Abstract
Little is known about how community composition affects vertical patterns of leaf characteristics for submerged macrophytes in freshwater lakes. Here, after sampling Hydrilla verticillata in both single and mixed communities in shallow and deep areas in a shallow lake, we measured vertical patterns of leaf biofilm and physiology characteristics. Upper leaves of H. verticillata always had more attached abiotic biofilm matters, and all biofilm characteristics exhibited declining trends from top to bottom segments in deep areas. Moreover, the amount of attached biofilm matter in the mixed community was less than in the single community in shallow areas, but the reverse was true in deep areas. The vertical pattern of leaf physiology characteristics was obvious in the mixed community. In the shallow area, leaf pigment concentrations showed increasing trends with an increasing water depth, but the enzymatic specific activity of peroxidase (POD-ESA) was precisely the opposite. In the deep area, leaf chlorophyll concentrations were greatest in the leaves of bottom segments and lowest in top segments, while carotenoids and POD-ESA were greatest in the leaves of the middle segment-II. Light intensity and biofilm were found to play an important role in regulating the vertical patterns of photosynthetic pigments and POD-ESA. Our study highlighted the effect of community composition on the vertical pattern of leaf physiology and biofilm characteristics.
Highlights
Biofilm characteristics always showed increasing trends with increasing water depth.
Community composition changed the amount of attached biofilm matter.
The vertical pattern of leaf physiology was more obvious in mixed communities.
Light intensity and biofilm regulated the vertical pattern of leaf physiology.
Similar content being viewed by others
Data availability
The availability of data and materials on the base of personal request.
References
Alahuhta J, Kanninen A, Hellsten S, Vuori K-M, Kuoppala M, Hämäläinen H (2013) Variable response of functional macrophyte groups to lake characteristics, land use, and space: implications for bioassessment. Hydrobiologia 737:201–214. https://doi.org/10.1007/s10750-013-1722-3
Asaeda T, Sultana M, Manatunge J, Fujino T (2004) The effect of epiphytic algae on the growth and production of Potamogeton perfoliatus L. in two light conditions. Environ Exp Bot 52:225–238. https://doi.org/10.1016/j.envexpbot.2004.02.001
Bernhardt-Römermann M et al (2011) Functional traits and local environment predict vegetation responses to disturbance: a pan-European multi-site experiment. J Ecol 99:777–787. https://doi.org/10.1111/j.1365-2745.2011.01794.x
Bornette G, Puijalon S (2010) Response of aquatic plants to abiotic factors: a review. Aquat Sci 73:1–14. https://doi.org/10.1007/s00027-010-0162-7
Cao Y, Chen D, Ji X, Zhang S, Huang Q, Wang W (2019) Effects of water depth gradient on physiological characteristics of Vallisneria natans. J Freshw Ecol 34:405–417. https://doi.org/10.1080/02705060.2019.1592029
Chambers PA, Prepas EE (1990) Competition and coexistence in submerged aquatic plant communities: the effects of species interactions versus abiotic factors. Freshw Biol 23:541–550
Chmara R, Szmeja J, Banaś K (2018) The relationships between structural and functional diversity within and among macrophyte communities in lakes. J Limnol 77:100–108. https://doi.org/10.4081/jlimnol.2017.1630
Ding M, Zhou R, Chen T, He L, Jeppesen E, Li L (2020) Physiological adaptations of the submerged macrophyte Vallisneria spinulosa in response to water level fluctuations. Aquat Ecol 55:33–45. https://doi.org/10.1007/s10452-020-09808-3
Dong B, Han R, Wang G, Cao X (2014) O2, pH, and redox potential microprofiles around Potamogeton malaianus measured using microsensors. Plos One 9:e101825. https://doi.org/10.1371/journal.pone.0101825
Dong B, Qin B, Li W, Gao G (2016) Growth and community composition of submerged macrophytes in Lake Taihu (China): assessment of changes in response to sediment characteristics. Wetlands 37:233–243. https://doi.org/10.1007/s13157-016-0861-5
Guan J, Jacoby CA, Frazer TK (2020) Light attenuation by periphyton on Vallisneria americana. Ecol Ind 116:106498. https://doi.org/10.1016/j.ecolind.2020.106498
Hao B, Wu H, Li W, Xing W (2020) Periphytic algae mediate interactions between neighbor and target submerged macrophytes along a nutrient gradient. Ecol Ind 110:105898. https://doi.org/10.1016/j.ecolind.2019.105898
Lalonde S, Downing JA (1991) Epiphyton biomass is related to lake trophic status, depth, and macrophyte architecture. Can J Fish Aquat Sci 48:2285–2291. https://doi.org/10.1139/f91-268
Li D, Zhang S, Adyel TM, Liu K, Gong L (2020) Negative effects on the leaves of submerged macrophyte and associated biofilms growth at high nitrate induced-stress. Aquatic Toxicol 226:105559. https://doi.org/10.1016/j.aquatox.2020.105559
Li W, Fu H, Cao T, Zhang X, Zhong J, Ni L, Xie P, Fan H (2017): Distribution and carbon, nitrogen and phosphorus stoichiometric characteristics of submersed macrophytes in Lake Fuxian. J Lake Sci 29, 448–457 [in chinese]. https://doi.org/10.18307/2017.0221
Li X, Chu Q, Tang N, AbduroOgo H, Xing W (2022) Functional trait-based potential invasiveness of exotic submerged macrophytes and their effects on sediment bacterial community. Hydrobiologia 849:3061–3077. https://doi.org/10.1007/s10750-022-04914-9
Liu H, Liu G, Xing W (2021) Functional traits of submerged macrophytes in eutrophic shallow lakes affect their ecological functions. Sci Total Environ 760:143332. https://doi.org/10.1016/j.scitotenv.2020.143332
Ma F, Zuo Z, Yang L, Li D, Wang H, Li F, Fan S, Liu C, Yu D (2022) The effect of trait-based diversity on productivity results mainly from intraspecific trait variability in the macrophyte community. Freshw Biol 67:1137–1149. https://doi.org/10.1111/fwb.13906
McCreary NJ (1991) Competition as a mechanism of submersed macrophyte community structure. Aquat Bot 41:177–193. https://doi.org/10.1016/0304-3770(91)90043-5
Pan Y, Cieraad E, Armstrong J, Armstrong W, Clarkson BR, Colmer TD, Pedersen O, Visser EJW, Voesenek LACJ, van Bodegom PM (2020) Global patterns of the leaf economics spectrum in wetlands. Nature Commun 11:4519. https://doi.org/10.1038/s41467-020-18354-3
Petruzzella A, Leeuwen CHA, Donk E, Bakker ES, Catford J (2020) Direct and indirect effects of native plants and herbivores on biotic resistance to alien aquatic plant invasions. J Ecol 108:1487–1496. https://doi.org/10.1111/1365-2745.13380
Pizarro H, Vinocur A, Tell G (2002) Periphyton on artificial substrata from three lakes of different trophic status at Hope Bay (Antarctica). Polar Biol 25:169–179. https://doi.org/10.1007/s003000100323
R Development Core Team (2020) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Rao Q, Su H, Deng X, Xia W, Wang L, Cui W, Ruan L, Chen J, Xie P (2020) Carbon, nitrogen, and phosphorus allocation strategy among organs in submerged macrophytes is altered by eutrophication. Front Plant Sci 11:524450. https://doi.org/10.3389/fpls.2020.524450
Reitsema RE, Wolters J-W, Preiner S, Meire P, Hein T, De Boeck G, Blust R, Schoelynck J (2020) Response of submerged macrophyte growth, morphology, chlorophyll content and nutrient stoichiometry to increased flow velocity and elevated CO2 and dissolved organic carbon concentrations. Front Environ Sci 11:527801. https://doi.org/10.3389/fenvs.2020.527801
Sand-Jensen K, Revsbech NP, Jorgensen BB (1985) Microprofiles of oxygen in epiphyte communities on submerged macrophytes. Mar Biol 89:55–62. https://doi.org/10.1007/BF00392877
Sultana M, Asaeda T, Ekram Azim M, Fujino T (2009) Morphological responses of a submerged macrophyte to epiphyton. Aquat Ecol 44:73–81. https://doi.org/10.1007/s10452-009-9291-2
Titus JE, Stephens MD (1983) Neighbor influences and seasonal growth patterns for Vallisneria americana in a mesotrophic lake. Oecologia 56, 23–29. https://www.jstor.org/stable/4216856
Vilas MP, Marti CL, Adams MP, Oldham CE, Hipsey MR (2017) Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: a proposed feedback mechanism of macrophyte loss. Front Plant Sci 8:2097. https://doi.org/10.3389/fpls.2017.02097
Vis C, Hudon C, Carignan R (2006) Influence of the vertical structure of macrophyte stands on epiphyte community metabolism. Can J Fish Aquat Sci 63:1014–1026. https://doi.org/10.1139/f06-021
Wang J, Yu D, Xiong W, Han Y (2008) Above- and belowground competition between two submersed macrophytes. Hydrobiologia 607:113–122. https://doi.org/10.1007/s10750-008-9371-7
Wang L, Wang X, Han X, Gao Y, Liu B, Zhang X, Wang G (2021a) Potamogeton crispus responses to varying water depth in morphological plasticity and physiological traits. Environ Sci Pollut Res 28:4253–4261. https://doi.org/10.1007/s11356-020-10806-z
Wang M, Liu Z, Luo F, Lei G, Li H (2016) Do amplitudes of water level fluctuations affect the growth and community structure of submerged macrophytes? Plos One 11:e0146528. https://doi.org/10.1371/journal.pone.0146528
Wang Y, Jiang W, Cheng Y, Li D, Zhang Z, Zhang X, Wang G (2021b) Vertical patterns of leaf physiology and biofilm characteristics for submerged macrophytes in a shallow subtropical lake. Mar Freshw Res 72:1233–1242. https://doi.org/10.1071/mf20350
Wang Y, Xu X, Li D, Lu Y, Zhang X, Yang C, Jin Q, Wang G (2023) Effect of light and nutrients on interspecific interactions between submerged macrophytes: Implications for restoration of multispecies aquatic vegetation in eutrophic lakes. J Oceanol Limnol. https://doi.org/10.1007/s00343-022-2230-y
Xing W, Wu H, Hao B, Liu G (2013) Stoichiometric characteristics and responses of submerged macrophytes to eutrophication in lakes along the middle and lower reaches of the Yangtze River. Ecol Eng 54:16–21. https://doi.org/10.1016/j.ecoleng.2013.01.026
Yang C, Shi X, Nan J, Huang Q, Shen X, Li J (2022) Morphological responses of the submerged macrophyte Vallisneria natans along an underwater light gradient: A mesocosm experiment reveals the importance of the Secchi depth to water depth ratio. Sci Total Environ 808:152199. https://doi.org/10.1016/j.scitotenv.2021.152199
Yu Q, Wang H, Xu C, Li Y, Ma S, Liang X, Jeppesen E, Wang H (2018) Higher tolerance of canopy-forming potamogeton crispus than rosette-forming vallisneria natans to high nitrogen concentration as evidenced from experiments in 10 ponds With contrasting nitrogen levels. Front Plant Sci 9:1845. https://doi.org/10.3389/fpls.2018.01845
Zhang C, Pei H, Lu C, Liu C, Wang W, Zhang X, Liu P, Lei G (2022) Indirect herbivore biomanipulation may halt regime shift from clear to turbid after macrophyte restoration. Environ Pollut 313:120242. https://doi.org/10.1016/j.envpol.2022.120242
Zhang C, Pei H, Lu C, Liu P, Liu C, Lei G (2022b) Eutrophication drives regime shift via changes in stoichiometric homeostasis-based submerged macrophyte assemblages. NPJ Clean Water 5. https://doi.org/10.1038/s41545-022-00161-6
Zhang M, Cao T, Ni L, Xie P, Li Z (2010) Carbon, nitrogen and antioxidant enzyme responses of Potamogeton crispus to both low light and high nutrient stresses. Environ Exp Bot 68:44–50. https://doi.org/10.1016/j.envexpbot.2009.09.003
Zhang X, Liu X, Ding Q (2012) Morphological responses to water-level fluctuations of two submerged macrophytes, Myriophyllum spicatum and Hydrilla verticillata. J Plant Ecol 6:64–70. https://doi.org/10.1093/jpe/rts009
Zhu G, Li W, Zhang M, Ni L, Wang S (2012) Adaptation of submerged macrophytes to both water depth and flood intensity as revealed by their mechanical resistance. Hydrobiologia 696:77–93. https://doi.org/10.1007/s10750-012-1185-y
Funding
This work was supported by the National Key Research and Development Program (2022YFC3204302), the National Natural Science Foundation of China (41971043), the Major Science and Technology Program for the Water Pollution Control and Treatment (2017ZX07203-003), the Cooperation and Guidance Project of Prospering Inner Mongolia through Science and Technology (2021CG0037), and the Research Fund of Nanjing Hydraulic Research Institute (Y221011).
Author information
Authors and Affiliations
Contributions
The manuscript was reviewed and approved for publication by all authors. ZXH and LYJ conceived and designed the experiments. WYP, XXG, ZSY, and GZM performed the experiments. WYP, XXG, ZSY, YQ, and ZLQ analyzed the data. WYP wrote the paper. ZXH, LYJ, and WGX reviewed and revised the paper.
Corresponding author
Ethics declarations
Ethical approval
The manuscript was reviewed and ethically approved for publication by all authors.
Consent to participate
The manuscript was reviewed, and all authors consent to participate.
Consent for publication
The manuscript was reviewed, and all authors consent to publish.
Conflict of interest
The authors declare no competing interests.
Additional information
Responsible Editor: Gangrong Shi
Publisher's note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
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
Wang, Y., Xu, X., Zhang, S. et al. Vertical patterns of leaf physiology and biofilm characteristics for Hydrilla verticillata in both single and mixed communities. Environ Sci Pollut Res 30, 59802–59812 (2023). https://doi.org/10.1007/s11356-023-26473-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-26473-9