Skip to main content
Log in

Allelopathic Inhibition Effects of Myriophyllum spicatum on Growths of Bloom-Forming Cyanobacteria and Other Phytoplankton Species in Coexistence Experiments

  • Research Article
  • Published:
Journal of Plant Biology Aims and scope Submit manuscript

Abstract

Many studies have attempted to find measures for control of cyanobacterial harmful algal blooms (cyanoHABs) caused by Microcystis, Anabaena, and other bloom-forming plankton species. We have investigated allelopathic inhibition of the submerged macrophyte Myriophyllum spicatum on four phytoplankton species of two taxonomic groups: Chlorophyta Selenastrum capricornutum, Scenedesmus obliquus, and cyanobacteria Microcystis aeruginosa (different strains for toxic, non-toxic, the North Han River originated (NHR) and colonies) and Anabaena circinalis. Inhibitions of unicellular cyanobacteria M. aeruginosa were over 50% for three consecutive days from the 3rd to the 5th day of the coexistence. M. spicatum even inhibited M. aeruginosa at a high initial concentration (1.1 mg L−1 Chl-a). Moreover, M. aeruginosa in a mixture of four phytoplankton species (S. capricornutum, S. obliquus, M. aeruginosa and A. circinalis) was selectively inhibited by M. spicatum. The inhibition of toxic, non-toxic, and NHR of Microcystis by M. spicatum were not significantly different. Colonial cyanobacteria strains were mostly not inhibited by M. spicatum.

This is a preview of subscription content, log in via an institution to check access.

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Adams MSDMM (1974) Seasonal production of the Myriophyllum component of the littoral of Lake Wingra. Wisconsin J Ecol 62:457–465

    Article  Google Scholar 

  • Bauer N, Blaschke U, Beutler E, Gross EM, Jenett-Siems K, Siems K, Hilt S (2009) Seasonal and interannual dynamics of polyphenols in Myriophyllum verticillatum and their allelopathic activity on Anabaena variabilis. Aquat Bot 91:110–116. https://doi.org/10.1016/j.aquabot.2009.03.005

    Article  CAS  Google Scholar 

  • Bold HC (1949) The morphology of Chlamydomonas chlamydogama Sp. Nov. Bull Torrey Bot Club 76:101–108

    Article  Google Scholar 

  • Canter-Lund H, Lund JW (1995) Freshwater algae: their microscopic world explored, 1st edn, Balogh Scientific Books

  • 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

    Article  CAS  Google Scholar 

  • Desikachary TV (1959) Cyanophyta. Indian Council of Agricultural Research, pp 81–98

  • Eaton AD, Clesceri LS, Rice EW, Greenberg AE (2005) Standard methods for the examination of water and wasteater, centennial edition, 21st edn. Amer Public Health Assn

  • EPA, United States Environmental Protection Agency (2019) Recommendations for cyanobacteria and cyanotoxin monitoring in recreational waters. EPA 823-R-19-001

  • Gross EM (1999) Allelopathy in benthic and littoral areas: case studies on allelochemicals from benthic cyanobacteria and submersed macrophytes. In: Principles and practices in plant ecology. CRC Press, pp 179–199

  • Gross EM (2000) Seasonal and spatial dynamics of allelochemicals in the submersed macrophyte Myriophyllum spicatum L. SIL Proc 27:2116–2119

    CAS  Google Scholar 

  • Gross EM (2003) Allelopathy of aquatic autotrophs CRC. Crit Re Plant Sci 22:313–339. https://doi.org/10.1080/713610859

    Article  Google Scholar 

  • Gross EM, Sütfeld R (1994) Polyphenols with algicidal activity in the submerged macrophyte Myriophyllum spicatum L. Int Symp Nat Phenols Plant Resist 381:710–716

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Gross EM, Meyer H, Schilling G (1996) Release and ecological impact of algicidal hydrolysable polyphenols in Myriophyllum spicatum. Phytochemistry 41, 133–138. https://doi.org/10.1016/0031-9422(95)00598-6

    Article  CAS  Google Scholar 

  • He Y, Zhou QH, Liu BY, Cheng L, Tian Y, Zhang YY, Wu ZB (2016) Programmed cell death in the cyanobacterium Microcystis aeruginosa induced by allelopathic effect of submerged macrophyte Myriophyllum spicatum in co-culture system. J Appl Phycol. https://doi.org/10.1007/s10811-016-0814-7

    Article  Google Scholar 

  • Hilt (nee Körner), S., (2006) Allelopathic inhibition of epiphytes by submerged macrophytes. Aquat Bot 85:252–256. https://doi.org/10.1016/j.aquabot.2006.05.004

    Article  Google Scholar 

  • Hilt (nee Körner)Lombardo SP (2010) Effects of macrophytes on phytoplankton: nutrient uptake versus allelopathy. SIL Proc (1922–2010) 30:1317–1320. https://doi.org/10.1080/03680770.2009.11902323

    Article  Google Scholar 

  • Hilt S, Gross EM (2008) Can allelopathically active submerged macrophytes stabilise clear-water states in shallow lakes? Basic Appl Ecol 9:422–432. https://doi.org/10.1016/j.baae.2007.04.003

    Article  Google Scholar 

  • Huisman J, Codd GA, Paerl HW, Ibelings BW, Verspagen JMH, Visser PM (2018) Cyanobacterial blooms. Nat Rev Microbiol 16:471–483. https://doi.org/10.1038/s41579-018-0040-1

    Article  CAS  PubMed  Google Scholar 

  • Jasser I (1995) The influence of macrophytes on a phytoplankton community in experimental conditions. Hydrobiologia 306:21–32

    Article  CAS  Google Scholar 

  • Jančula D, Maršálek B (2011) Critical review of actually available chemical compounds for prevention and management of cyanobacterial blooms. Chemosphere 85:1415–1422. https://doi.org/10.1016/j.chemosphere.2011.08.036

    Article  CAS  PubMed  Google Scholar 

  • Joo S, Jung J, Park S (2007) Inhibition of submerged macrophytes on phytoplankton-1. Field evidence for submerged macrophyte inhibition on phytoplankton biomass. Korean J Limnol 40:511–519

    Google Scholar 

  • Jung J (1993) Illustration of the freshwater algae of Korea. Academy Books

  • Kim K, Kim B, Park M, Hwang S (2008) Effect of a freshwater bivalve (Unio douglasiae) and a submerged plant (Potamogeton crispus) on the growth inhibition of a cyanobacterium Oscillatoria sp. Korean J Limnol 41:68–76

    Google Scholar 

  • Körner S, Nicklisch A (2002) Allelopathic growth inhibition of selected phytoplankton species by submerged macrophytes. J Phycol 38:862–871

    Article  Google Scholar 

  • Kwon S, Na H, Jung J, Baek N (2012) A comparison of radical scavenging activity and cyanobacteria growth inhibition of aquatic vascular plants. Korean J Ecol Environ 45:11–20

    Google Scholar 

  • Latour D, Sabido O, Salençon MJ, Giraudet H (2004) Dynamics and metabolic activity of the benthic cyanobacterium Microcystis aeruginosa in the Grangent reservoir (France). J Plankton Res 26:719–726. https://doi.org/10.1093/plankt/fbh075

    Article  CAS  Google Scholar 

  • Leu E, Krieger-Liszkay A, Goussias C, Gross EM (2002) Polyphenolic allelochemicals from the aquatic angiosperm Myriophyllum spicatum inhibit photosystem II. Plant Physiol 130:2011–2018. https://doi.org/10.1104/pp.011593

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lombardo P, Mjelde M, Källqvist T, Brettum P (2013) Seasonal and scale-dependent variability in nutrient- and allelopathy-mediated macrophyte-phytoplankton interactions. Knowl Manag Aquat Ecosyst 409:31. https://doi.org/10.1051/kmae/20130s55

    Article  Google Scholar 

  • Ministry of Environment Republic of Korea (2019) 2018 Annual report of HABs

  • Molisch (1937) Einfluss einer pflanze auf die andere, allelopathie. English (2001)

  • Nakai S, Inoue Y, Hosomi M, Murakami A (2000) Myriophyllum spicatum-released allelopathic polyphenols inhibiting growth of blue-green algae Microcystis aeruginosa. Water Res 34:3026–3032. https://doi.org/10.1016/S0043-1354(00)00039-7

    Article  CAS  Google Scholar 

  • Nakai S, Yamada S, Hosomi M (2005) Anti-cyanobacterial fatty acids released from Myriophyllum spicatum. Hydrobiologia 543:71–78. https://doi.org/10.1007/s10750-004-6822-7

    Article  CAS  Google Scholar 

  • Nakai S, Zou G, Okuda T, Nishijima W, Hosomi M, Okada M (2012) Polyphenols and fatty acids responsible for anti-cyanobacterial allelopathic effects of submerged macrophyte Myriophyllum spicatum. Water Sci Technol 66:993–999. https://doi.org/10.2166/wst.2012.272

    Article  CAS  PubMed  Google Scholar 

  • Nam S, Joo S, Kim S, Baek NI, Choi HK, Park S (2008) Induced metabolite changes in Myriophyllum spicatum during co-existence experiment with the cyanobacterium Microcystis aeruginosa. J Plant Biol 51:373–378. https://doi.org/10.1007/BF03036141

    Article  CAS  Google Scholar 

  • OECD (2011) Guide lines for the testing of chemicals; Freshwater alga and cyanobacteria, growth inhibition test, #201

  • Park MH, Kim KH, Lee HH, Kim JS, Hwang SJ (2010) Selective inhibitory potential of silver nanoparticles on the harmful cyanobacterium Microcystis aeruginosa. Biotechnol Lett 32:423–428. https://doi.org/10.1007/s10529-009-0161-8

    Article  CAS  PubMed  Google Scholar 

  • Planas D, Sarhan F, Dube L, Godmaire H, C.C., (1981) Ecological significance of phenolic compounds of Myriophyllum spicatum. SIL Proc 21:492–1496

    Google Scholar 

  • Prasanna R, Kumar R, Sood A, Prasanna BM, Singh PK (2006) Morphological, physiochemical and molecular characterization of Anabaena strains. Microbiol Res 161:187–202. https://doi.org/10.1016/j.micres.2005.08.001

    Article  CAS  PubMed  Google Scholar 

  • Santonja M, Le Rouzic B, Thiébaut G (2018) Seasonal dependence and functional implications of macrophyte—phytoplankton allelopathic interactions. Freshw Biol 63:1161–1172. https://doi.org/10.1111/fwb.13124

    Article  CAS  Google Scholar 

  • Shin J, Park Y (2018) Spatiotemporal and longitudinal variability of hydro-meteorology, basic water quality and dominant algal assemblages in the eight weir pools of regulated river (Nakdong). Korean J Ecol Environ 51:268–286. https://doi.org/10.11614/ksl.2018.51.4.268

    Article  Google Scholar 

  • Spencer DF, Ksander GG (1999) Seasonal changes in chemical composition of Eurasian watermilfoil (Myriophyllum spicatum L.) and water temperature at two sites in northern California: implications for herbivory. J Aquat Plant Manag 37:61–66

    Google Scholar 

  • Stanier RY, Kunisawa R, Mandel MCBG (1971) Purification and properties of unicellular blue-green algae (order Chroococcales). Bact Rev 35:171–205

    Article  CAS  Google Scholar 

  • Starr RCZJ (1993) UTEX—the culture collection of algae at the University of Texas at Austin. J Phycol 29:1–106

    Article  Google Scholar 

  • Švanys A, Paškauskas R, Hilt S (2014) Effects of the allelopathically active macrophyte Myriophyllum spicatum on a natural phytoplankton community: a mesocosm study. Hydrobiologia 737:57–66. https://doi.org/10.1007/s10750-013-1782-4

    Article  CAS  Google Scholar 

  • Van Donk E, 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

    Article  Google Scholar 

  • Welschmeyer NA (1994) Fluorometric analysis of chlorophyll a in the presence of chlorophyll b and pheopigments. Limnol Oceanogr 39:1985–1992

    Article  CAS  Google Scholar 

  • Yang Z, Kong F (2012) Formation of large colonies: a defense mechanism of Microcystis aeruginosa under continuous grazing pressure by flagellate Ochromonas sp. J Limnol 71:5. https://doi.org/10.4081/jlimnol.2012.e5

    Article  Google Scholar 

  • Yang D, Park S (2017) Freshwater anostracan, Branchinella kugenumaensis, as a potential controlling consumer species on toxic cyanobacteria Microcystis aeruginosa. Aquat Ecol 51:449–461. https://doi.org/10.1007/s10452-017-9628-1

    Article  Google Scholar 

  • Yuan R, Li Y, Li J, Ji S, Wang S, Kong F (2020) The allelopathic effects of aqueous extracts from Spartina alterniflora on controlling the Microcystis aeruginosa blooms. Sci Total Environ 712:136332. https://doi.org/10.1016/j.scitotenv.2019.136332

  • Zhu J, Liu B, Wang J, Gao Y, Wu Z (2010) Study on the mechanism of allelopathic influence on cyanobacteria and chlorophytes by submerged macrophyte (Myriophyllum spicatum) and its secretion. Aquat Toxicol 98:196–203. https://doi.org/10.1016/j.aquatox.2010.02.011

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Research Foundation of Korea [2016R1A2B4015235].

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Sangkyu Park.

Supplementary Information

Below is the link to the electronic supplementary material.

12374_2021_9322_MOESM1_ESM.tif

Supplementary file1 Supplementary Fig. 1. Chlorophyll a based relative biomass of a green algal species Parachlorella sp. and a cyanobacteria species Synechocystis sp. from individual coexistence experiments with M. spicatum. Error bars show standard errors (n = 5). Student t tests, Welch’s t tests (when non-homogeneity of variance was found) and Wilcoxon-Mann-Whitney tests (for non-parametric data) were performed at 0.05 significance level, and differences between control (without M. spicatum) and treated group (with M. spicatum) on each day are indicated by asterisks. Apical shoot 8 cm of M. spicatum and 50 ml of unialgal cultures for each test vial were used for the experiments (M. spicatum for Parachlorella sp.: 0.24 g dw L−1, ± 0.02, M. spicatum for Synechocystis sp.: 0.37 g dw L−1, ± 0.01 at the end of the experiments). Two algal species were cultivated in 3NBBM. (TIF 12242 kb)

12374_2021_9322_MOESM2_ESM.tif

Supplementary file2 Supplementary Fig. 2 Chlorophyll a based inhibition (%) of three different strains of M. aeruginosa (toxin strain: UTEX 2385, non-toxin: UTEX 2386, the North Han River originated: NHR) from coexistence experiments with M. spicatum. Error bars show standard errors (n = 5). Different small letters indicate significant differences among the three strains assessed by one-way analysis of variance (ANOVA) with subsequent post hoc analysis (Tukey’s HSD test) and non-parametric Kruskal-Wallis test with subsequent Bonferroni test, p < 0.05. (TIF 3579 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Jeong, S., Yang, D., Joo, S. et al. Allelopathic Inhibition Effects of Myriophyllum spicatum on Growths of Bloom-Forming Cyanobacteria and Other Phytoplankton Species in Coexistence Experiments. J. Plant Biol. 64, 501–510 (2021). https://doi.org/10.1007/s12374-021-09322-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12374-021-09322-5

Keywords

Navigation