Freshwater cyanobacteria in waters intended for human consumption in Serbia: two decades of changes in diversity

Jelena Jovanović; Slađana  Popović; Gordana  Subakov Simić; Verica  Jovanović; Dragana  Predojević; Dragana  Jovanović; Vesna  Karadžić

doi:10.2298/ABS220518020J

Authors

Jelena Jovanović Institute of Public Health of Serbia ‘Doktor Milan Jovanović Batut’, Doktora Subotića 5, 11000 Belgrade, Serbia https://orcid.org/0000-0002-8114-3630
Slađana Popović University of Belgrade, Faculty of Biology, Institute of Botany and Botanical Garden ‘Jevremovac’, Department of Algology, Mycology and Lichenology, Studentski trg 16, 11000 Belgrade, Serbia https://orcid.org/0000-0001-7112-5853
Gordana Subakov Simić University of Belgrade, Faculty of Biology, Institute of Botany and Botanical Garden ‘Jevremovac’, Department of Algology, Mycology and Lichenology, Studentski trg 16, 11000 Belgrade, Serbia https://orcid.org/0000-0002-0500-7354
Verica Jovanović Institute of Public Health of Serbia ‘Doktor Milan Jovanović Batut’, Doktora Subotića 5, 11000 Belgrade, Serbia https://orcid.org/0000-0002-9650-0709
Dragana Predojević University of Belgrade, Faculty of Biology, Institute of Botany and Botanical Garden ‘Jevremovac’, Department of Algology, Mycology and Lichenology, Studentski trg 16, 11000 Belgrade, Serbia https://orcid.org/0000-0003-4939-6969
Dragana Jovanović Institute of Public Health of Serbia ‘Doktor Milan Jovanović Batut’, Doktora Subotića 5, 11000 Belgrade, Serbia
Vesna Karadžić Institute of Public Health of Serbia ‘Doktor Milan Jovanović Batut’, Doktora Subotića 5, 11000 Belgrade, Serbia

DOI:

https://doi.org/10.2298/ABS220518020J

Keywords:

cyanobacteria, diversity, distribution, potentially toxic, alien/invasive

Abstract

Paper description:

Cyanobacteria are an important component of aquatic ecosystems that are impacted by global environmental changes.
Changes in cyanobacterial diversity in waters intended for human consumption were assessed for two decades. The research included sample analysis from different localities and a literature search.
Great changes occurred during the investigated period, including an increased (doubled) number of identified taxa, increased frequency of potentially toxic and bloom-forming species, and expansion of alien species, especially Raphidiopsis raciborskii and Sphaerospermopsis aphanizomenoides.
The latter points to an urgent need for a more detailed investigation.

Abstract: Herein we provide an assessment of cyanobacterial diversity and habitat preferences of potentially toxic and alien taxa, which could be an important tool for human health risk assessment regarding recreational and water-supply waterbodies. The diversity changes of cyanobacteria in waters intended for human consumption in Serbia were analyzed two decades after the first floristic study was published. The examination included phytoplankton and phytobenthic sample analysis from 35 localities in the period between 2012 and 2017, together with published literature records. The results indicate that the number of identified taxa doubled since the first Serbian Flora of Cyanobacteria was released two decades ago. The changes most likely occurred due to environmental factors, including hydrological transformations of habitats, cultural eutrophication and global warming. Many frequently recorded taxa are potentially toxic and bloom-forming. The spread of alien species with potentially invasive characteristics has also been noted. Canonical correspondence analysis (CCA) indicates that shallow waterbodies are the most vulnerable regarding the occurrence and expansion of bloom-forming, potentially toxic and invasive taxa. This shows the urgent need for a more detailed investigation. Additionally, although most of the research was focused on planktonic forms, benthic cyanobacteria represent an important component for public health risk assessment and therefore should be more frequently investigated.

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References

Merel S, Walker D, Chicana R, Snyder S, Baurès E, Thomas O. State of knowledge and concerns on cyanobacterial blooms and cyanotoxins. Environ Int. 2013;59:303-27.

https://doi.org/10.1016/j.envint.2013.06.013

Paerl HW, Paul VJ. Climate change: links to global expansion of harmful cyanobacteria. Water Res. 2012;46(5):1349-63.

https://doi.org/10.1016/j.watres.2011.08.002

Paerl HW, Otten TG. Harmful cyanobacterial blooms: causes, consequences, and controls. Microb Ecol. 2012;65(4):995-1010.

https://doi.org/10.1007/s00248-012-0159-y

Ribeiro KF, Duarte L, Crossetti LO. Everything is not everywhere: a tale on the biogeography of cyanobacteria. Hydrobiologia. 2018;820(1):23-48.

https://doi.org/10.1007/s10750-018-3669-x

Scholz SN, Esterhuizen-Londt M, Pflugmacher S. Rise of toxic cyanobacterial blooms in temperate freshwater lakes: Causes, correlations and possible countermeasures. Toxicol Environ Chem. 2017;99(4):543-577.

https://doi.org/10.1080/02772248.2016.1269332

Chorus I, Welker M. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management, 2nd edition. Geneva (CH): CRC Press - Taylor & Francis Group, Boca Raton (FL), on behalf of the World Health Organization; 2021. 858 p.

https://doi.org/10.1201/9781003081449

Salmaso N, Bernard C, Humbert JF, Akçaalan R, Albay M, Ballot A, Catherine A, Fastner J, Häggqvist K, Horecká M, Izydorczyk K, Köker L, Komárek J, Maloufi S, Mankiewicz-Boczek J, Metcalf JS, Quesada A, Quiblier C, Yéprémian C. Basic guide to detection and monitoring of potentially toxic cyanobacteria. In: Meriluoto J, Spoof L, Codd GA, editors. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. 1st ed. Hoboken (NJ): John Wiley & Sons; 2017. p. 46-69.

https://doi.org/10.1002/9781119068761.ch6

Whitton BA, Potts M. Introduction to the cyanobacteria. In: Whitton BA, editor. Ecology of Cyanobacteria II. Dordrecht (NL): Springer; 2012. p. 1-13.

https://doi.org/10.1007/978-94-007-3855-3_1

Visser PM, Verspagen JM, Sandrini G, Stal LJ, Matthijs HC, Davis TW, Paerl HW, Huisman J. How rising CO2 and global warming may stimulate harmful cyanobacterial blooms. Harmful Algae. 2016;54:145-59.

https://doi.org/10.1016/j.hal.2015.12.006

Watson SB, Monis P, Baker P, Giglio S. Biochemistry and genetics of taste-and odor-producing cyanobacteria. Harmful Algae. 2016;54:112-27.

https://doi.org/10.1016/j.hal.2015.11.008

Chorus I, Bartram J. Toxic cyanobacteria in water: a guide to their public health consequences, monitoring and management, 1st ed. [London (UK)]: E & FN Spon, on behalf of the World Health Organization; 1999. 400 p.

https://doi.org/10.1201/9781482295061

Komárek J, Kaštovský J, Mareš J, Johansen JR. Taxonomic classification of cyanoprokaryotes (cyanobacterial genera) 2014, using a polyphasic approach. Preslia. 2014;86:295-335.

Komárek J. Review of the cyanobacterial genera implying planktic species after recent taxonomic revisions according to polyphasic methods: state as of 2014. Hydrobiologia. 2016;764(1):259-70.

https://doi.org/10.1007/s10750-015-2242-0

Komárek J. Delimitation of the family Oscillatoriaceae (Cyanobacteria) according to the modern polyphasic approach (introductory review). Rev Bras Bot. 2018; 41(2):449-56.

https://doi.org/10.1007/s40415-017-0415-y

Mai T, Johansen JR, Pietrasiak N, Bohunicka M, Martin MP. Revision of the Synechococcales (Cyanobacteria) through recognition of four families including Oculatellaceae fam. nov. and Trichocoleaceae fam. nov. and six new genera containing 14 species. Phytotaxa. 2018;365(1):1-59.

https://doi.org/10.11646/phytotaxa.365.1.1

Komárek J. A polyphasic approach for the taxonomy of cyanobacteria: principles and applications. Eur J Phycol. 2016;51(3):346-53.

https://doi.org/10.1080/09670262.2016.1163738

Kaštovský J, Hauer T, Komárek J, Skácelová O. The list of cyanobacterial species of the Czech Republic to the end of 2009. Fottea. 2010;10(2):245-9.

https://doi.org/10.5507/fot.2010.015

Gkelis S, Ourailidis I, Panou M, Pappas N. Cyanobacteria of Greece: an annotated checklist. Biodivers Data J. 2016;4:e10084.

https://doi.org/10.3897/BDJ.4.e10084

Cvijan M, Blaženčić J. Flora algi Srbije, Cyanophyta 1 [Algae flora of Serbia, Cyanophyta 1]. Belgrade (RS): Naučna knjiga; 1996. 290 p. Serbian.

Cvijan M, Laušević R. Floristički sastav algi Vlasinskog jezera u periodu 1949-1993.godine [Floristic composition of algae of the Vlasina Lake in the period 1949-1993]. In: Blaženčić J, editor. Vlasinsko jezero - hidrobiološka studija [Vlasina Lake - hydrobiological study]. Belgrade (RS): Faculty of Biology, University of Belgrade; 1997. p. 61-90. Serbian.

Simić SB. Distribution of blue-green algae (Cyanophyta) in streams of Mt. Stara Planina: Serbia. Arch Biol Sci. 2002;54(3-4):141-8.

https://doi.org/10.2298/ABS0204141S

Karadžić V, Subakov Simić G, Natić D, Ržaničanin A, Ćirić M, Gačić Z. Changes in the phytoplankton community and dominance of Cylindrospermopsis raciborskii (Wolosz.) Subba Raju in a temperate lowland river (Ponjavica, Serbia). Hydrobiologia. 2013;711(1):43-60.

https://doi.org/10.1007/s10750-013-1460-6

Simeunović J, Svirčev Z, Krstić S, Lazić L. Occurrence of cyanobacterial blooms in Vojvodina water ecosystems. Geogr Pannonica. 2005;9:13-9.

https://doi.org/10.5937/GeoPan0509013S

Predojević D, Popović S, Kljajić Ž, Subakov Simić G, Blagojević A, Jovanović J, Lazić M. Diversity of Cyanobacteria in the Zasavica river, Serbia. Arch Biol Sci. 2015;67(2):355-66.

https://doi.org/10.2298/ABS141023024P

Jovanović J, Trbojević I, Subakov Simić G, Popović S, Predojević D, Blagojević A, Karadžić V. The effect of meteorological and chemical parameters on summer phytoplankton assemblages in an urban recreational lake. Knowl Manag Aquat Ecosyst. 2017;418:48.

https://doi.org/10.1051/kmae/2017038

Blagojević Ponjavić A, Kostić D, Marjanović P, Trbojević I, Popović S, Predojević D, Subakov Simić G. Bloom of the potentially toxic cyanobacterium P. rubescens: seasonal distribution and possible drivers of its proliferation in the Vrutci reservoir (Serbia). Oceanol Hydrobiol Stud. 2019;48(4):316-27.

https://doi.org/10.2478/ohs-2019-0029

Đorđević NB, Simić SB. Cyanobacterial blooms in oligosaline and alkaline microaccumulation before and after rehabilitation. Pol J Environ Stud. 2014;23(6):1975-82.

Svirčev Z, Tokodi N, Drobac D. Review of 130 years of research on cyanobacteria in aquatic ecosystems in Serbia presented in a Serbian Cyanobacterial Database. Adv Oceanogr Limnol. 2017;8(1):153-60.

https://doi.org/10.4081/aiol.2017.6360

Đorđević NB, Simić SB, Ćirić AR. First Identification of the Cylindrospermopsin (Cyn)-Producing Cyanobacterium Cylindrospermopsis raciborskii (Woloszynska) Seenayya & Subba Raju in Serbia. Fresenius Environ Bull. 2015;24(11a):3736-42.

EN 15708:2010. Water quality - Guidance standard for the surveying, sampling and laboratory analysis of phytobenthos in shallow running water. European Committee for Standardization (CEN). 2010. 22 p.

EN 16698:2016. Water quality - Guidance on quantitative and qualitative sampling of phytoplankton from inland waters. European Committee for Standardization (CEN). 2016. 35 p.

Komárek J, Anagnostidis K. Cyanoprokaryota 1. Teil: Chroococcales. In: Büdel B, Gärtner G, Krienitz L, Schagerl M, editors. Süsswasserflora von Mitteleuropa, Bd. 19/1. Spektrum Akademischer Verlag (DE): Springer; 1998. 759 p.

Komárek J, Anagnostidis K. Cyanoprokaryota 2. Teil: Oscillatoriales. In: Büdel B, Gärtner G, Krienitz L, Schagerl M, editors. Süsswasserflora von Mitteleuropa, Bd. 19/2. Spektrum Akademischer Verlag (DE): Springer; 2005. 548 p.

Komárek J. Cyanoprokaryota 3. Teil: Heterocystous Genera. In: Büdel B, Gärtner G, Krienitz L, Schagerl M, editors. Süßwasserflora von Mitteleuropa, Bd. 19/3. Verlag-Berlin-Heidelberg (DE): Springer; 2013. 1130 p.

https://doi.org/10.1007/978-3-8274-2737-3

Guiry MD, Guiry GM. AlgaeBase. World-wide electronic publication, National University of Ireland, Galway [Internet]. [updated 2021 Oct 4; cited 2022 Jan 24]. Available from: https://www.algaebase.org.

Jovanović J. Rasprostranjenje cijanobakterija u površinskim vodama namenjenim za vodosnabdevanje i rekreaciju u Srbiji [The distribution of cyanobacteria in surface waters in relation to water supply and recreation in Serbia] [dissertation]. [Belgrade]: Faculty of Biology, University of Belgrade (RS). 2020. 291 p. Serbian.

Dow CS, Swoboda UK. Cyanotoxins. In: Whitton BA, Potts M, editors. The ecology of cyanobacteria: their diversity in time and space. [New York (NY)]: Springer Science & Business Media; 2007. p. 612-22.

Quiblier C, Wood S, Echenique-Subiabre I, Heath M, Villeneuve A, Humbert J-F. A review of current knowledge on toxic benthic freshwater cyanobacteria-ecology, toxin production and risk management. Water Res. 2013;47(15):5464-79.

https://doi.org/10.1016/j.watres.2013.06.042

Rangel M, Martins JC, Garcia AN, Conserva GA, Costa-Neves A, Sant'Anna CL, de Carvalho LR. Analysis of the toxicity and histopathology induced by the oral administration of Pseudanabaena galeata and Geitlerinema splendidum (cyanobacteria) extracts to mice. Mar Drugs. 2014;12(1):508-24.

https://doi.org/10.3390/md12010508

Bernard C, Ballot A, Thomazeau S, Maloufi S, Furey A, Mankiewicz-Boczek J, Pawlik-Skowrońska B, Capelli C, Salmaso N. Appendix 2: Cyanobacteria associated with the production of cyanotoxins. In: Meriluoto J, Spoof L, Codd GA, editors. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. 1st ed. Hoboken (NJ): John Wiley & Sons; 2016. p. 501-25.

https://doi.org/10.1002/9781119068761.app2

Cirés S, Ballot A. A review of the phylogeny, ecology and toxin production of bloom-forming Aphanizomenon spp. and related species within the Nostocales (cyanobacteria). Harmful Algae. 2016;54:21-43.

https://doi.org/10.1016/j.hal.2015.09.007

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, Janeček EA review of the alien and expansive species of freshwater cyanobacteria and algae in the Czech Republic. Biol Invasions. 2010;12(10):3599-625.

https://doi.org/10.1007/s10530-010-9754-3

Wilk-Woźniak E, Najberek, K. Towards clarifying the presence of alien algae in inland waters - can we predict places of their occurrence? Biologia. 2013;68(5):838-44.

https://doi.org/10.2478/s11756-013-0221-3

Kokociński M, Akçaalan R, Salmaso N, Stoyneva-Gärtner MP, Sukenik A. Expansion of alien and invasive cyanobacteria. In: Meriluoto J, Spoof L, Codd GA, editors. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. 1st ed. Hoboken (NJ): John Wiley & Sons; 2017. p. 28-39.

https://doi.org/10.1002/9781119068761.ch4

Ter Braak CJF, Šmilauer P. Canoco Reference Manual and User's Guide: Software for Ordination, Version 5.0. Ithaca (GR): Microcomputer Power; 2012. 496 p.

Suthers MI, Rissik D. Plankton - A guide to their ecology and monitoring for water quality. Clayton (AU): CSIRO Publishing; 2009. 248 p.

https://doi.org/10.1071/9780643097131

O'Neil JM, Davis TW, Burford MA, Gobler CJ. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful algae. 2012;14:313-34.

https://doi.org/10.1016/j.hal.2011.10.027

Shan K, Song L, Chen W, Li L, Liu L, Wu Y, Jia Y, Zhou Q, Peng L. Analysis of environmental drivers influencing interspecific variations and associations among bloom-forming cyanobacteria in large, shallow eutrophic lakes. Harmful algae. 2019;84:84-94.

https://doi.org/10.1016/j.hal.2019.02.002

Almanza V, Pedreros P, Laughinghouse IV HD, Félez J, Parra O, Azócar M, Urrutia R. Association between trophic state, watershed use, and blooms of cyanobacteria in south-central Chile. Limnologica. 2019;75:30-41.

https://doi.org/10.1016/j.limno.2018.11.004

Watson SB, Whitton BA, Higgins SN, Paerl HW, Brooks BW, Wehr JD. Harmful Algal Blooms. In: Wehr JD, Sheath RG, Kociolek JP, editors. Freshwater Algae of North America: Ecology and Classification, 2nd ed. [Cambridge (MA)]: Academic Press (imprint of Elsevier); 2015. p. 873-920.

https://doi.org/10.1016/B978-0-12-385876-4.00020-7

Watson SB, Zastepa A, Boyer GL, Matthews E. Algal bloom response and risk management: on-site response tools. Toxicon. 2017;129:144-52.

https://doi.org/10.1016/j.toxicon.2017.02.005

Kosten S, Huszar VL, Bécares E, Costa LS, van Donk E, Hansson LA, Jeppesen E, Kruk C, Lacerot G, Mazzeo N, de Meester L, Moss B, Lürling M, Nõges T, Romo S, Scheffer M. Warmer climates boost cyanobacterial dominance in shallow lakes. Glob Chang Biol. 2012;18(1):118-26.

https://doi.org/10.1111/j.1365-2486.2011.02488.x

Fabrin TMC, Stabile BHM, da Silva MV, Jati S, Rodrigues L, de Oliveira AV. Cyanobacteria in an urban lake: hidden diversity revealed by metabarcoding. Aquatic Ecol. 2020;54(2):671-5.

https://doi.org/10.1007/s10452-020-09763-z

Jasser I, Callieri C. Picocyanobacteria: The Smallest Cell‐Size Cyanobacteria. In: Meriluoto J, Spoof L, Codd GA, editors. Handbook of Cyanobacterial Monitoring and Cyanotoxin Analysis. 1st ed. Hoboken (NJ): John Wiley & Sons; 2017. p. 19-27.

https://doi.org/10.1002/9781119068761.ch3

Gaysina LA, Saraf A, Singh P. Cyanobacteria in diverse habitats. In: Mishra AK, Tiwari DN, Rai AN, editors. Cyanobacteria: From Basic Science to Applications. Cambridge (MA): Academic Press; 2019. p. 1-28.

https://doi.org/10.1016/B978-0-12-814667-5.00001-5

Stockner J, Callieri C, Cronberg G. Picoplankton and other non-bloom-forming cyanobacteria in lakes. In: Whitton BA, Potts M, editors. The ecology of cyanobacteria. Dordrecht (NL): Springer; 2000. p. 195-231.

https://doi.org/10.1007/0-306-46855-7_7

Śliwińska-Wilczewska S, Maculewicz J, Barreiro Felpeto A, Latała A. Allelopathic and bloom-forming picocyanobacteria in a changing world. Toxins. 2018;10(1):48.

https://doi.org/10.3390/toxins10010048

Thomson-Laing G, Puddick J, Laroche O, Fulton S, Steiner K, Heath MW, Wood SA. Broad and fine scale variability in bacterial diversity and cyanotoxin quotas in benthic cyanobacterial mats. Front microbiol. 2020;11:129.

https://doi.org/10.3389/fmicb.2020.00129

Kokociński M, Soininen J. New insights into the distribution of alien cyanobacterium Chrysosporum bergii (Nostocales, Cyanobacteria). Psychol Res. 2019;67(3):208-214.

https://doi.org/10.1111/pre.12373

Budzyńska A, Gołdyn R. Domination of invasive Nostocales (Cyanoprokaryota) at 52° N latitude. Psychol Res. 2017;65(4):322-32.

https://doi.org/10.1111/pre.12188