Skip to main content
SpringerLink
Log in

Morphological and ecological characteristics of potentially toxic invasive cyanobacterium Sphaerospermopsis aphanizomenoides (Forti) Zapomelová, Jezberová, Hrouzek, Hisem, Reháková & Komárková (Nostocales, Cyanobacteria) in Serbia

Brazilian Journal of Botany volume 39, pages 225–237 (2016)Cite this article

Abstract

This study investigates the morphology and occurrence of the potentially toxic invasive cyanobacterium recently detected in Serbia, Sphaerospermopsis aphanizomenoides (Forti) (Zapomelová et al. 2010), in correlation with several environmental parameters. The presence of this species was recorded during warm months in three of four studied sites in the Ponjavica River. It was found in a community with invasive Cylindrospermopsis raciborskii (Woloszynska) (Seenayya and Subba Raju 1972) and Raphidiopsis mediterranea (Skuja 1937) in this small, shallow, eutrophic river, with slow water flow. The peak of its abundance was observed in August 2008 (3.36 × 106 cell/ml). The proliferation of this cyanobacterium was caused by very high water temperatures at the beginning of the summer, which resulted in an increase in the biomass of this species in August. The blooms of S. aphanizomenoides often occur under nitrogen depletion due to the formation of heterocysts, but in our study, their number was in positive correlation with the concentration of total dissolved nitrogen at the end of the study period. However, PCA analysis, which included the whole study period, indicated that there is a negative correlation between these two parameters. According to this analysis, in this locality, the factors which control the formation of the akinetes of S. aphanizomenoides are both the concentration of phosphate in the water and temperature. The morphological characteristics (trichome length, dimensions of the vegetative cells, heterocysts and akinetes, and their position) of this species, first recorded in Serbia, were mainly in correlation with those from the Czech Republic. However, individuals of S. aphanizomenoides from Serbia have shown a greater range of morphological variability than previously recorded.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Figs. 1–4
Figs. 5–8
Figs. 9–12
Fig. 13–19
Fig. 20
Fig. 21
Fig. 22

Similar content being viewed by others

References

  • Adams DG, Duggan PS (1999) Tansley Review No. 107, Heterocyst and akinete differentiation in cyanobacteria. New Phytol 144:3–33

    Article  Google Scholar 

  • Argueta C, Summers M (2005) Characterization of a model system of the study of Nostoc punctiforme akinetes. Arch Microbiol 183:338–346

    Article  CAS  PubMed  Google Scholar 

  • Bauersachs T, Stal L, Grego M, Schwark L (2014) Temperature induced changes in the heterocyst glycolipid composition of N2 fixing heterocystous cyanobacteria. Org Geochem 69:98–105

    Article  CAS  Google Scholar 

  • Bittencourt-Oliveira M, Piccin-Santos V, Kujbida P, do Nascimento Moura A (2011) Cylindrospermopsin in water supply reservoirs in brazil determined by immunochemical and molecular methods. J Water Resour Prot 3:349–355

    Article  CAS  Google Scholar 

  • Bostock PD, Holland AE (2010) Census of the Queensland Flora. Queensland Herbarium Biodiversity and Ecosystem Sciences, Department of Environment and Resource, Brisbane Management

  • Brient L, Lengronne M, Bormans M, Fastner J (2008) First occurrence of Cylindrospermopsin in freshwater in France. Environ Toxicol 24:415–420

    Article  Google Scholar 

  • Broady PA, Merican F (2012) Phylum Cyanobacteria: blue-green bacteria, blue-green algae. In: Gordon DP (ed) New Zealand inventory of biodiversity, vol 3. Kingdoms Bacteria, Protozoa, Chromista, Plantae, Fungi. Canterbury University Press, Christchurch, pp 50–69

  • Caraus I (2002) The algae of Romania. Studii si Cercetari. Universitatea Bacau, Bacau

    Google Scholar 

  • Comas González A (2008) Algunas características de la Flora de algas y cianoprocariotas de agua dulce de Cuba. ALGAS. Bol de la Soc Esp de Ficología 39:21–29

    Google Scholar 

  • Day SA, Wickham RP, Entwisle TJ, Tyler PA (1995) Bibliographic check-list of non-marine algae in Australia. Flora Aust Suppl Ser 4:1–276

    Google Scholar 

  • Devercelli M (2006) Phytoplankton of the middle Paraná River during an anomalous hydrological period: a morphological and functional approach. Hydrobiologia 563:465–478

    Article  Google Scholar 

  • Dokulil MT, Teubner K (2000) Cyanobacterial dominance in lakes. Hydrobiologia 438:1–12

    Article  CAS  Google Scholar 

  • EN 15204:2006—Water quality—guidance standard on the enumeration of phytoplankton using inverted microscopy (Utermöhl Technique). European Committee for Standardization, Brussels

  • Ersanli E, Gönülol A (2006) A study on the phytoplankton of Lake Simenit, Turkey. Cryptogam Algol 27:289–305

    Google Scholar 

  • Figueiredo DR, Antunes SC, Pereira MJ, Goncalves F (2004) Chronic effects of Aphanizomenon flos-aquae on the survival and reproduction of daphnids. Fresenius Environ Bull 13:665–670

    Google Scholar 

  • Figueiredo DR, Alves A, Pereira MJ, Correia A (2010) Molecular characterization of bloom-forming Aphanizomenon strains isolated from Vela Lake (Western Central Portugal). J Plankton Res 32:239–252

    Article  Google Scholar 

  • Figueiredo DR, Gonçalves AMM, Castro BB, Gonçalves F, Pereira MJ, Correia A (2011) Differential inter- and intra-specific responses of Aphanizomenon strains to nutrient limitation and algal growth inhibition. J Plankton Res 33:1606–1616

    Article  Google Scholar 

  • Fogg GE, Stewart WDP, Fay P, Walsby AE (1973) The Blue-Green algae. Academic Press, London

    Google Scholar 

  • Geitler L (1932) Cyanophyceae, Rabenhorst’s Kryptogamen—Flora von Deutschland, Österreich und der Schweiz, 2nd edn. Koeltz Scientific Books, Koenigstein

  • Gugger M, Lyra C, Henriksen P, Couté A, Humbert J-F, Sivonen K (2002) Phylogenetic comparison of the cyanobacterial genera Anabaena and Aphanizomeon. Int J Syst Evol Microbiol 52:1867–1880

    CAS  PubMed  Google Scholar 

  • Haselkorn R (2010) A new player in the regulatory cascade controlling heterocyst differentiation in cyanobacteria. Mol Microbiol 77:537–539

    Article  CAS  PubMed  Google Scholar 

  • Hašler P, Štěpánková J, Špačková J, Neustupa J, Kitner M, Hekera P, Veselá J, Burian J, Poulíčková A (2008) Epipelic cyanobacteria and algae: a case study from Czech ponds. Fottea 8:133–146

    Google Scholar 

  • Hillebrand H, Durselen CDD, Kirschtel U, Pollingher T, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424

    Article  Google Scholar 

  • Hindák F (2000) Morphological variation of four planktic nostocalean cyanophytes—members of the genus Aphanizomenon or Anabaena? Hydrobiologia 438:107–116

    Article  Google Scholar 

  • Hoffmann L (1996) Geographic distribution of freshwater blue-green algae. Hydrobiologia 336:33–40

    Article  Google Scholar 

  • Horecká M, Komárek J (1979) Taxonomic position of three planktonic blue-green algae from the genera Aphanizomenon and Cylindrospermopsis. Preslia 51:289–312

    Google Scholar 

  • Ishihara J, Tachikawa M, Iwasaki H, Mochizuki A (2015) Mathematical study of pattern formation accompanied by heterocyst differentiation in multicellular cyanobacterium. J Theor Biol 371:9–23

    Article  PubMed  Google Scholar 

  • John MD, Whitton AB, Brook JA (2002) The freshwater algal flora of the British Isles: an identification guide to freshwater and terrestrial algae. The Natural History Museum, Cambridge

    Google Scholar 

  • Karadžić V, Subakov Simić G, Natić D, Ržaničanin A, Ćirić M, Gačić Z (2013) Changes in the phytoplankton community and dominance of Cylindrospermopsis raciborskii (Wolosz.) Subba Raju in a temperate lowland river (Ponjavica, Serbia). Hydrobiologia 711:43–60

    Article  Google Scholar 

  • Kaštovský J, Hauer T, Mareš J, Krautová M, Bešta T, Komárek J, Desortová B, Heteša J, Hindáková A, Houk V, Janeček E, Kopp R, Marvan P, Pumann P, Skácelová O, Zapomĕlová E (2010) A review of the alien and expansive species of freshwater cyanobacteria and algae in the Czech Republic. Biol Invasions 12:3599–3625

    Article  Google Scholar 

  • Kearns K, Hunter M (2001) Toxin-producing Anabaena flos-aquae induces settling of Chlamydomonas reinhardtii, a competing motile alga. Microbiolial Ecol 42:80–86

    CAS  Google Scholar 

  • Kling JH (2009) Cylindrospermopsis raciborskii (Nostocales, Cyanobacteria): a brief historic overview and recent discovery in the Assiniboine River (Canada). Fottea 9:45–47

    Article  Google Scholar 

  • Kokciński M, Soininen J (2012) Environmental factors related to the occurrence of Cylindrospermopsis raciborskii (Nostocales, Cyanophyta) at the north-eastern limit of its geographical range. Eur J Phycol 47:12–21

    Article  Google Scholar 

  • Komárek J (1994) Current trends and species delimitation in cyanoprokaryote taxonomy. Algol Stud 75:11–29

    Google Scholar 

  • Komárek J (2013) Cyanoprokaryota 3. Teil: Heterocytous genera. In: Büdel B, Gärtner G, Krienitz L, Schagerl M (eds) Süβwasserflora von Mitteleuropa. Springer Spectrum Verlag, Heidelberg

    Google Scholar 

  • Komárek J, Mareš J (2012) An update to modern taxonomy (2011) of freshwater planktonic heterocystous cyanobacteria. Hydrobiologia 698:327–351

    Article  Google Scholar 

  • Koreiviené J, Kasperovičiené J (2011) Alien cyanobacteria Anabaena bergii var. limnetica Couté et Preisig from Lithuania: some aspects of taxonomy, ecology and distribution. Limnologica 41:325–333

    Article  Google Scholar 

  • Leão PN, Vasconcelos MT, Vasconcelos VM (2009) Allelopathy in freshwater cyanobacteria. Crit Rev Microbiol 35:271–282

    Article  PubMed  Google Scholar 

  • Ledreuxa A, Thomazeaua S, Catherinea A, Duvala C, Yéprémiana C, Marieb A, Bernarda C (2010) Evidence for saxitoxins production by the cyanobacterium Aphanizomenon gracile in a French recreational water body. Harmful Algae 10:88–97

    Article  Google Scholar 

  • Lee E, Ryan UM, Monis P, McGregor GB, Bath A, Gordon C, Paparini A (2014) Polyphasic identification of cyanobacterial isolates from Australia. Water Res 59:248–261

    Article  CAS  PubMed  Google Scholar 

  • Li R, Watanabe M, Watanabe MM (1997) Akinete formation in planktonic Anabaena spp. (cyanobacteria) by treatment with low temperature. J Phycol 33:576–584

    Article  Google Scholar 

  • Mehnert G, Leunert F, Cirés S, Jöhnk KD, Rücker J, Nixdorf B, Wiender C (2010) Competitiveness of invasive and native cyanobacteria from temperate freshwaters under various light and temperature conditions. J Plankton Res 32:1009–1021

    Article  CAS  Google Scholar 

  • Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O (2013) State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int 59:303–327

    Article  CAS  PubMed  Google Scholar 

  • Moore D, O’Donohue M, Shaw G, Critchley C (2003) Potential triggers for akinete differentiation in an Australian strain of the cyanobacterium Cylindrospermopsis raciborskii (AWT 205/1). Hydrobiologia 506–509:175–180

    Article  Google Scholar 

  • Nichols JM, Adams DG (1982) Akinetes. In: Carr NG, Whitton BA (eds) The biology of cyanobacteria. Blackwell Scientific, Oxford, pp 387–412

    Google Scholar 

  • Obušković Lj (1991) Phytoplankton and saprobiological characteristic as indication of accelerated eutrophication of the river Ponjavica (South Banat). Conference ‘‘Water protection ‘91’’, The Book of referates, pp 333–337

  • Ogawa RE, Carr JF (1969) The influence of nitrogen on heterocyst production in blue-green algae. Limnol Oceanogr 14:342–351

    Article  CAS  Google Scholar 

  • Otsuka S, Suda S, Shibata S, Oyaizu H, Matsumoto S, Watanabe MM (2001) A proposal for the unification of five species of the cyanobacterial genus Microcystis Kützing ex Lemmermann 1907 under the rules of the Bacteriological Code. Int J Syst Evol Microbiol 51:873–879

    Article  CAS  PubMed  Google Scholar 

  • Padisák J (2004) Phytoplankton. In: O’Sullivan PE, Reynolds CS (eds) The lakes handbook, vol 1: limnology and limnetic ecology. Blackwell Science Ltd, Oxford

    Google Scholar 

  • Padisák J, Crossetti LO, Naselli-Flores L (2009) Use and misuse in the application of the phytoplankton functional classification: a critical review with updates. Hydrobiologia 621:1–19

    Article  Google Scholar 

  • Papadimitrioua T, Katsiapic M, Kormasa KA, Moustaka-Gounic M, Kagaloua I (2013) Artificially-born “killer” lake: phytoplankton based water quality and microcystin affected fish in a reconstructed lake. Sci Total Environ 452–453:116–124

    Article  Google Scholar 

  • Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annu Rev Ecol Evol Syst 37:637–669

    Article  Google Scholar 

  • Pham MN, Tan HTW, Mitrovic S, Yeo HHT (2011) A checklist of the algae of Singapore. Raffles Museum of Biodiversity Research, National University of Singapore, Singapore

    Google Scholar 

  • Reynolds CS, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428

    Article  Google Scholar 

  • Sabour B, Loudiki M, Oudra B, Vasconcelos V, Oubraim S, Fawzi B (2005) Dynamics and toxicity of Anabaena aphanizomenoides (Cyanobacteria) waterblooms in the shallow brackish Oued Mellah lake (Morocco). Aquat Ecosyst Health Manage 8:95–104

    Article  CAS  Google Scholar 

  • Seenayya G, Subba Raju N (1972) On the ecology and systematic of the alga known as Anabaenopsis raciborskii (Wolosz.) Elenk. and a critical evaluation of the forms described under the genus Anabaenopsis. In: Desikachary TV (ed) Papers submitted to the first international symposium on taxonomy and biology of blue-green algae. University of Madras, Madras, pp 52–57

    Google Scholar 

  • Skuja H (1937) Süsswasseralgen aus Griechenland und Kleinasien. Hedwigia 77:15–70

    Google Scholar 

  • Stefaniak K, Kokciński M (2005) Occurrence of invasive Cyanobacteria species in polimictic lakes of the Wielkopolska region (Western Poland). Oceanol Hydrobiol Stud 36:137–148

    Google Scholar 

  • Stüken A, Rücker J, Endrulat T, Preußel K, Hemm M, Nixdorf B, Karsten U, Wiedner C (2006) Distribution of three alien cyanobacterial species (Nostocales) in Northeast Germany: cylindrospermopsis raciborskii, Anabaena bergii and Aphanizomenon aphanizomenoides. Phycologia 45:696–703

    Article  Google Scholar 

  • Stüken A, Campbel R, Quesada A, Sukenik A, Dadheech P, Wiedner C (2009) Genetic and morphologic characterization of four putative cylindrospermopsin producing species of the cyanobacterial genera Anabaena and Aphanizomenon. J Plankton Res 31:465–480

    Article  Google Scholar 

  • Sun J, Liu D (2003) Geometric models for calculating cell biovolume and surface area for phytoplankton. J Plankton Res 25:1331–1346

    Article  Google Scholar 

  • Täuscher L (2011) Checklisten und Gefährdungsgrade der Algen des Landes Brandenburg I. Einleitender Überblick, Checklisten und Gefährdungsgrade der Cyanobacteria/Cyanophyta, Rhodophyta und Phaeophyceae/Fucophyceae. Verhandlungen des Botanischen Vereins von Berlin und Brandenburg 144:177–192

    Google Scholar 

  • Ter Braak CJF, Šmilauer P (2012) Canoco reference manual and user’s guide: software for ordination, version 5.0. Microcomputer Power, Ithaca

    Google Scholar 

  • Vardaka E, Moustaka-Gouni M, Cook MC, Lanaras Z (2005) Cyanobacterial blooms and water quality in Greek waterbodies. J Appl Phycol 17:391–401

    Article  Google Scholar 

  • Varol M, Sen B (2014) Dicle Nehrinin Planktonik Alg Floras [Flora of the Planktonic Algae of the Tigris River]. J Fish Sci 8:1–14

    Google Scholar 

  • Vinogradova OM, Wasser SP, Nevo E (2000) Cyanoprocaryota. In: Nevo E, Wasser SP (eds) Biodiversity of cyanoprocaryotes algae and fungi of Israel Cyanoprocaryotes and algae of continental Israel. A.R.A Gantner Verlag K.-G., Ruggell, pp 32–141

  • Whitton BA, John DM, Johnson LR, Boulton PNG, Kelly MG, Haworth EY (1998) A coded list of freshwater algae of the British Isles. Institute of Hydrology & NERC, Wallingford

    Google Scholar 

  • Wu Z, Shi J, Lin S, Li R (2010) Unraveling molecular diversity and phylogeny of Aphanizomenon (Nostocales, Cyanobacteria) strains isolated from China. J Phycol 46:1048–1058

    Article  CAS  Google Scholar 

  • Yamamoto Y, Nakahara H (2009) Seasonal variations in the morphology of bloom-forming cyanobacteria in a eutrophic pond. Limnology 10:185–193

    Article  Google Scholar 

  • Zagajewski P, Gołdyn R, Fabiś M (2009) Cyanobacterial volume and microcystin concentration in recreational lakes (Poznań—Western Poland). Int J Oceanogr Hydrobiol 38:113–120

    Google Scholar 

  • Zapomĕlová E, Jezberová J, Hrouzek P, Hisem D, Řeháková K, Komárková J (2009) Polyphasic characterization of three strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (Cyanobacteria) and their reclassification to Sphaerospermum gen. nov. (Incl. Anabaena kisseleviana). J Phycol 45:1363–1373

    Article  PubMed  Google Scholar 

  • Zapomelová E, Jezberová J, Hrouzek P, Hisem D, Reháková K, Komárková J (2010) Nomenclatural note: polyphasic characterization of three strains of Anabaena reniformis and Aphanizomenon aphanizomenoides (cyanobacteria) and their reclassification to Sphaerospermum gen. nov. (incl. Anabaena kisseleviana) (45:1363–73). J Phycol 46:415

    Article  Google Scholar 

  • Zapomelová E, Hrouzek P, Rezanka T, Jezberová J, Řeháková K, Hisem D, Komárková J (2011) Polyphasic characterization of Dolichospermum spp. and Sphaerospermopsis spp. (Nostocales, Cyanobacteria): morphology, 16S rRNA gene sequences and fatty acid and secondary metabolites profiles. J Phycol 47:1152–1163

    Article  PubMed  Google Scholar 

  • Zapomĕlová E, Skácelová O, Pumann P, Kopp R, Janacěk E (2012) Biogeographically interesting planktonic Nostocales (Cyanobacteria) in the Czech Republic and their polyphasic evaluation resulting in taxonomic revisions of Anabaena bergii Ostenfeld 1908 (Chrysosporum gen. nov.) and A. tenericaulis Nygaard 1949 (Dolichospermum tenericaule comb. nova). Hydrobiologia 698:353–365

    Article  Google Scholar 

  • Zhang CC, Laurent S, Sakr S, Peng L, Bédu S (2006) Heterocyst differentiation and pattern formation in cyanobacteria: a chorus of signals. Mol Microbiol 59:367–375

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This research was supported by the Ministry of Science and Technological Development, Republic of Serbia, Project No. ON 176020. We express our thanks to Grainne Boyle Orlic and Ana Anđelković for language correction. We are also grateful to anonymous reviewers for their comments on an earlier version of the manuscript.

Author information

Authors and Affiliations

  1. Faculty of Biology, University of Belgrade, Institute of Botany and Botanical Garden “Jevremovac”, Takovska 43, Belgrade, 11000, Serbia

    Jelena Jovanović

  2. Institute of Public Health of Serbia “Dr Milan Jovanović Batut”, Dr Subotića 5, Belgrade, 11000, Serbia

    Vesna Karadžić

  3. Faculty of Biology, University of Belgrade, Studentski trg 16, Belgrade, 11000, Serbia

    Dragana Predojević, Ana Blagojević, Slađana Popović, Ivana Trbojević & Gordana Subakov Simić

Authors
  1. Jelena Jovanović
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Vesna Karadžić
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Dragana Predojević
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Ana Blagojević
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Slađana Popović
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ivana Trbojević
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Gordana Subakov Simić
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Vesna Karadžić.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jovanović, J., Karadžić, V., Predojević, D. et al. Morphological and ecological characteristics of potentially toxic invasive cyanobacterium Sphaerospermopsis aphanizomenoides (Forti) Zapomelová, Jezberová, Hrouzek, Hisem, Reháková & Komárková (Nostocales, Cyanobacteria) in Serbia. Braz. J. Bot 39, 225–237 (2016). https://doi.org/10.1007/s40415-015-0223-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s40415-015-0223-1

Keywords

search

Navigation