Diversity of Cyanobacteria in the Zasavica River, Serbia
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Arch. Biol. Sci., Belgrade, 67(2), 355-366, 2015 DOI:10.2298/ABS141023024P Diversity of Cyanobacteria in the Zasavica River, Serbia Dragana Predojević1,*, Slađana Popović1, Željko Kljajić2, Gordana Subakov-Simić1, Ana Blagojević1, Jelena Jovanović1 and Milojko Lazić2 1 Faculty of Biology, Institute of Botany and Botanical Garden “Jevremovac”, University of Belgrade, 11000 Belgrade, Serbia 2 Faculty of Mining and Geology, Department of Hydrogeology, University of Belgrade, 11000 Belgrade, Serbia *Corresponding author: [email protected] Abstract: Cyanobacteria are ancient organisms that are capable of colonizing different habitats in various climatic zones due to their plasticity and rapid accommodation. They are a widely studied group of microorganisms due to the presence of many potentially toxic and invasive species. The aim of this research was a diversity exploration of the freshwater Cyanobacteria in the Zasavica River, which is part of the Special Nature Reserve “Zasavica” in Serbia. Organisms were sampled once a month at two study sites during one year. Phytoplankton and metaphyton analysis showed the presence of 50 freshwater cyanobacterial taxa, of which 12 are new taxa for Serbia. Three invasive and potentially toxic species (Cylindrospermopsis raciborskii, Sphaerospermopsis aphanizomenoides and Raphidiopsis mediterranea) were recorded only in metaphyton in April at one site. It can be expected that, if conditions change, this species can migrate and form phytoplankton blooms. Key words: Cyanobacteria; Zasavica; toxic; invasive Received October 23, 2014; Revised January 20, 2015; Accepted January 22, 2015 INTRODUCTION phytoplankton in most of the world’s surface wa- ters. They fulfill key roles in the biogeochemical Cyanobacteria, also known as blue-green algae, are cycling of matter and in the structure, maintenance ancient, cosmopolitan inhabitants of fresh, brack- and biodiversity of microbial and higher organism ish and marine environments, of soil and moist communities (Codd et al., 2005). However, high surfaces. Their plasticity and rapid accommodation cyanobacterial biomass has long been recognized make them very successful organisms that are able mainly as a cause of taste and odor problems in to colonize different habitats in various climatic freshwater bodies, but it also contributes to aes- zones. Cyanobacteria are a natural component of thetic problems, reduces recreational use, etc. 355 356 Predojević et al. The increase in human population and the 2007, 2009, 2013) has been recognized as a seri- consequent intensification of agriculture and in- ous problem and is of important socioeconomic dustry along with deficient water management concern in many places worldwide. Knowledge lead to the enhancement of eutrophication in many about the function of these species, their toxins freshwater bodies (De Figueiredo et al., 2004). The and the distribution of particular compounds occurrence of phytoplanktonic blooms, caused by that cyanobacteria of different genotypes, mor- the appearance of cyanobacteria in high biomass, photypes and ecology produce, is important for is also becoming more frequent worldwide. Many hydrobiology and water quality monitoring, as cyanobacterial species produce toxins that cause well as theoretical studies about diversity and mortality or illness in freshwater organisms, live- chemotaxonomy (Hrouzek, 2010). Noteworthy stock and even humans (Chorus at al., 2000; Codd, is that not all cyanobacterial blooms are toxic, 2000; Duy et al., 2000; Hitzfeld et al., 2000; Car- neither are all strains within one species. Toxic michael, 2001; De Figueiredo et al., 2004; Svirčev and non-toxic strains show no predictable dif- et al., 2009; Karadžić, 2011). The presence of algal ference in appearance (Spoof et al., 2003). Envi- toxins in the aquatic environment (Svirčev at al., ronmental conditions such as higher temperature Table 1. Results of physicochemical analysis during the study period (from December 2012 to November 2013) at both study sites. Month Temperature Transpar- Conductivity Depth (m) pH Thickness Dissolved (ºC) ency (m) (μs cm-1) of ice oxygen (m) (mg L-1) M XII 0.6 1 250 1 8.42 0.07 15.1 I 4.5 1.4 420 1.4 8.38 0 12.6 O II 6.7 0.9 470 1.4 8.07 0 10.5 III 15.2 1.2 780 1.2 8 0 12.1 L IV 19.6 1.4 700 1.4 7.92 0 10.2 V 18.7 1.7 760 1.7 7.77 0 3.9 O VI 22.6 1.3 710 1.4 8.1 0 9 VII 28.3 0.95 585 1.1 7.81 0 9.27 VIII 20.9 0.95 500 0.95 7.75 0 0.24 IX 13.2 0.95 595 0.95 7.6 0 3.45 X 14.7 1.1 680 1.1 7.88 0 6.45 XI 0.4 1.2 438 1.2 8.45 0 13.12 M XII 2.1 0.8 480 0.9 8.82 0.1 14.1 I 3.3 1.35 462 1.35 8.4 0 15.2 O II 6.2 1.3 500 1.3 8.08 0 12 III 14.4 1.3 820 1.3 7.87 0 11.5 S IV 18.8 1.3 745 1.3 7.8 0 7.5 V 18.1 1.7 725 1.7 7.79 0 1.92 T VI 21.2 1.3 720 1.3 7.6 0 1.59 VII 25 0.2 600 1 7.56 0 7.85 I VIII 19.4 0.48 472 0.48 8 0 2.16 IX 12.6 0.75 485 0.75 8 0 5.6 Ć X 11 0.4 490 0.4 8.14 0 5.98 XI 3.9 0.9 598 0.9 8.23 0 11.9 CYanobacteria of the Zasavica River 357 and pH values, low turbulence and high nutri- The aim of this research was to explore the di- ent inputs (particularly phosphorus, as well as versity of freshwater cyanobacteria in the River nitrogen) favor the development of planktonic Zasavica with special attention to the presence cyanobacteria. Some advantageous characteristics, of potentially toxic species. such as lower nutrient requirements and buoyan- cy regulation in the water column for achieving MATERIALS AND METHODS better light and nutrient level conditions, make some species dominant at the surface water layer The Zasavica River is the center of the Special (De Figueiredo et al., 2004). Nature Reserve “Zasavica” in Serbia (Predojević et al., 2014; Predojević et al., 2015) which has There are numerous papers from the previ- very high biodiversity. This river can be charac- ous floristic, taxonomic and ecological studies terized as both flowing and standing water ac- in Serbia that contain information about taxa cording to its properties. from Cyanobacteria division. The presence of Cyanobacteria in Serbia is first mentioned in The samples for physicochemical and biologi- a hydrobiology study by Schaarschmidt (1883). cal analyses from the Zasavica River were taken Fig 1. Photographs of potentially toxic Cyanobacteria taxa in the Zasavica River during the study period: (a) Cylindrospermopsis raciborskii; (b) Woronichinia naegeliana; (c) Oscillatoria limosa; (d) Microcystis aeruginosa; (e) Planktothrix isothrix; (f) Snowella lacustris; (g) Syn- echocystis aquatilis; (h) Aphanocapsa holsatica; ( i) Sphaerospermopsis aphanizomenoides; (j) Aphanizomenon klebahnii; (k) Geitlerinema acutissimum; (l) Pseudanabaena catenata; (m) Raphidiopsis mediterranea 358 Predojević et al. once a month from December 2012 to November the submerged vegetation. These samples were 2013 at two study sites, “Molo” (44º57’26.14” N fixed with Lugol’s solution immediately. and 19º31’37.58” E) and “Mostić” (44º56’59.26” N and 19º29’38.84” E). Qualitative analysis of algological material was performed using a Carl Zeiss AxioImager M1 The main physical parameters were measured microscope and digital camera AxioCam MRc5 using the following standard analytical methods with AxioVision 4.8 software. Taxonomic identi- and instruments: a multi digital thermometer for fications of Cyanobacteria were made according measuring the temperature, ECTestr 11+ multi to widely used taxonomic keys (Komárek, 2013; range for electrical conductivity and WTW multi Komárek and Anagnostidis, 1998, 2005). 3430 multiparameter meter for measuring pH value and dissolved oxygen. The transparency of Phytoplankton samples for quantitative anal- the river was measured by Secchi disc. ysis were collected using a Ruttner bottle (1 L volume), after which they were put in 1 L plas- The samples for qualitative phytoplankton tic bottles and fixed with Lugol’s solution. Phy- analysis were collected at these two study sites toplankton quantitative analysis was performed by towing a plankton net (pore diameter 22 µm) with a Leica inverted microscope using the Uter- through the open water. In the field, phytoplank- möhl method (Utermöhl, 1958). The results were ton samples were placed in a plastic bottle (0.1 L) expressed as the number of cells mL-1 and num- and preserved with Lugol’s solution. One more ber of individuals mL-1. sample that was taken for qualitative analysis was not preserved immediately, but after exploration All samples were analyzed and stored in the on the same day of sampling. The metaphyton Institute of Botany and Botanical Garden “Jevre- samples were collected by towing a plastic bottle movac” at the Faculty of Biology, University of (0.1 L) through the water near the bank, among Belgrade. Table 2. The list of all identified Cyanobacteria taxa from December 2012 to November 2013 in the phytoplankton and metaphyton of the Zasavica River. The new taxa for Serbia are marked with an asterisk. Cyanobacteria taxa Phytoplankton Metaphyton "Molo" "Mostić" "Molo" "Mostić" Chroococcales *Aphanocapsa conferta (W. et G.S. West) Komárkova-Legnerová et Cronberg + + Aphanocapsa holsatica (Lemmermann) Cronberg et Komárek + + *Aphanocapsa nubilum Komárek et Kling + Chrococcus minutus (Kützing) Nägeli + + *Chrococcus subnudus (Harsgirg) Cronberg et Komárek + Chrococcus turgidus (Kützing) Nägeli + + + *Cyanobiumplancticum (Drews) Komárek et al. + + Cyanothece Komárek sp. + Merismopedia glauca (Ehrenberg) Kützing + + *Merismopedia hyalina (Ehrenberg) Kützing + + CYanobacteria of the Zasavica River 359 Cyanobacteria taxa Phytoplankton Metaphyton