Abstract
Eutrophication is recognized as the main water quality problem worldwide, mainly due to the prevalence of harmful cyanobacterial blooms. Submerged macrophytes can control cyanobacterial biomass by removing nutrients from the water column or producing allelopathic compounds. As a result, they are highlighted as a potential strategy for restoring eutrophic waters. However, studies in semi-arid tropical ecosystems have shown inconsistent results regarding the effects of submerged macrophytes on cyanobacterial communities and cyanotoxin production. The aim of this study was to assess the effect of submerged macrophytes on cyanobacterial community structure and microcystin production in a tropical semi-arid reservoir subject to intense periods of water level drawdown. Submerged macrophyte cover, surface water physical and chemical variables, cyanobacterial community biovolume and microcystin concentration were measured monthly between October 2014 and July 2015 at the entrance of the river (Zone I) and dam zones (Zone II) of a reservoir. Although both zones were dominated by the submerged macrophyte Egeria densa, there were significant differences in macrophyte cover: Zone I had greater submerged macrophyte cover and Zone II had lower submerged macrophyte cover. Higher total cyanobacterial biovolume, potential microcystin producer biovolume and microcystin concentrations were observed in the zone with the greater submerged macrophyte cover. Moreover, our results showed that nutrient concentrations (total phosphorous, total nitrogen and ammonium) and physical variables (water temperature and turbidity) were also associated with the zone with greater submerged macrophyte cover. This study highlights that the water level drawdown of the reservoir appears to have favored an increase in nutrient concentration, especially in the zones with dense vegetation, which may have contributed to the coexistence of the high cyanobacteria biomass, high submerged macrophyte coverage and high microcystin concentration. Thus, developing strategies for the management of submerged macrophyte cover during water level drawdown events is essential for improving water quality and reducing the risk of harmful cyanobacterial blooms at the ecosystem level in tropical semi-arid aquatic ecosystems.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Availability of data and material
Following the acceptance of the manuscript, data can be obtained from the author on request.
Code availability
Not applicable.
References
AESA (2021) Agência Executiva de Gestão das Águas do Estado da Paraíba. http://www.aesa.pb.gov.br
Alvares CA, Stape JL, Sentelhas PC, Moraes G, Leonardo J, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Z 22:711–728. https://doi.org/10.1127/0941-2948/2013/0507
Amorim CA, Ulisses C, Moura AN (2017) Biometric and physiological responses of Egeria densa Planch. cultivated with toxic and non-toxic strains of Microcystis. Aquat Toxicol 191:201–208. https://doi.org/10.1016/j.aquatox.2017.08.012
Amorim CA, Moura AN (2020) Effects of the manipulation of submerged macrophytes, larger zooplankton, and nutrients on a cyanobacterial bloom: a mesocosm study in a tropical shallow reservoir. Environ Pollut 265:114997. https://doi.org/10.1016/j.envpol.2020.114997
ANA (2017) Agência Nacional de Águas (Brasil). Reservatórios do Semiárido Brasileiro: Hidrologia, Balanço Hídrico e Operação. Brasília, Brasil
Anderson MJ (2017) Permutational multivariate analysis of variance (PERMANOVA). In: Balakrishnan N, Colton T, Everitt B, Piegorsch W, Ruggeri F, Teugels JL (eds) Wiley StatsRef: Statistics Reference Online. Wiley, Hoboken. https://doi.org/10.1002/9781118445112.stat07841
Andersen MR, Sand-Jensen K, Woolway RI, Jones ID (2017) Profound daily vertical stratification and mixing in a small, shallow, wind-exposed lake with submerged macrophytes. Aquat Sci 79:395–406. https://doi.org/10.1007/s00027-016-0505-0
Antunes JT, Leão PN, Vasconcelos VM (2015) Cylindrospermopsis raciborskii: review of the distribution, phylogeography, and ecophysiology of a global invasive species. Front Microbiol 6:473. https://doi.org/10.3389/fmicb.2015.00473
APHA (2005) Standard methods for the examination of water and wastewater, vol 21, pp 258–259
Bachmann RW, Horsburgh CA, Hoyer MV, Mataraza LK, Canfield DE (2002) Relations between trophic state indicators and plant biomass in Florida lakes. Hydrobiologia 470:219–234. https://doi.org/10.1023/a:1015660922494
Baker P (1991) Urban Water Research Association of Australia. Identification of Common Noxious Cyanobacteria, Part 1: Nostocales. Australian Centre for Water Treatment and Water Quality Research. Research Report
Baker P (1992) Urban Water Research Association of Australia. Identification of Common Noxious Cyanobacteria, Part 2: Chroococcales, Oscillatoriales. Australian Centre for Water Treatment and Water Quality Research. Research Report
Baldwin DS, Gigney H, Wilson JS, Watson G, Boulding NA (2008) Drivers of water quality in a large water storage reservoir during a period of extreme drawdown. Water Res 42:4711–4724. https://doi.org/10.1016/j.watres.2008.08.020
Barbosa JEL, Medeiros ESF, Brasil J, Cordeiro RS, Crispim MCB, Silva GHG (2012) Aquatic systems in semi-arid Brazil: limnology and management. Acta Limnol Bras 24:103–118. https://doi.org/10.1590/S2179-975X2012005000030
Barbosa VV, Barbosa JEL, Hepp LU, Santino MBC, Nery JF (2017) Anaerobic decomposition of submerged macrophytes in semiarid aquatic systems under different trophic states, Paraíba State, Brazil. Afr J Biotechnol 16:2258–2266. https://doi.org/10.5897/AJB2017.16146
Barbosa VV, Severiano JS, Oliveira DA, Barbosa JEL (2020) Influence of submerged macrophytes on phosphorus in a eutrophic reservoir in a semiarid region. J Limnol. https://doi.org/10.4081/jlimnol.2020.1931
Barbosa JEL, Severiano JS, Cavalcante H, Lucena-Silva D, Mendes CF, Barbosa VV, Silva RDS, Oliveira DA, Molozzi J (2021) Impacts of inter-basin water transfer on the water quality of receiving reservoirs in a tropical semi-arid region. Hydrobiologia 848:651–673. https://doi.org/10.1007/s10750-020-04471-z
Barros MUG, Wilson AE, Leitão JIR, Pereira SP, Buley RP, Fernandez-Figueroa EG, Capelo-Neto J (2019) Environmental factors associated with toxic cyanobacterial blooms across 20 drinking water reservoirs in a semi-arid region of Brazil. Harmful Algae 86:128–137. https://doi.org/10.1016/j.hal.2019.05.006
Barroso GM (1984) Sistemática de angiospermas do Brasil. Minas Gerais, Brazil
Bove CP, Paz J (2009) Guia de campo das plantas aquáticas do Parque Nacional da Restinga de Jurubatiba. Rio de Janeiro
Brasil J, Attayde JL, Vasconcelos FR, Dantas DDF, Huszar VLM (2016) Drought-induced water-level reduction favors cyanobacteria blooms in tropical shallow lakes. Hydrobiologia 770:145–164. https://doi.org/10.1007/s10750-015-2578-5
Camargo A, Pezzato M, Henry-Silva G, Assumpção A (2006) Primary production of Utricularia foliosa L., Egeria densa Planchon and Cabomba furcata Schult & Schult. from rivers of the coastal plain of the State of São Paulo, Brazil. Hydrobiologia 570:35–39. https://doi.org/10.1007/s10750-006-0190-4
Canfield DF Jr, Shireman JV, Colle DE, Haller WT, Watkins CEII, Maceina MJ (1984) Prediction of chlorofyll-a concentrations in Florida lakes: importance of aquatic macrophytes. Can J Fish Aquat Sci 41:497–501. https://doi.org/10.1139/f84-059
Chang X, Eigemann F, Hilt S (2012) Do macrophytes support harmful cyanobacteria? Interactions with a green alga reverse the inhibiting effects of macrophyte allelochemicals on Microcystis aeruginosa. Harmful Algae 19:76–84. https://doi.org/10.1016/j.hal.2012.06.002
Codd GA, Morrison LF, Metcalf JS (2005) Cyanobacterial toxins: risk management for health protection. Toxicol Appl Pharmacol 203(3):264–272. https://doi.org/10.1016/J.TAAP.2004.02.016
Costa DF, Barbosa JEL, Dantas EW (2016) Productivity-diversity relationships in reservoir phytoplankton communities in the semi-arid region of northeastern Brazil. J Arid Environ 129:64–70. https://doi.org/10.1016/j.jaridenv.2016.02.010
Dittmann E, Wiegand C (2006) Cyanobacterial toxins—occurrence, biosynthesis and impact on human affairs. Mol Nutr Food Res 50(1):7–17. https://doi.org/10.1002/mnfr.200500162
Dokulil MT (2015) Vegetative survival of Cylindrospermopsis raciborskii (Cyanobacteria) at low temperature and low light. Hydrobiologia 764:241–247. https://doi.org/10.1007/s10750-015-2228-y
Donk EV, van de Bund WJ (2002) Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquat Bot 72:261–274. https://doi.org/10.1016/s0304-3770(01)00205-4
Douma M, Loudiki M, Oudra B, Mouhri K, Ouahid Y, del Campo FF (2009) Taxonomic diversity and toxicological assessment of Cyanobacteria in Moroccan inland waters. Revue des sciences de l'eau 22(3):435–449. https://doi.org/10.7202/037781ar
Downing TG, Phelan RR, Downing S (2015) A potential physiological role for cyanotoxins in cyanobacteria of arid environments. J Arid Environ 112:147–151. https://doi.org/10.1016/j.jaridenv.2014.02.005
Eigemann F, Hilt S, Schmitt-Jansen M (2013) Flow cytometry as a diagnostic tool for the effects of polyphenolic allelochemicals on phytoplankton. Aquat Bot 104:5–14. https://doi.org/10.1016/j.aquabot.2012.10.005
Gross EM, Hilt S, Lombardo P, Mulderij G (2007) Searching for allelopathic effects of submerged macrophytes on phytoplankton-state of the art and open questions. Hydrobiologia 584:77–88. https://doi.org/10.1007/s10750-007-0591-z
Ha MH, Contardo-Jara V, Pflugmacher S (2014) Uptake of the cyanobacterial neurotoxin, anatoxin-a, and alterations in oxidative stress in the submerged aquatic plant Ceratophyllum demersum. Ecotoxicol Environ Saf 101:205–212. https://doi.org/10.1016/j.ecoenv.2013.12.023
Ha MH, Pflugmacher S (2013) Phytotoxic effects of the cyanobacterial neurotoxin anatoxin-a: morphological, physiological and biochemical responses in aquatic macrophyte, Ceratophyllum demersum. Toxicon 70:1–8. https://doi.org/10.1016/j.toxicon.2013.03.021
Herb WR, Stefan HG (2004) Temperature stratification and mixing dynamics in a shallow lake with submersed macrophytes. Lake Reserv Manag 20:296–308. https://doi.org/10.1080/07438140409354159
Hillebrand H, Dürselen CD, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424. https://doi.org/10.1046/j.1529-8817.1999.3520403.x
Hilt S, Gross EM (2008) Can allelopathically active submerged macrophytes stabilise Clearwater states in shallow eutrophic lakes? Bas Appl Ecol 9:422–432. https://doi.org/10.1016/j.baae.2007.04.003
Jasser I (1995) The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306:21–32. https://doi.org/10.1007/bf00007855
Keitel J, Zak D, Hupfer M (2016) Water level fluctuations in a tropical reservoir: the impact of sediment drying, aquatic macrophyte dieback, and oxygen availability on phosphorus mobilization. Environ Sci Pollut Res 23:6883–6894. https://doi.org/10.1007/s11356-015-5915-3
Kim K, Park C, Yoon Y, Hwang S (2018) Harmful cyanobacterial material production in the North Han river (South Korea): genetic potential and temperature-dependent properties. Int J Environ Res Public Health 15(3):444–461. https://doi.org/10.3390/ijerph15030444
Komarek J, Anagnostidis K (1986) Modern approach to the classification system of cyanophytes. 2-Chroococcales. Arch Hydrobiol Suppl 73(2):157–226
Kosten S, Lacerot G, Jeppesen E, Marques DDM, van Nes EH, Mazzeo N, Scheffer M (2009) Effects of submerged vegetation on water clarity across climates. Ecosystems 12:1117–1129. https://doi.org/10.1007/s10021-009-9277-x
Lacet JB, Moura AN, Dantas EW (2019) Invasion of Egeria densa Planch. in semiarid reservoirs. Braz J Bot 42:491–497. https://doi.org/10.1007/s40415-019-00548-9
Legendre P, Legendre L (1998) Numerical ecology. Second English edition. Elsevier Science, Amsterdam, The Netherlands
Li X, Dreher TW, Li R (2016) An overview of diversity occurrence genetics and toxin production of bloom-forming Dolichospermum (Anabaena) species. Harmful Algae 54:54–68. https://doi.org/10.1016/j.hal.2015.10.015
Lins RPM, Barbosa LG, Minillo A, Ceballos BSO (2016) Cyanobacteria in a eutrophicated reservoir in a semi-arid region in Brazil: dominance and microcystin events of blooms. Braz J Bot 39(2):583–591. https://doi.org/10.1007/s40415-016-0267-x
Lu J, Bunn SE, Burford MA (2018) Nutrient release and uptake by littoral macrophytes during water level fluctuations. Sci Total Environ 622–623:29–40. https://doi.org/10.1016/j.scitotenv.2017.11.199
McCullagh P, Nelder JA (1989) Generalized linear models, 2nd edn. Chapman & Hall, London, p 532
Meerhoff M, Clemente JM, De Mello FT, Iglesias C, Pedersen AR, Jeppesen E (2007) Can warm climate related structure of littoral predator assemblies weaken the clear water state in shallow lakes? Glob Chang Biol 13:1888–1897. https://doi.org/10.1111/j.1365-2486.2007.01408.x
Meerhoff M, Fosalba C, Bruzzone C, Mazzeo N, Noordoven W, Jeppesen E (2006) An experimental study of habitat choice by Daphnia: plants signal danger more than refuge in subtropical lakes. Freshw Biol 51:1320–1330. https://doi.org/10.1111/j.1365-2427.2006.01574.x
Mez K, Beattie K, Codd G, Hanselmann K, Hauser B, Naegeli H, Preisig H (1997) Identification of a microcystin in benthic cyanobacteria linked to cattle deaths on alpine pastures in Switzerland. Eur J Phycol 32(2):111–117. https://doi.org/10.1080/09670269710001737029
Mohamed ZA (2017) Macrophytes-cyanobacteria allelopathic interactions and their implications for water resources management—a review. Limnologica 63:122–132. https://doi.org/10.1016/j.limno.2017.02.006
Mohamed ZA, Al-Shehri AM (2010) Microcystin production in epiphytic cyanobacteria on submerged macrophytes. Toxicon 55(7):1346–1352. https://doi.org/10.1016/j.toxicon.2010.02.007
Mohamed ZA, Al-Shehri AM (2013) Grazing on Microcystis aeruginosa and degradation of microcystins by the heterotrophic flagellate Diphylleia rotans. Ecotox Environ Safe 96:48–52. https://doi.org/10.1016/j.ecoenv.2013.06.015
Mori ES, Martins D, Velini ED, Marino CL, Gouvêa CF, Leite SMM, Camacho E, Guries RP (2012) Genetic diversity in Egeria densa and E. najas in Jupiá Reservoir. Brazil Cien Inv Agric 39:321–330. https://doi.org/10.4067/S0718-16202012000200008
Moura AN, Aragão-Tavares NKC, Amorim CA (2018) Cyanobacterial blooms in freshwater bodies from a semiarid region, Northeast Brazil: a review. J Limnol 77(2):179–188. https://doi.org/10.4081/jlimnol.2018.1646
Muri G, Čermelj B, Jaćimović R, Ravnikar T, Šmuc A, Turšič J, Vreča P (2018) Factors that contributed to recent eutrophication of two Slovenian mountain lakes. J Paleolimnol 59(4):411–426. https://doi.org/10.1007/s10933-017-9996-5
Naselli-Flores L (2003) Man-made lakes in Mediterranean semi-arid climate: the strange case of Dr Deep Lake and Mr Shallow Lake. Hydrobiologia 506:13–21. https://doi.org/10.1023/B:HYDR.0000008550.34409.06
Panou M, Zervoub SK, Kaloudisc T, Hiskiab A, Gkelis S (2018) A Greek Cylindrospermopsis raciborskii strain: missing link in tropic invader’s phylogeography tale. Harmful Algae 80:96–106. https://doi.org/10.1016/j.hal.2018.10.002
Pekár S, Brabec M (2017) Generalized estimating equations: A pragmatic and flexible approach to the marginal GLM modelling of correlated data in the behavioural sciences. Ethology 124(2):86–93. https://doi.org/10.1111/eth.12713
Pflugmacher S (2004) Promotion of oxidative stress in C. demersum due to exposure to cyanobacterial toxin. Aquat Toxicol 70:169–178. https://doi.org/10.1016/j.aquatox.2004.06.010
R Core Team (2019) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.rproject.org/
Redekop P, Hofstra D, Hussner A (2016) Elodea canadensis shows a higher dispersal capacity via fragmentation than Egeria densa and Lagarosiphon major. Aquat Bot 130:45–49. https://doi.org/10.1016/j.aquabot.2016.01.004
Reynolds C, Huszar V, Kruk C, Naselli-Flores L, Melo S (2002) Towards a functional classification of the freshwater phytoplankton. J Plankton Res 24:417–428. https://doi.org/10.1093/plankt/24.5.417
Riis T, Olesen B, Clayton JS, Lambertini C, Brix H, Sorrell BK (2012) Growth and morphology in relation to temperature and light availability during the establishment of three invasive aquatic plant species. Aquat Bot 102:56–64. https://doi.org/10.1016/j.aquabot.2012.05.002
Romero-Oliva CS, Contardo-Jara V, Block T, Pflugmacher S (2014) Accumulation of microcystin congeners in different aquatic plants and crops—a case study from lake Amatitlán. Guatemala Ecotoxicol Environ Saf 102:121–128. https://doi.org/10.1016/j.ecoenv.2014.01.031
Sand-Jensen K, Andersen MR, Martinsen KT, Borum J, Kristensen E, Kragh T (2019) Shallow plant-dominated lakes—extreme environmental variability, carbon cycling and ecological species challenges. Ann Bot XX:1–12. https://doi.org/10.1093/aob/mcz084
Sand-Jensen K, Møller CL, Borum J (2015) High resistance of oligotrophic isoetid plants to oxic and anoxic dark exposure. Freshw Biol 60:1044–1051. https://doi.org/10.1111/fwb.12570
Silva RDS, Severiano JS, Oliveira DA, Mendes CF, Barbosa VV, Chia MA, Barbosa JEL (2019) Spatio-temporal variation of cyanobacteria and cyanotoxins in public supply reservoirs of the semi-arid region of Brazil. J Limnol. https://doi.org/10.4081/jlimnol.2019.1893
Smith VH, Schindler DW (2009) Eutrophication science: where do we go from here? Trends Ecol Evol 24(4):201–207. https://doi.org/10.1016/j.tree.2008.11.009
Štern A, Rotter A, Novak M, Filipič M, Žegura B (2019) Genotoxic effects of the cyanobacterial pentapeptide nodularin in HepG2 cells. Food Chem Toxicol 124:349–358. https://doi.org/10.1016/j.fct.2018.12.019
Švanys A, Eigemann F, Grossart HP, Hilt S (2016) Microcystins do not necessarily lower the sensitivity of Microcystis aeruginosa to tannic acid. FEMS Microbiol Lett 363:fnv227. https://doi.org/10.1093/femsle/fnv227
Szigeti ZM, Jámbrik K, Roszik J, M-Hamvas M, Tándor I, Beyer D, Vasas G, Vereb G, Surányi G, Máthe C (2010) Cytoskeletal and developmental alterations in Ceratophyllum demersum induced by microcystin-LR, a cyanobacterial toxin. Aquat Bot 92:179–184. https://doi.org/10.1016/j.aquabot.2009.11.003
Utermöhl H (1958) Zurvervollkommnung der quantitativen phytoplankton-methodik. Mitt Int Ver Theor Angew Limnol 9:1–38
Vanderstukken M, Mazzeo N, Van Colen W, Declerck SAJ, Muylaert K (2011) Biological control of phytoplankton by the subtropical submerged macrophytes Egeria densa and Potamogeton illinoensis: a mesocosm study. Freshw Biol 56:1837–1849. https://doi.org/10.1111/j.1365-2427.2011.02624.x
Vilas MP, Marti CL, Adams MP, Oldham CE, Hipsey MR (2017) Invase MAcrophytes COntrol the spatial and temporal patterns of temperature and dissolved oxygen in shallow lake: a proposed feedback mechanism of macrophyte loss. Front Plant Sci 8:2097. https://doi.org/10.3389/fpts.2017.02097
Vilas MP, Marti CL, Oldham CE, Hipsey MR (2018) Macrophyte-induced thermal stratification in a shallow urban lake promotes conditions suitable for nitrogen-fixing cyanobacteria. Hydrobiologia 806:411–426. https://doi.org/10.1007/s10750-017-3376-z
Warton DI, Lyons M, Stoklosa J, Ives AR (2016) Three points to consider when choosing a LM or GLM test for count data. Methods Ecol Evol 7(8):882–890. https://doi.org/10.1111/2041-210X.12552
Funding
This study was funded by Ministry of Science, Technology and Innovation/Financier of Studies and Projects (MCTI/FINEP—CTHIDRO 01/2013) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior—Brazil (CAPES)—Finance Code 001.
Author information
Authors and Affiliations
Contributions
FMM and JELB helped in conceptualization; FMM contributed to data curation and methodology; FMM and GCM formally analyzed the study and wrote the original draft; FMM, GCM, JSS, CFM investigated; JELB acquired the funding, administrated the project and contributed to resources; JSS and JELB supervised the project; FMM, GCM, JSS, JELB validated the study; FMM, GCM, JSS, CFM, JELB helped in visualization and writing—review & editing.
Corresponding author
Ethics declarations
Conflicts of interest
The authors declare that they have no known competing financial interests or personal relationships that may have influenced the work reported in this paper.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Handling Editor: Man Xiao.
Rights and permissions
About this article
Cite this article
Monteiro, F.M., Moura, G.C., Severiano, J.S. et al. Submerged macrophytes support cyanobacteria and microcystin production in a drawdown tropical semi-arid reservoir. Aquat Ecol 55, 875–890 (2021). https://doi.org/10.1007/s10452-021-09866-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10452-021-09866-1