Abstract
In shallow eutrophic lakes, submersed macrophytes are significantly influenced by two main factors: light availability and benthic fish disturbance. Plant foraging is one of the most crucial aspects of plant behavior. The present study was carried out to effects of light regimes and fish disturbance on the foraging behavior of Vallisneria natans in heterogeneous sediments. V. natans was cultivated in heterogeneous sediments with four treatments: high-light regime (H), high-light regime with benthic fish (HF), low-light regime (L), and low-light regime with benthic fish (LF). We use plant trait network analysis to evaluate the relationships between traits in heterogeneous sediments. We found the plant foraging intensity was positively correlated with trait network modularity. The biomass of stem, maternal plant biomass ratio, and ramet number were the hub traits of plant growing in heterogeneous habitats. Although the plant relative growth rate (RGR) was positively correlated with foraging intensity, the hub traits had closer links with plant RGR than foraging intensity. Light regime and benthic fish indirectly affected the plant foraging intensity by changing the chlorophyll a content and pH of overlying water. Overall, our analysis provides valuable insights into plant foraging behavior in response to environmental changes.
Similar content being viewed by others
Data availability
The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.
References
Alon U (2003) Biological networks: the tinkerer as an engineer. Science 301:1866–1867
APHA (1999) Standard methods for the examination of water and wastewater, 20th edn. American Public Health Association, Washington DC
Badiou PHJ, Goldsborough LG (2015) Ecological impacts of an exotic benthivorous fish, the common carp (Cyprinus carpio L.), on water quality, sedimentation, and submerged macrophyte biomass in wetland mesocosms. Hydrobiologia 755:107–121
Bakker ES, Wood KA, Pagès J, Veen G, Hilt S (2016) Herbivory on freshwater and marine macrophytes: a review and perspective. Aquat Bot 135:18–36
Bentler PM, Bonett DG (1980) Significance tests and goodness of fit in the analysis of covariance structure. Psychol Bull 88:588–606
Cahill JF, McNickle GG (2011) The behavioral ecology of nutrient foraging by plants. Annu Rev Ecol Evol Syst 42:289–311
Cao TE, Leyi NI, Xie P, Jun XU, Zhang M (2011) Effects of moderate ammonium enrichment on three submersed macrophytes under contrasting light availability. Freshw Biol 56:1620–1629
Chambers PA, Jacob K (1987) Light and nutrients in the control of aquatic plant community structure. I. In situ experiments. J Ecol 75:621–628
Chen J, Chou Q, Ren W, Su H, Zhang M, Cao T, Zhu T, Ni L, Liu Z, Xie P (2022) Growth, morphology and C/N metabolism responses of a model submersed macrophyte, Vallisneria natans, to various light regimes. Ecol Indic 136:108652
Chen J, Hu X, Cao T, Zhang X, Xi Y, Wen X, Su H, de Silva W, Zhu T, Ni L, Xie P (2017) Root-foraging behavior ensures the integrated growth of Vallisneria natans in heterogeneous sediments. Environ Sci Pollut Res 24:8108–8119
Chen J, Liu Z, Xiao S, Chen R, Luo C, Zhu T, Cao T, Ni L, Xie P, Su H, Zhang M (2020a) Effects of benthivorous fish disturbance on chlorophyll a contents in water and the growth of two submersed macrophytes with different growth forms under two light regimes. Sci Total Environ 704:132569
Chen J, Su H, Zhou G, Dai Y, Hu J, Zhao Y, Liu Z, Cao T, Ni L, Zhang M, Xie P (2020b) Effects of benthivorous fish disturbance and snail herbivory on water quality and two submersed macrophytes. Sci Total Environ 713:136734
Clauset A, Mej N, Moore C (2004) Finding community structure in very large networks. Phys Rev 70:6
Falkowski PG, Raven JA (2007) Aquatic photosynthesis, 2nd edn. Princeton University Press, p 484
Fernández-Zamudio R, García-Murillo P, Díaz-Paniagua C (2016) Aquatic plant distribution is driven by physical and chemical variables and hydroperiod in a Mediterranean temporary pond network. Hydrobiologia 774:123–135
Flores-Moreno H, Fazayeli F, Banerjee A, Datta A, Kattge J, Butler EE (2019) Robustness of trait connections across environmental gradients and growth forms. Glob Ecol Biogeogr 28:1806–1826
Gameiro C, Zwolinski J, Brotas V (2011) Light control on phytoplankton production in a shallow and turbid estuarine system. Hydrobiologia 669:249–263
Gilarranz LJ, Rayfield B, Linan-Cembrano G, Bascompte J, Gonzalez A (2017) Effects of network modularity on the spread of perturbation impact in experimental metapopulations. Science 357:199–201
Grime JP, Mackey J (2002) The role of plasticity in resource capture by plants. Evol Ecol 16:299–307
He N, Li Y, Liu C, Xu L, Li M, Zhang J, He J, Tang Z, Han X, Ye Q (2020) Plant trait networks: improved resolution of the dimensionality of adaptation — ScienceDirect. Trends Ecol Evol 35:908–918
Holloway GJ (2002) Phenotypic plasticity: beyond nature and nurture. Heredity 89:410
Huber H, Chen X, Hendriks M, Keijsers D, Voesenek L, Pierik R, Poorter H, Kroon HD, Visser E (2012) Plasticity as a plastic response: how submergence-induced leaf elongation in Rumex palustris depends on light and nutrient availability in its early life stage. New Phytol 194:572–582
Hutchings M, de Kroon H (1994) Foraging in plants: the role of morphological plasticity in resource acquisition. Adv Ecol Res 25:159–238
Hutchings MJ, Wijesinghe DK (1997) Patchy habitats, division of labour and growth dividends in clonal plants. Trends Ecol Evol 12:390–394
Ikegami M, Hal SV, Rheenen JWAV, Whigham DF, Werger MJA (2008) Spatial division of labour of Schoenoplectus americanus. Plant Ecol 199:55–64
Jeppesen E, Sondergaard M, Sondergaard M, Christoffersen K (1998) The structuring role of submerged macrophytes in lakes: II Interactions between grazing birds and macrophytes. Ecol Stud 131:175–196
Kembel S, Cahill J (2005) Plant phenotypic plasticity belowground: a phylogenetic perspective on root foraging trade-offs. Am Nat 166:216–230
Kleyer M, Trinogga J, Piqueras MC, Blasius B (2019) Trait correlation network analysis identifies biomass allocation traits and stem specific length as hub traits in herbaceous perennial plants. J Ecol 107:829–842
Kroon HD, Stuefer JF, Ming D, During HJ (1994) On plastic and non-plastic variation in clonal plant morphology and its ecological significance. Folia Geobot 29:123–138
Li L, Mccormack ML, Ma CG, Kong DL, Zhang Q, Chen XY, Zeng H, Niinemets U, Guo DL (2015) Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests. Ecol Lett 18:899–906
Li Y, Liu C, Sack L, Xu L, Li M, Zhang J, He N, Penuelas J (2022) Leaf trait network architecture shifts with species-richness and climate across forests at continental scale. Ecol Lett 25:1442–1457
Li Z (2016) Current situation of Misgurnus anguillicaudatus culture industry in Hebei province and suggestions for its development. Hebei Fisheries 12:45–47
Liang SC, Zhang SM, Fei-Hai YU, Dong M (2007) Small-scale spatial cross-correlation between ramet population variables of Potentilla reptans Var. sericophylla and soil available phosphorus. J Plant Ecol 31:613–618
Matesanz S, Blanco-Sánchez M, Ramos-Muoz M, Cruz MDL, Benavides R, Escudero A (2021) Phenotypic integration does not constrain phenotypic plasticity: differential plasticity of traits is associated to their integration across environments. New Phytol 231:2359–2370
Rao Q, Chen J, Chou Q, Ren W, Cao T, Zhang M, Xiao H, Liu Z, Chen J, Haojie S, Xie P (2023) Linking trait network parameters with plant growth across light gradients and seasons. Funct Ecol. https://doi.org/10.1111/1365-2435.14327
Rao Q, Su H, Ruan L, Deng X, Xie P (2021) Stoichiometric and physiological mechanisms that link hub traits of submerged macrophytes with ecosystem structure and functioning. Water Res 202:117392
Reich PB (2014) The world-wide ‘fast-slow’ plant economics spectrum: a traits manifesto. (Special Feature: The tree of life in ecosystems: evolution of plant effects on carbon and nutrient cycling.). J Ecol 102:275–301
Ren W, Wen Z, Cao Y, Wang H, Yuan C, Zhang X, Ni L, Xie P, Cao T, Li K, Jeppesen E (2022) Cascading effects of benthic fish impede reinstatement of clear water conditions in lakes: a mesocosm study. J Environ Manage 301:113898
Song Y, He XJ, Chen M, Zhang LL, Li J, Deng Y (2018) Effects of pH on the submerged macrophyte Hydrilla verticillata. Russ J Plant Physiol 65:611–619
Su H, Wu Y, Xie P, Chen J, Cao T, Xia W (2016) Effects of taxonomy, sediment, and water column on C:N:P stoichiometry of submerged macrophytes in Yangtze floodplain shallow lakes, China. Environ Sci Pollut Res 23:22577–22585
Su H, Zheng W, Li M, Wang C, Fu G, Le R, Sun G (2023) Effects of benthic fish and light regimes on water quality and the growth of Vallisneria natans with two sediment types. Environ Sci Pollut Res Int 30:74560–73569
Thomas SM, Melles SJ, Mackereth RW, Tunney TD, Johnston TA (2020) Climate and landscape conditions indirectly affect fish mercury levels by altering lake water chemistry and fish size. Environ Res 188:109750
Tuna S (1967) Determination of chlorophyll and pheo-pigments: spectrophotometric equations. Limnol Oceanogr 12:343–346
Wang T, Li X, Liu C-H, Yu D (2016) The compromising foraging of a clonal submerged plant in variable environments of substrate type and light condition: a simulation study. J Plant Ecol 10:538–545
Wang Z, van Kleunen M, During HJ, Werger MJ (2013) Root foraging increases performance of the clonal plant Potentilla reptans in heterogeneous nutrient environments. PloS One 8:e58602
Xiao K, Dan YU, Wang J (2006) Habitat selection in spatially heterogeneous environments: a test of foraging behaviour in the clonal submerged macrophyte Vallisneria spiralis. Freshw Biol 51:1552–1559
Xie D, Yu D, You WH, Wang LG (2013) Morphological and physiological responses to sediment nutrients in the submerged macrophyte Myriophyllum spicatum. Wetlands 33:1095–1102
Xing W, Wu HP, Hao BB, Liu GH (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
Yang L, Sun G, Pan X, Fang Y, Chen B, Hu P (2011) Response of paddy soil nutrients to bioturbation of Misgurnus anguillicaudatus. J Anhui Agric Sci 39:3884–3885
Zhang R, Ma B, Yang Z, Ying Z, Su L, Ping Y, Liu H (2016) Research advances and application situation of Vallisneria in water environmental restoration. Chinese Agri Sci Bull 32:144–154
Zhang T, Li Z (2007) Fish resources and fishery utilization of Lake Poyang. J Lake Sci 19:434–444
Zhong J, Yi S, Yu Y, Huang S, Shen Y, Guo Q, Wang W (2015) Investigation of Misgurnus anguillicaudatus and Paramisgurnus dabryanus in the Yangtze River basin. J Fisheries of China 39:1089–1098
Zhu T, Jiang W, Shen H, Yuan J, Chen J, Gong Z, Wang L, Zhang M, Rao Q (2023) Characteristics of plant trait network and its influencing factors in impounded lakes and channel rivers of South-to-North Water Transfer Project, China. Front Plant Sci 14:1127209
Zimmermann TG, Andrade ACS, Richardson DM (2016) Experimental assessment of factors mediating the naturalization of a globally invasive tree on sandy coastal plains: a case study from Brazil. AoB Plants 8:plw042
Funding
This study was supported by the National Science of Foundation of Fujian Province (Grant No. 2020J01383), the National Natural Science Foundation of China (Grant No. 32101406), the Education Department of Fujian Province/Sanming University (JAT190716/B201929), and the Sanming University Scientific Research Foundation for High-level Talent (19YG17, 18YG01, 18YG02).
Author information
Authors and Affiliations
Contributions
All authors contributed to the study conception and design. Material preparation was performed by Guanbao Fu and Ruijie Le and data collection and analysis were performed by Mingfan Li and Chao Wang. The first draft of the manuscript was written by Hong Su and Gang Sun and all authors commented on previous versions of the manuscript. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Ethical approval
Not applicable.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Thomas Hein
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary information
ESM 1
(DOCX 66 kb)
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
Su, H., Li, M., Wang, C. et al. Effects of light regimes and benthic fish disturbance on the foraging behavior of Vallisneria natans in heterogeneous sediments. Environ Sci Pollut Res 31, 331–342 (2024). https://doi.org/10.1007/s11356-023-31196-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-31196-y