Three New Records for Diatoms from the Nišava River and Its Tributary, the Jerma River (Southern Serbia)| 19

Oceanological and Hydrobiological Studies International Journal of Oceanography and Hydrobiology

Volume 41, Issue 3

ISSN 1730-413X (17–23) eISSN 1897-3191 2012

DOI: 10.2478/s13545-012-0021-3 Received: August 31, 2011 Original research paper Accepted: December 12, 2011

INTRODUCTION Three new records for diatoms from the Nišava River and its tributary, the Jerma Diatoms are considered very useful indicators of environmental changes in aquatic ecosystems (Lowe River (Southern Serbia) & Pan 1996, Stevenson & Pan 1999). Species which are common, and which regularly occur in European freshwater habitats have well-known ecological * Jelena Z. Andrejić , Jelena Krizmanić, Mirko preferences (e.g. Van Dam et al. 1994, Kelly 1998, Cvijan Coste et al. 2009). On the other hand, species that are rarely found might have incomplete data about habitats they prefer, and new information on their Institute for Botany and Botanical Garden “Jevremovac” ecological requirements is valuable (e.g. Wojtal 2001, Faculty of Biology, University of Belgrade 2004), especially in the context of changing 11000 Belgrade, Serbia environmental conditions. Therefore, it is globally desirable that diatom species used as bioindicators are identified correctly, and their ecology described as Key words: diatom new records, distribution, well as possible. ecology, Nišava River Analysis of algal flora from the Nišava River was previously done by Branković et al. (2007) and Trajković et al. (2008), with 17 diatom species recorded. Recently, an endangered red alga Bangia Abstract atropurpurea (A. Roth) C. Agardh was found at the estuary of the Jerma River, a tributary of the Nišava The main objective of this paper is to report three benthic River (Andrejić et al. 2010). In the present study, we diatom species from the Nišava and Jerma Rivers, which prove sampled benthic diatoms to evaluate the floristic to be new findings in the context of the Serbian diatom flora. These are also new distributional records for all three species. richness of the river. Three species were found which Monthly samples (from stones, sediments and macrophytes) proved to be new to the Serbian diatom flora were collected from May 2008 to May 2009. Diatom frustules (Krizmanić 2009). The primary objectives of this were cleaned using chemical agents, and mounted on permanent paper are to report these species, give main valve slides. Descriptions (main valve measurement of the populations in the Nišava and Jerma Rivers), ecology, distribution in Serbia measurements of the populations, and briefly discuss and Europe, and appropriate photomicrographs of three species their ecology. are presented. Navicula novaesiberica Lange-Bertalot and Neidiomorpha binodiformis (Krammer) Lange-Bertalot & Cantonati STUDY AREA are rarely found in Europe, while Parlibellus protracta (Grunow) Witkowski is more common. Navicula novaesiberica and Neidiomorpha binodiformis were found at higher water temperatures The Nišava River is the biggest tributary of the in comparison to temperatures reported in the existing literature. South Morava River. It belongs to the Black Sea These new taxa significantly contribute to diatom floristic drainage basin and originates in the Stara Planina richness of the Nišava and Jerma Rivers in Serbia. Mountains (near the village of Toden) in Bulgaria. It is 218 km long with a catchment area of 4068 km2 * Corresponding author: [email protected]

18 | Jelena Z. Andrejić, Jelena Krizmanić, Mirko Cvijan

(the Serbian part is 151 km long, the catchment area and their ecology. Main valve measurements of the of 2971.5 km2). It enters Serbia 6 km from the town populations in the Nišava River are shown in Table of Dimitrovgrad, flows generally westward, until it 1, and chemical analyses of the water for each discharges into the Južna Morava River, about 10 km sampling site in Table 2. from the city of Niš. The major tributaries of the Nišava River are Temska, Visočica and Jerma Rivers Order: Naviculales (Gavrilović & Dukić 2002). There were 13 sampling Family: Naviculaceae sites along the river, and three species were found at Genus: Navicula four sampling sites: Navicula novaesiberica was found Species: Navicula novaesiberica Lange-Bertalot upstream of the town of Pirot (sampling site 1993 (Fig. 2A-C) ”Pirot”), Paribellus protracta at two sites upstream and downstream of Dimitrovgrad (sampling sites References: Lange-Bertalot 1993 (page 126, Fig. “Dimitrovgrad” and “Biolaguens”) and Neidiomorpha 61:1-8), Lange-Bertalot 2001 (page 89, Plate 37:1-7) binodiformis was found also upstream of Dimitrovgrad and at the confluence of Jerma and Nišava Rivers Description: Valves elliptic-lanceolate, ends obtusely (sampling site “Jerma”) (Fig. 1). rounded, length 30.5-37.7 µm, width 7.1-8.3 µm, raphe branches filiform, striae strongly radiate in the MATERIALS AND METHODS middle, abruptly parallel towards the ends and becoming convergent, 9-11 in 10 µm. Some valves Sampling was done every month from May 2008 have visible lineolae, approximately 28 in 10 µm. We to May 2009. Benthic diatoms were collected from found the species to be similar with Navicula stones and macrophytes by cleaning with a viridulacalcis Lange-Bertalot, also present in our toothbrush, and sediments were collected using a samples along with Navicula novaesiberica Lange- glass pipette. The algological material was preserved Bertalot, though lateral valve edges are more linear- in 4% formalin. Conductivity, pH and water lanceolate. temperature were measured with a Lovibond Multimeter WTW 340i at each sampling site. Ecology: According to Lange-Bertalot (2001), the Ammonium ions, nitrates, nitrites, phosphates, species seems to prefer β-mesosaprobic waters with silicates and total hardness were measured using a an average electrolyte content, and Szabo et al. (2007) Lovibond photometer PC Multidirect. Algological reported it in the Danube River with a conductivity samples were digested using the concentrated sulfuric range of 424-543 μS cm-1. Conductivities at the acid (H2SO4), potassium permanganate (KMnO4) and ”Pirot” sampling site were slightly elevated (622 μS oxalic acid (Krammer & Lange-Bertalot 1986), then cm-1) compared with conductance reported by Szabo rinsed repeatedly with deionized water until the pH et al. (2007), who also gave a narrow water was approximately 7, and mounted on slides with temperature range (1.7-4.6°C). Noga & Siry 2010 Naphrax® mounting medium. Microscopic gave a wider temperature range from 7 to 22°C, examination and counting of the valves was done which compares well with our data (19.1°C). Neutral using a Zeiss Axio-Imager M1 microscope. Images pH (6.64), slightly hard water (36), good silica were captured with AxioCam MR5, processed using availability (8), and low concentrations of other the software Axio-Imager version 4.8 and merged nutrients. using the Photoshop C2 imaging program. Valves were identified according to Krammer & Lange- Distribution (Serbia): N. novaesiberica was found in Bertalot 1986, Lange-Bertalot 1993, Lange-Bertalot August 2008 at the sampling site located upstream of 2001, Cantonati et al. 2010. The abundance was the town of Pirot (sampling site ”Pirot”, see Fig. 1) in estimated by counting 300 valves of each taxa relatively low abundance on stone (0.6%). present on one slide, and by counting the percentage of valves for the three species. Distribution (Europe): Relatively rare: the Danube River in Hungary (Szabó et al. 2007), Poland RESULTS AND DISCUSSION (Rakowska 1996, Szulc 2007, Noga & Siry 2010), France (Coste et al. 2009, Rimet 2009), and Germany The paper present the description and (Lange-Bertalot 2001). distribution of the three species in Serbia and Europe

Three new records for diatoms from the Nišava River and its tributary, the Jerma River (Southern Serbia)| 19

Fig. 1. Distribution of the sampling sites along the Nišava River. 1. “Dimitrovgrad” 2. “Biolagunes” 3. “Jerma” 4. “Pirot”.

Table 1

Main valve measurements of the populations from the Nišava River. Valve measurements Navicula novaesiberica Paribellus protracta Neidiomorpha binodiformis Length (μm) 30.5-37.7 28.9-37.8 32.7-53.6 Breadth (μm) 7.1-8.3 9.8-10.7 11.1-12.7 Striae number in 10 μm 9-11 14-16 11-13 Lineolae in 10 μm 28 - 4

Table 2

Chemical water parameters at the sampling sites. Navicula novaesiberica Paribellus protracta Neidiomorpha binodiformis Locality Pirot Dimitrovgrad Biolagunes Dimitrovgrad Dimitrovgrad Jerma (month/year) (8/08) (8/08) (8/08) (9/08) (10/08) (9/08) Water temperature (°C) 19.1 17.7 17.5 17.1 12.8 16 pH 6.64 6.69 8.51 6.37 6.49 7.51 Total hardness 36 24 18 19 11 14 Conductivity (μS cm-1) 622 527 948 503 505 396 Ammonium ion (mg l-1) 0.16 0.17 0.4 0.17 0.09 0.04 Nitrates (mg l-1) 1.0 >1 >1 >1 >1 >1 Nitrites (mg l-1) >0.01 >0.01 0.03 0.01 >0.01 0.02 Phosphates (mg l-1) 0.07 >0.04 0.25 0.06 0.09 0.07 Silicates (mg l-1) 8 6 9 6 5 6

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20 | Jelena Z. Andrejić, Jelena Krizmanić, Mirko Cvijan

Order: Naviculales References: Krammer & Lange-Bertalot 1986 (page Family: Naviculaceae 271, Fig. 100:6-8), Cantonati et al. 2010 (page 198, Genus: Parlibellus Figs 10-15) Species: Parlibellus protracta (Grunow) Witkowski, Lange-Bertalot & Metzeltin 2000 (Fig. 2D-F) Description: Valves with a central constriction and rounded ends, raphe filiform, the central area References: Krammer & Lange-Bertalot, 1986 (page elliptical, parallel longitudinal lines, length 32.7-53.6 163, Fig. 55:5-10), Witkowski et al. 2000 µm, width 11.1-12.7 µm, areolae visible with LM, app. 4 in 10 µm. Description: Valves linear-elliptical to elliptical, with protracted ends, length 28.9-37.8 µm, width 9.8-10.7 Ecology: According to Krammer & Lange-Bertalot µm, raphe filiform, the central area circular, striae 1986, the species prefers freshwaters with moderate moderately to slightly radial along the valve, in the conductivity levels. Cantonati et al. 2010 quote a middle more distant from each other, 14-16 in 10 conductivity range from 230 to 260 μS cm-1, while µm. Lineolae not visible in LM. our measured range was higher (396-505 μS cm-1). The previous report quotes a low to medium water Ecology: According to Krammer & Lange-Bertalot temperature range (6-9°C), in contrast to our (1986), the species prefers freshwaters with a high measured temperature range (12.8-17.1°C), with pH electrolyte content, which agrees with the elevated around neutral (6.37-7.51), total hardness soft to conductivity recorded at the “Biolagunes” site (948 slightly hard (11-19), good availability of silica (5-6) μS cm-1). These authors state that the species can as well as other nutrients. even be found in brackish waters, reported also by Van Dam et al. 1994 (′brackish-fresh waters′). Distribution (Serbia): Found in September and Nutrient concentrations at the “Dimitrovgrad” site October 2008 at the “Dimitrovgrad” sampling site, were undetectable (below the minimum levels), water and in September 2008 at the sampling site “Jerma”, temperature was around 17°C (17.5-17.7°C), pH which is located at the Jerma estuary (see Fig. 1), in varied from neutral to slightly alkaline (6.69-8.51), higher abundance on stone and sandy sediments water was slightly hard (18-24), and good silica (3.6%). availability (6-9). Distribution (Europe): Recorded in Romania Distribution (Serbia): P. protracta was found in (Cărăuş, 2003), Macedonia (Levkov et al. 2005), Italy August 2008 at two sampling sites, which were (Torrisi & Delluomo 2009) and Austria (Schönhuber located upstream and downstream of Dimitrovgrad 2007). (sampling sites “Dimitrovgrad” and “Biolagunes”, see Fig. 1), in moderate abundance in muddy The three benthic diatoms from the Nišava River, sediments (1.6%). reported in this paper, are new to the Serbian diatom flora. The current flora has 661 taxa reported (from Distribution (Europe): Found in Romania (Cărăuş, the subclass Bacillaripohycidae), collected from 2003), Macedonia (Levkov et al. 2005), Spain various aquatic ecosystems in Serbia (Krizmanić (Álvarez Cobelas & García 1982), Turkey (Ersanli & 2009). The previous study on biota from the Nišava Gönülol 2003), Czech Republic (Gross et al. 2002), River (Branković et al. 2007, Trajković et al. 2008) the Netherlands (Van Dam et al. 1994), Austria reported 17 diatom species. The number of samples (Schönhuber 2007), Poland (Zgrundo et al. 2009, studied in our study (326 samples in total), collected Żelazna-Wieczorek & Ziułkiewicz 2009), Albania monthly from diverse microhabitats, was probably (Miho et al. 2004, Miho & Witkowski 2005) and the factor contributing to the much larger number of France (Rimet 2009). taxa identified (194 diatom taxa). We plan to present the complete list of diatom taxa from the Nišava Order: Naviculales River and its two tributaries in future papers. Many Family: Naviculaceae aquatic ecosystems in Serbia are understudied, and Genus: Neidiomorpha until further detailed research on the diatom flora is Species: Neidiomorpha binodiformis (Krammer) carried out, we cannot state for certain that the Lange-Bertalot & Cantonati 2010 (Fig. 2 G-J) Nišava River is the only location at which these three

Three new records for diatoms from the Nišava River and its tributary, the Jerma River (Southern Serbia)| 21

species can be found. Paribellus protracta was found in samples from sandy sediments, Navicula novaesiberica was found only in samples scraped from stone, while Neidiomorpha binodiformis was found on both the sediment and stone. Neither of the species was found on samples from macrophytes. The availability of these microhabitats might play an important role in determining the spatial distribution of the species, though distinct niche preferences of diatoms in samples collected from rivers, may not be so obvious (Round 1991, Round 1998). In addition, chemical parameters downstream of the cities Pirot and Niš, as the major sources of pollution (Branković et al. 2009, Miljojković et al. 2010), showed a clear increase in nutrient concentration compared with samples upstream of those cities. This is probably the factor influencing the distribution of the species in the upper and middle reaches of the river, where the intensity of pollution is lesser. In the Nišava River, Navicula novaesiberica and Neidiomorpha binodiformis were found at higher water temperatures (see Table 2) as compared with the temperatures reported in the existing literature, which probably means that they can tolerate warmer water, and that other factors may play a role in their distribution and occurrence. Being an important water resource for southern Serbia, new information on biota, which may serve as potential bioindicators, is much needed (Savić et al. 2010, Jovanović et al. 2011). Evaluation of the floristic richness of diatoms in the river is a necessary, further step. These new and rare taxa significantly contribute to diatom biodiversity of the Nišava River and Serbia, though the importance of rare diatom taxa in bioassessment studies is still unclear (Potapova & Charles 2004, Gillett et al. 2011). This new information increases our knowledge of the river system and the relationship between diatom species and chemical parameters, which is important for further predictions of the water quality based on the occurrence of diatoms as bioindicators, and monitoring programs.

ACKNOWLEDGMENTS

We thank M. Sc. Saša Branković of the Institute Figs 2. LM micrographs of the diatom species. (A-C) for Nature Conservation of Serbia, as well as friends Navicula novaesiberica Lange-Bertalot; (D-F) and editors for their kind and useful comments. Parlibellus protracta (Grunow) Witkowski, Lange- Bertalot & Metzeltin; (G-J) Neidiomorpha binodiformis (Krammer) Lange-Bertalot & Cantonati.

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22 | Jelena Z. Andrejić, Jelena Krizmanić, Mirko Cvijan

REFERENCES Lowe R.L., Pan Y., 1996, Benthic algae communities as biological monitors. In: Stevenson R.J., Bothwell M.L. & Lowe R.L., Álvarez Cobelas M. & Estévez García A., 1982, Catálogo de las (eds), Algal Ecology. Freshwater benthic ecosystems. algas continentales españolas. I. Diatomophyceae Rabenhorst 1864. Academic Press, pp. 753 Lazaroa, 4: 269-85. Miho A., Tase D., Lange-Bertalot H., 2004, Overview on diatoms Andrejić J.Z., Cvijan M., Simić S., 2010, New record of endangered red from Ohrid Lake. BALWOIS 2004, Ohrid, Republic of alga Bangia atropurpurea (A. Roth) C. Agardh (Bangiales, Macedonia. pp. 1-9 Rhodophyta) in the Nišava River, Serbia. Arch. Biol. Sci., Miho A., Witkowski A., 2005, Diatom (Bacillariophyta) flora of Belgrade, 62 (4): 1239-43 Albanian coastal wetlands taxonomy and ecology: A review, Proc. Branković S., Simić V. Trajković S., 2007, Hydrobiological Calif. Acad. Sci. 56(12): 129-45 investigation of the Nišava River according to Water Framework Miljojković D., Milenković S., Miljojković, I., 2010, Influence of Directive. Zbornik radova Građevinsko-arhitektonskog Pirot′s waste water on water quality of River Nišav,. BALWOIS fakulteta, Niš. No. 22: 143-48. (In Serbian) 2010, Ohrid, Republic of Macedonia, pp. 1-7 Branković S., Trajković S., Gocić M., 2009, Water quality analysis of Noga T., Siry T., 2010, Diversity of diatom flora in the Łubienka stream the Nišava River downstram of Sićevo gorge. Zbornik radova (the Dynów foothills, south-eastern Poland), Polish Society of Građevinsko-arhitektonskog fakulteta, Niš. No. 24: 179-86. Ecological Engineering, Issue 12, pp. 75-86 (in Polish) (In Serbian) Potapova M., Charles D.F., 2004, Potential use of rare diatoms as Cantonati M., Lange-Bertalot H., Angeli, N., 2010, Neidiomorpha environmental indicators in USA rivers. In: Poulin M. (ed.), gen. nov. (Bacillariophyta): A new freshwater diatom genus separated Proceeding of the 17th Diatom Syposium. Biopress Ltd., from Neidium Pfitzer. Botanical Studies 51: 195-202. Bristol, UK, pp. 95-281. Cărăuş I., 2003, Algae of Romania. A distributional checklist of actual Rakowska B., 1996, The benthic diatom community of a reservoir after the algae. Studii şi Cercetări (Biologie) 7, 1-694. Universitatea exploration of brown coal in Konin (Central Poland), Algol. Stud., Bacău. 82: 103-116 Coste M., Boutry S., Tison-Rosbery J., Delmas F., 2009, Rimet F., 2009, Benthic diatom assemblages and their correspondence with Improvements of the Biological Diatom Index (BDI): Description and ecoregional classification: case study of rivers in north-eastern France. efficiency of the new version (BDI-2006). Ecol. Indic., 9(4): 621- Hydrobiologia 636: 137-151 50. Round F.E., 1991, Diatoms in river water-monitoring studies. Journal Ersanli, E. & Gönülol, A. (2003). Study on the phytoplankton of Applied Phycology. Vol. 3 (2): 129-146. and seasonal variation of Lake Simenit (Terme – Samsun, Round F.E., 1998, A problem in algal ecology & contamination of Turkey), Turkish Journal of Fisheries and Sciences 3: 29-39. habitats from adjacent communities. Cryptogamie Algol. 19 (1-2): Gavrilović L., Dukić D., 2002, Reke Srbije. Radunić, Beograd. 218 49-55. p. Savić A., Ranđelović V., Krpo-Ćetković J., 2010, Seasonal Gillett N.D., Pan Y., Manoylov K.M., Stancheva R., Weilhoefer variability in community structure and habitat selction of mayflies C.L., 2011, The potential indicator value of rare taxa richness in (Ephemeroptera) in the Nišava River (Serbia), Biotechnol. diatom-based stream bioassessment. J. Phcol. 47: 471-482. Biotechnol. Equip., special edition, Plovdiv. Vol. 24(2): 639- Gross W., Oesterhelt C., Tischendorf G., Lederer F., 2002, 645. Characterization of a non-thermophilic strain of the red algal genus Schönhuber M., 2007, Kieselalgengemeinschaften von ausgewählten Galdieria isolated from Soos (Czech Republic), Eur. J. Phycol., 37: Kärntner Seen. Kärtner Institut Für Seenforschung, pp. 1-18 477-482. Stevenson R.J., Pan Y., 1999, Assessing environmental conditions in Jovanović B., Mihaljev Ž., Maletin S., Palić, D., 2011, Assessment rivers and streams with diatoms. In: Stoermer E.F. & Smol J.P. of heavy metal load in chub liver (Cyprinidae-Leucisus cephalus) from (eds.), 1999, The Diatoms. Application for the environmental the Nišava River (Serbia). Biologica Nyssana, 2(1): 1-7. and earth sciences. Cambridge University Press, pp. 469 Kelly M.G.,1998, Use of the trophic diatom index to monitor Szabó K.E., Kiss K.T., Tóth B., Metzeltin D., Ács É., 2007, eutrophication in rivers, Water Res. 32, 236-42. Navicula novaesiberica Lange- Bertalot; a new record of the species from Krammer K., Lange-Bertalot, H., 1986, Bacillariophyceae. 1. Teil: the Danube River in Hungary. Diatom Research 22 (2): 497-502. Naviculaceae. in Ettl, H., Gerloff, J., Heynig, H. & Mollenhauer, D. Szulc B., 2007, Benthic diatoms of the Pilica River 50 years ago and (eds) Süsswasser flora von Mitteleuropa, Band 2/1. Gustav Fischer today. Oceanol. Hydrobiol. St. 39(1): 221-226. Verlag: Stuttgart, New York. 876 pp. Torrisi M., Dell′uomo A., 2009, Diatomee bentoniche del corso superior Krizmanić J., 2009, Floristic, taxonomical and ecological investigations of di alcuni fiumi centro-appenninici. Studi Trent. Sci. Nat., 84: 139- siliceous algae (Bacillariophyceae, Bacillariophycideae, Bacillariophyta) 151. in Serbia, PhD thesis, University of Belgrade, Faculty of Trajković S., Branković, S., Gocić, M., 2008, Analysis of biological Biology, Serbia, pp. 545 (in Serbian with English summary) water quality parameters of the River Nišava upstream of water Lange-Bertalot H., 1993, 85 Neue Taxa und über 100 weitere neu treatment plant “Mediana”, BALWOIS 2008, Ohrid, Republic definierte Taxa ergänzend zur Süsswasserflora von Mitteleuropa vol. of Macedonia, pp. 1-5 2/1-4, Bibliotheca Diatomologica 27: 164 pp. Van Dam H., Mertens A., Sinkeldam J.. 1994, A coded checklist and Lange-Bertalot H., 2001, Navicula sensu stricto. 10 Genera separated ecological indicator values of freshwater diatoms from the Netherlands, from Navicula sensu lato. Frustulia. In: Diatoms of Europe. Aquat. Ecol., Vol. 28 (1): 117-133. Diatoms of the European Inland Waters and Comparable Witkowski A., Lange-Bertalot H., Metzeltin D., 2000, Diatom Habitats (H. Lange-Bertalot, ed.), 1-526. A.R.G. Ganter Flora of Marine Coasts I. In: Lange-Bertalot H. (ed.), Verlag K.G. Ruggell. Iconographia Diatomologica, Annotated Diatom Levkov Z., Krstic S., Nakov T., Melovski Lj., 2005, Diatom Micrographs, Vol. 7. Diversity-Taxonomy-Identification. assemblages on Shara and Nidze Mountains, Macedonia, Nova Koeltz Scientific Books, Königstein, Germany, pp. 925 Hedwigia 81(3-4): 501-537. Wojtal A, 2001, New or rare species of the genus Navicula (Bacillaripohyceae) in the diatom flora of Poland, Polish Bot. J.

Three new records for diatoms from the Nišava River and its tributary, the Jerma River (Southern Serbia)| 23

46(2): 161-167 Wojtal A., 2004, New or rare species of the genera Achnanthidium and Psammonthidium (Bacillaripohyceae) in the diatom flora of Poland, Polish Bot. J. 49(2): 215-220 Żelazna-Wieczorek J., Ziułkiewicz M., 2009, Using benthic diatoms in the assessment of spring water quality in suburban areas, Oceanol. Hydrobiol. St. 38: 121-131 Zgrundo A., Dziengo-Czaja M., Bubak I., Bogaczewicz- Adamczak B., 2009, Studies on the biodiversity of contemporary diatom assemblages in the Gulf of Gdańsk, Oceanol. Hydrobiol. St. (37): 139-153.