for details about the sampling methodology and sampling localities see OstOjić et al. 2012). We used data published in journals, as well as those in the proceedings from Serbian and international conferences. Only the taxa that belong to free-living freshwater heterotrophic protists were included in the checklist. The checklist comprises the valid name of each taxon and a reference of the first records in Serbia.

ResultsAltogether, 160 taxa of free-living freshwater heter-otrophic protists of three supergroups and one taxon from Incertae sedis Eukaryota, or in total 161 taxa, were recorded in the territory of Serbia (Table 1). The greatest number of taxa (128) was identified on the level of species, 23 taxa were identified on the level of genus, while within the groups Amebozoa and SAR ten taxa were identified below the genus level (subspecies, variety or form – see the list of taxa in Table 2).

DiscussionDuring recent years, based on molecular research, there have been great changes in taxonomy of Protozoa (adl et al. 2005, 2012, nikolaev et al. 2004, Cavalier-SmiTh 2009, PaWloWSki, burki 2009). Rhizopoda (the former superclass Rhizopodea, which comprised protists that have lopobodia, filopodia, and reticulopodia) were subdivided into Amoebozoa and Rhizaria. The supergroup Amoebozoa includes all naked and testate lobose amoebae, which are tra-ditionally classified in the class Lobosea (PaWloWSki, burki 2009), while Rhizaria is a supergroup of eu-karyotes, most recently recognised, which includes commonly organisms bearing “root-like reticulose or filose pseudopodia” (Cavalier-SmiTh 2002, cit. PaWloWSki, burki 2009). This supergroup contains the majority of protists that were traditionally classi-fied among Rhizopoda (Filosea, Granuloreticulosea) and Actinopoda (PaWloWSki, burki 2009).

Table 1. The number of recorded taxa of free-living freshwater heterotrophic protists in Serbia and their taxonomic level

Supergroups Genus sp. Species Ssp./var./f. Total

Amebozoa 5 74 8 87SAR 17 53 2 72Excavata 1 1Incertae sedis Eukaryota 1 1Total 23 128 10 161

Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia

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Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia

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On the grounds of ultrastructure-based stud-ies and molecular evidence (nikolaev et al. 2004), “Heliozoa” represents an artificial assemblage. Thus, phylum Actinophryida (which includes all the species of heliozoans recorded in Serbia), as well as Ciliophora, were placed in the supergroup Chromalveolata (adl et al. 2005), or Chromista (Cavalier-SmiTh 2009). In the revised classification of eukaryotes (adl et al. 2012), the status of so-called supergroups Amebozoa and Excavata remained the same. However, Rhizaria, with Alveolata (which includes Ciliophora) and Stramenopiles (which in-cludes Actinophryida), were included in a new su-pergroup – SAR. Some groups, namely those with unclear status (e.g., Acanthocystis), were marked as Incertae sedis Eukaryota.

The greatest number of recorded taxa in Serbia belongs to the groups of Amebozoa (Tubulinea) and SAR (Rhizaria) (Table 2). This conclusion is based primarily on the results of the research by the out-standing Bulgarian protozoologist golemanSky (1966, 1968) and of the studies by ŽivKOvić (1975a,b, MilOvanOvić, ŽivKOvić 1950, 1953, 1963, ogden, ŽivKOvić 1983). As may be seen from the present checklist of the recorded freshwater protists in Serbia, they are mostly widespread generally. At the same time, thanks to the detailed morphological investiga-tions of Difflugiidae collected from Vlasina peat bog, several new species, unknown to science so far, were discovered (Ogden, ŽivKOvić 1983), as follows:

Cucurbitella vlasinensis Ogden and Živković, 1983

Difflugia balcanica Ogden and Živković, 1983Difflugia bistrica Ogden and Živković, 1983Difflugia dragana Ogden and Živković, 1983Difflugia serbica Ogden and Živković, 1983Difflugia serrata Ogden and Živković, 1983Difflugia styla Ogden and Živković, 1983Pontigulasia montana Ogden and Živković,

1983 ogden (1987) attributed P. montana to the ge-

nus Lagenodifflugia on the basis of having a single opening in a well constructed diaphragm – L. mo-natana (Ogden and Živković, 1983).

In addition to the abovementioned species, Živković described three more species, new to sci-ence, discovered in the Danube River (ŽivKOvić 1975a,b):

Colaropyxidia stankovicii Živković, 1975Protocucurbitella danubialis Živković, 1975Protocucurbitella longicornis Živković, 1975Some of these species were recorded later

in other countries: bobrov et al. (2012) found C. vlasinensis in Donghu Lake (China); Todorov,

golemanSky (1998) found D. balcanica in Ezerets Lake (Northeastern Bulgaria) and davidova (2012) ascertained the same species in Ovcharitsa Reservoir (Southeastern Bulgaria); davidova et al. (2008) found D. bistrica in Ticha Reservoir (Northeastern Bulgaria); davidova et al. (2008) found D. dragana in Ticha Reservoir (Northeastern Bulgaria), as well as davidova, vaSilev (2012) in Durankulak Lake (Northeastern Bulgaria), davidova (2010) in Rabisha Reservoir (Northwestern Bulgaria) and davidova (2012) in Ovcharitsa Reservoir (Southeastern Bulgaria); Todorov et al. (2008) found D. ser-bica in the Batak Reservoir (Southern Bulgaria) as well as davidova et al. (2008) in Ticha Reservoir (Northeastern Bulgaria) and davidova (2012) in Ovcharitsa Reservoir (Southeastern Bulgaria); davidova (2010) found D. styla in Rabisha Reservoir (Northwestern Bulgaria); bobrov et al. (2012) found P. montana in Moshan hill and Donghu Lake floodplain (China), but it is listed as Lagenodifflugia montana (Ogden and Živković, 1983) Ogden 1987; ChardeZ, gaSPar (1984) found P. danubialis in Belgium (near Arden) and Snegovaya, alekPerov (2010) in the Kamishevka River (Azerbaijan).

When it comes to the fauna of the free-living freshwater heterotrophic protists in neighbouring countries, the data are partially available. In Former Yugoslav Republic of Macedonia a smaller number of taxa was recorded in relation to Serbia, 42 species, 37 of which are restricted to Lake Ohrid (griFFin, PeTkovSki 2001), while the higher number of taxa was recorded in Croatia, 268 taxa (RadOvić et al. 2009). The best studied is the fauna of Bulgaria, pri-marily the fauna of testacenas. golemanSky, Todorov (1993) recorded a total of 78 taxa of testate amoebae in Beli Iskar Reservoir (the Rila Mountin). Todorov, golemanSky (1998) recorded 93 taxa belonging to 22 genera of testate amoebae in the coastal lakes Shabla and Ezerets (Northeastern Bulgaria). The same authors recorded 118 taxa testaceans belong-ing to 31 genera in glacial lakes in the Rila National Park (Todorov, golemanSky 2000). Todorov (2005) reported 86 taxa testaceans, belonging to 26 genera, collected from the benthos, the littoral zone and the wet coastal mosses of the Smradlivo Ezero glacial lake in the Rila National Park. A total of 197 species and varieties belonging to 44 genera of naked and testate amoebae were found in 31 localities at differ-ent habitats of the Western Rhodopes (golemanSky et al. 2006). davidova et al. (2008) found 104 taxa (species and varieties) belonging to 24 genera of testate amoebae in three biotopes of the Ticha Reservoir (Northeastern Bulgaria). TODOROV et al. (2008) reported 93 taxa of testate amoebae in

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Received: 09.12.2013 Accepted: 27.05.2014