Abstract
The invasion of submerged aquatic plants potentially results in a loss of native biodiversity in these ecosystems. There has been little attention paid to the impact of invasive submerged plants on epiphytic algal communities. We conducted a 30-day outdoor mesocosm experiment on the shore of subtropical Lake Liangzihu, China, to investigate the effects of two submerged plant species, an invasive species (Elodea nuttallii) and a native species (Hydrilla verticillata), on epiphytic algal communities. We also explored the relationship between macrophyte secondary metabolites and epiphytic algae by conducting a laboratory cultivation experiment. Our results indicate that the epiphytic algal communities on the invasive plant had lower biomass, photosynthesis, abundance, and richness, compared to those on the native species. Secondary metabolites were significantly higher in the invasive plant compared to the native species. Secondary metabolites of plants had the greatest impact on the composition and traits of the epiphytic algal community. The slopes of epiphytic algal community traits were lower across gradients of native plant biomass and secondary metabolites compared to those across gradients of the invasive plant. Our findings suggest that the invasive plant E. nuttallii has a stronger inhibitory effect on epiphytic algae than the native species H. verticillata. This is due to the invasive plant’s higher concentrations of secondary metabolites, which limit the growth of epiphytic algae. These findings emphasize the importance of native aquatic vegetation restoration for biodiversity conservation in shallow aquatic ecosystems, considering the impact of invasive species on epiphytic algal communities.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data are provided as private-for-peer review (shared privately or publicly on a repository). All data used in the production of this article are available via Dryad: https://datadryad.org/stash/share/L1R0irsj4PH17PPvw0nK3n2jSegIT8BBehwyNJYGvig. We state the intended repository where data will be permanently archived if the paper is accepted for publication.
Change history
15 February 2024
A Correction to this paper has been published: https://doi.org/10.1007/s10530-024-03259-9
References
Buldrini F, Pezzi G, Barbero M et al (2022) The invasion history of Elodea canadensis and E. Nuttallii (Hydrocharitaceae) in Italy from herbarium accessions, field records and historical literature. Biol Invasions. https://doi.org/10.1007/s10530-022-02949-6
Callaway RM, Aschehoug ET (2000) Invasive plants versus their new and old neighbors: a mechanism for exotic invasion. Science 290:521–523. https://doi.org/10.1126/science.290.5491.521
Callaway RM, Ridenour WM (2004) Novel weapons: invasive success and the evolution of increased competitive ability. Front Ecol Environ 2:436–443. https://doi.org/10.1890/1540-9295(2004)002[0436:NWISAT]2.0.CO;2
Casartelli MR, Ferragut C (2018) The effects of habitat complexity on periphyton biomass accumulation and taxonomic structure during colonization. Hydrobiologia 807:233–246. https://doi.org/10.1007/s10750-017-3396-8
Cattaneo A, Galanti G, Gentinetta S et al (1998) Epiphytic algae and macroinvertebrates on submerged and floating-leaved macrophytes in an Italian lake. Freshw Biol 39:725–740. https://doi.org/10.1046/j.1365-2427.1998.00325.x
Chambers PA, Lacoul P, Murphy KJ et al (2008) Global diversity of aquatic macrophytes in freshwater. Hydrobiologia 595:9–26. https://doi.org/10.1007/s10750-007-9154-6
Chao C, Lv T, Wang L et al (2022) The spatiotemporal characteristics of water quality and phytoplankton community in a shallow eutrophic lake: implications for submerged vegetation restoration. Sci Total Environ 821:1–11. https://doi.org/10.1016/j.scitotenv.2022.153460
Crane K, Kregting L, Coughlan NE et al (2022) Abiotic and biotic correlates of the occurrence, extent and cover of invasive aquatic Elodea nuttallii. Freshw Biol 67:1559–1570. https://doi.org/10.1111/fwb.13960
Effiong KS, Inyang AI (2015) Epiphyton algae on aquatic macrophyte (water hyacinth) in a tropical lagoon and their possible use as indicator. Int J Environ Monit Anal 3:404–410. https://doi.org/10.11648/j.ijema.20150306.14
Erhard D, Gross EM (2006) Allelopathic activity of Elodea canadensis and Elodea nuttallii against epiphytes and phytoplankton. Aquat Bot 85:203–211. https://doi.org/10.1016/j.aquabot.2006.04.002
Felpeto AB, Roy S, Vasconcelos VM (2017) Allelopathy prevents competitive exclusion and promotes phytoplankton biodiversity. Oikos. https://doi.org/10.1111/oik.04046
Fileto-Perez HA, Rutiaga-Quinones OM, Sytsma MD et al (2015) GC/MS analysis of some extractives from Eichhornia crassipes. BioResources 10:7353–7360
Fleming JP, Dibble ED (2015) Ecological mechanisms of invasion success in aquatic macrophytes. Hydrobiologia 746:23–37
Foerster JW Jr (1965) Phyco-Periphyton in an oligotrophic lake. Trans Am Microscopical Soc 84:485–502
Gallardo B, Clavero M, Sánchez MI et al (2016) Global ecological impacts of invasive species in aquatic ecosystems. Glob Change Biol 22:151–163. https://doi.org/10.1111/gcb.13004
Gao YN, Liu BY, Xu D et al (2011) Phenolic compounds exuded from two submerged Freshwater macrophytes and their allelopathic effects on Microcystis aeruginosa. Pol J Environ Stud 20:1153–1159
Hao B, Wu H, Cao Y et al (2017) Comparison of periphyton communities on natural and artificial macrophytes with contrasting morphological structures. Freshw Biol 62:1783–1793. https://doi.org/10.1111/fwb.12991
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
Hu H, Wei Y (2006) The freshwater algae of China (systematics, taxonomy and ecology). Science Press, Beijing
Inderjit, Simberloff D, Kaur H et al (2021) Novel chemicals engender myriad invasion mechanisms. New Phytol 232:1184–1200. https://doi.org/10.1111/nph.17685
Jiang Z, Guo P, Chang C et al (2014) Effects of allelochemicals from Ficus microcarpa on Chlorella pyrenoidosa. Braz Arch Biol Technol 57:595–605. https://doi.org/10.1590/s1516-8913201401304
Kottuparambil S, Agusti S (2020) Cell-by-cell estimation of PAH sorption and subsequent toxicity in marine phytoplankton. Chemosphere 259:1–10. https://doi.org/10.1016/j.chemosphere.2020.127487
Kuiper JJ, Verhofstad MJJM, Louwers ELM et al (2017) Mowing submerged macrophytes in shallow lakes with alternative stable states: battling the good guys? Environ Manage 59:619–634. https://doi.org/10.1007/s00267-016-0811-2
Lai J, Zou Y, Zhang J et al (2022) Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca.hp R package. Methods Ecol Evol 00:1–7. https://doi.org/10.1111/2041-210X.13800
Li Y, Pang T, Liu J et al (2017) Light absorption and impacts of low salinities on photosynthetic behaviour in the epiphytic alga Neosiphonia Savatieri (Rhodomelaceae, Rhodophyta). J Appl Phycol 29:1–9
Lv T, He Q, Hong Y et al (2019) Effects of water quality adjusted by submerged macrophytes on the richness of the epiphytic algal community. Front Plant Sci 9:1–8. https://doi.org/10.3389/fpls.2018.01980
Lv T, Fan S, Wang H et al (2022) Invasion of water hyacinth and water lettuce inhibits the abundance of epiphytic algae. Divers Distrib 28:1650–1662. https://doi.org/10.1111/ddi.13527
Lv T, Guan X, Fan S et al (2022) Snail communities increase submerged macrophyte growth by grazing epiphytic algae and phytoplankton in a mesocosm experiment. Ecol Evol 12:e8615. https://doi.org/10.1002/ece3.8615
Mendiburu F (2020) Statistical procedures for agricultural research. 1.3-5 edn. R package
Mohamed ZA, Shehri AMA (2010) Differential responses of epiphytic and planktonic toxic cyanobacteria to allelopathic substances of the submerged macrophyte Stratiotes aloides. Int Rev Hydrobiol 95:224–234. https://doi.org/10.1002/iroh.200911219
Ni GY, Zhao P, Huang QQ et al (2012) Exploring the Novel weapons hypothesis with invasive plant species in China. Allelopathy J 29:199–213
Oksanen J, Blanchet FG, Friendly M et al (2020) Vegan: community ecology package. 2.5-7 edn. R package
Qian K, Liu X, Chen Y (2015) A review on methods of cell enumeration and quantification of freshwater phytoplankton. J Lake Sci 27:767–775
R Development Core Team (2021) R: a language and environment for statistical computing. 4.1.2 edn. R Foundation for Statistical Computing, Vienna
Raven JA, Beardall J, Giordano M (2014) Energy costs of carbon dioxide concentrating mechanisms in aquatic organisms. Photosynth Res 121:111–124. https://doi.org/10.1007/s11120-013-9962-7
Rodusky AJ, Anderson RT (2013) A comparison of epiphytic communities on natural and artificial substrates in a large subtropical lake (Lake Okeechobee, USA). Fundam Appl Limnol 183:189–204
Santos TRD, Ferragut C, Bicudo CEDM (2013) Does macrophyte architecture influence periphyton? Relationships among Utricularia foliosa, periphyton assemblage structure and its nutrient (C, N, P) status. Hydrobiologia 714:71–83. https://doi.org/10.1007/s10750-013-1531-8
Song Y, Wang J, Gao Y (2017) Effects of epiphytic algae on biomass and physiology of Myriophyllum spicatum L. with the increase of nitrogen and phosphorus availability in the water body. Environ Sci Pollut Res Int 24:1–8. https://doi.org/10.1007/s11356-017-8604-6
Souza M, Pellegrini B, Ferragut C (2015) Periphytic algal community structure in relation to seasonal variation and macrophyte richness in a shallow tropical reservoir. Hydrobiologia 1:183–197. https://doi.org/10.1007/s10750-015-2232-2
Svensson JR, Nylund GM, Cervin G et al (2013) Novel chemical weapon of an exotic macroalga inhibits recruitment of native competitors in the invaded range. J Ecol 101:140–148. https://doi.org/10.1111/1365-2745.12028
Tóth VR (2013) The effect of periphyton on the light environment and production of Potamogeton perfoliatus L. in the mesotrophic basin of Lake Balaton. Aquat Sci 75:523–534. https://doi.org/10.1007/s00027-013-0297-4
Vanderstukken M, Declerck SAJ, Decaestecker E et al (2014) Long-term allelopathic control of phytoplankton by the submerged macrophyte Elodea nuttallii. Freshw Biol 59:930–941. https://doi.org/10.1111/fwb.12316
Wang S, Wang J, Li M et al (2013) Six decades of changes in vascular hydrophyte and fish species in three plateau lakes in Yunnan, China. Biodivers Conserv 22:3197–3221. https://doi.org/10.1007/s10531-013-0579-0
Wang H, Wang Q, Bowler P et al (2016) Invasive aquatic plants in China. Aquat Invasions 11:1–9. https://doi.org/10.3391/ai.2016.11.1.01
Wijewardene L, Wu NA, Fohrer N et al (2022) Epiphytic biofilms in freshwater and interactions with macrophytes: current understanding and future directions. Aquat Bot. https://doi.org/10.1016/j.aquabot.2021.103467
Wu X, Wu H, Ye J et al (2015) Study on the release routes of allelochemicals from Pistia stratiotes Linn., and its anti-cyanobacteria mechanisms on Microcystis aeruginosa. Environ Sci Pollut Res 22:18994–19001. https://doi.org/10.1007/s11356-015-5104-4
Xia P, Yan D, Sun R et al (2020) Community composition and correlations between bacteria and algae within epiphytic biofilms on submerged macrophytes in a plateau lake, southwest China. Sci Total Environ. https://doi.org/10.1016/j.scitotenv.2020.138398
Xiong W, Yu D, Wang Q et al (2008) A snail prefers native over exotic freshwater plants: implications for the enemy release hypotheses. Freshw Biol 53:2256–2263. https://doi.org/10.1111/j.1365-2427.2008.02058.x
Xu X, Yang L, Huang X et al (2018) Water brownification may not promote invasions of submerged non-native macrophytes. Hydrobiologia 817:215–225. https://doi.org/10.1007/s10750-017-3387-9
Yang L, He H, Guan B et al (2020) Mesocosm experiment reveals a strong positive effect of snail presence on macrophyte growth, resulting from control of epiphyton and nuisance filamentous algae: implications for shallow lake management. Sci Total Environ 705:1–10. https://doi.org/10.1016/j.scitotenv.2019.135958
Zehnsdorf A, Hussner A, Eismann F et al (2015) Management options of invasive Elodea nuttallii and Elodea canadensis. Limnologica 51:110–117. https://doi.org/10.1016/j.limno.2014.12.010
Zhu X, Dao G, Tao Y et al (2021) A review on control of harmful algal blooms by plant-derived allelochemicals. J Hazard Mater. https://doi.org/10.1016/j.jhazmat.2020.123403
Funding
This study was financially supported by the Major Science and Technology Program for Water Pollution Control and Treatment (2015ZX07503-005) and the Special Foundation of National Science and Technology Basic Research (2013FY112300).
Author information
Authors and Affiliations
Contributions
Conceptualization: TL, CL; Methodology: TL; Investigation: TL, HW, QW, DL, CG, XL; Data analysis, data interpretation, preparation of figures and tables: TL; Writing—review and editing: TL, CL; Revision: TL, CL, TZ; Supervision: TL; Funding acquisition: CL.
Corresponding author
Ethics declarations
Conflict of interest
The authors have no relevant financial or non-financial interests to disclose.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
The original online version of this article was revised due to the author's name Qiuyue Wang was incorrectly written as Qiuye Wang.
Supplementary Information
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Lv, T., Wang, H., Wang, Q. et al. Invasive submerged plant has a stronger inhibitory effect on epiphytic algae than native plant. Biol Invasions 26, 1001–1014 (2024). https://doi.org/10.1007/s10530-023-03225-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10530-023-03225-x