Zoogeography and Faunistics
Research Article
ACTA ZOOLOGICA BULGARICA
Acta zool. bulg., 66 (3), 2014: 347-358
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: [email protected]
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
Introduction
Protozoa are ubiquitous; they are present in an active 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 communities, 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 various 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 segregated 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, phagotrophic 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 re347
Ostojić A., I. Radojević, M. Rakić
searched intensively, especially in relation to various 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 evolutionary classification (Zhang 2011). Mora et al.
(2011) estimated the total number of species of eukaryotes based on mathematical and statistical models. 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 species 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 primarily reffered to the fauna of Rotifera, Cladocera
and Copepoda (Ostojić 2010). The fauna of the
free-living freshwater protists was sporadically researched and a great number of results was presented
at local conferences and published in the proceedings. 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 territory 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 Methods
The 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.
Results
Altogether, 160 taxa of free-living freshwater heterotrophic 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).
Discussion
During 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 traditionally classified in the class Lobosea (Pawlowski,
Burki 2009), while Rhizaria is a supergroup of eukaryotes, 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 classified 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
87
SAR
17
53
2
72
Excavata
1
Incertae sedis Eukaryota
1
Total
23
348
1
1
128
10
161
Table 2. An updated list of the freshwater heterotrophic protist taxa of Serbia. Classification of the higher ranks of the protists was made according Adl et al. (2012)
Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia
349
Table 2. Continued
Ostojić A., I. Radojević, M. Rakić
350
Table 2. Continued
Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia
351
Table 2. Continued
Ostojić A., I. Radojević, M. Rakić
352
Table 2. Continued
Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia
353
Table 2. Continued
Ostojić A., I. Radojević, M. Rakić
354
Updated Checklist of Freshwater Free-living Unicellular Heterotrophic Protists of Serbia
On the grounds of ultrastructure-based studies 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 includes Actinophryida), were included in a new supergroup – 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 outstanding 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 investigations 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, 1983
Difflugia bistrica Ogden and Živković, 1983
Difflugia dragana Ogden and Živković, 1983
Difflugia serbica Ogden and Živković, 1983
Difflugia serrata Ogden and Živković, 1983
Difflugia styla Ogden and Živković, 1983
Pontigulasia montana Ogden and Živković,
1983
Ogden (1987) attributed P. montana to the genus Lagenodifflugia on the basis of having a single
opening in a well constructed diaphragm – L. monatana (Ogden and Živković, 1983).
In addition to the abovementioned species,
Živković described three more species, new to science, discovered in the Danube River (Živković
1975a,b):
Colaropyxidia stankovicii Živković, 1975
Protocucurbitella danubialis Živković, 1975
Protocucurbitella longicornis Živković, 1975
Some 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. serbica 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, primarily 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 belonging 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 different 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
355
Ostojić A., I. Radojević, M. Rakić
the Batak Reservoir (Southern Bulgaria). A total
of 78 species and varieties, belonging to 19 genera, were identified in the benthal and in the phytal
of the Rabisha Reservoir (Northwestern Bulgaria)
(Davidova 2010). Davidova (2012) found 75 taxa
in Ovcharitsa Reservoir (Southeastern Bulgaria)
and Davidova, Vasilev (2012) 91 taxa of the testae
amoebae, belonging to 20 genera, in Durankulak
Lake (Northeastern Bulgaria).
More detailed studies of the freshwater protist
fauna should be conducted in order to obtain more
realistic representation of their diversity and distribution in Serbia. Such studies have to include not
only field sampling, but also application of contemporary microscopic and molecular research.
Acknowledgements: We are deeply grateful to an anonymous
referee for his valuable critique and suggestions.
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Received: 09.12.2013
Accepted: 27.05.2014