Skip to main content
SpringerLink
Log in

Sediment nutrient drivers of the growth dynamics of the rare fern Marsilea quadrifolia

  • Primary Research Paper
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

In analysing the global decline of macrophytes, a scant attention was generally paid to the direct relations of rooted aquatic plants with sediment eutrophication. Nevertheless, the sediment is a pivotal driver of macrophyte dynamics. In order to add new data about aquatic plant–sediment interactions, a microcosm experiment was performed to gain knowledge on the growth dynamics of the rare aquatic fern Marsilea quadrifolia L. Healthy shoots of M. quadrifolia were grown under an increasing availability of nutrients (N and P) and reducing sediment conditions for a total incubation time of 42 days. The variation in biomass and number of fronds and knots was monitored regularly at intervals of 10–11 days. The results confirm the pivotal role of sediment in driving the growth of M. quadrifolia, which responds rapidly to the increase in nutrient availability up to a moderate excess. M. quadrifolia seems to be a slightly eutrophic-rooted aquatic species, able to tolerate pore-water concentrations up to ~450 and 4 μM of NH4 + and PO4 3−, respectively. The present data corroborate the need to consider the short-term dynamics when analysing plant adaptations to sediment eutrophication, as well as a physical and chemical characterization of sediments to evaluate their potential bioreceptivity.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Aspila, K. I., H. Agemian & A. S. Y. Chau, 1976. A semi-automated method for the determination of inorganic, organic and total phosphate in sediments. Analyst 101: 187–197.

    Article  CAS  PubMed  Google Scholar 

  • Bakker, E. S., J. M. Sarneel, R. D. Gulati, Z. Liu & E. van Donk, 2013. Restoring macrophyte diversity in shallow temperate lakes: biotic versus abiotic constraints. Hydrobiologia 710: 23–37.

    Article  Google Scholar 

  • Barko, J. W. & R. M. Smart, 1986. Sediment-related mechanisms of growth limitation in submerged macrophytes. Ecology 65: 1328–1340.

    Article  Google Scholar 

  • Bolpagni, R. & A. Piotti, 2015a. Hydro-hygrophilous vegetation diversity and distribution patterns in riverine wetlands in an agricultural landscape: a case study from the Oglio River (Po Plain, Northern Italy). Phytocoenologia 45: 69–84.

    Article  Google Scholar 

  • Bolpagni, R. & A. Piotti, 2015b. The importance of being natural in a human-altered riverscape: Role of wetland type in supporting habitat heterogeneity and the functional diversity of vegetation. Aquatic Conservation: Marine and Freshwater Ecosystems. doi:10.1002/aqc.2604.

    Google Scholar 

  • Bolpagni, R., M. Bartoli & P. Viaroli, 2013. Species and functional plant diversity in a heavily impacted riverscape: implications for threatened hydro-hygrophilous flora conservation. Limnologica 43: 230–238.

    Article  Google Scholar 

  • Bolpagni, R., A. Laini, E. Soana, M. Tomaselli & J. Nascimbene, 2015. Growth performance of Vallisneria spiralis under oligotrophic conditions supports its potential invasiveness in mid-elevation freshwaters. Weed Research 55: 185–194.

    Article  Google Scholar 

  • Bornette, G. & S. Puijalon, 2011. Response of aquatic plants to abiotic factors: a review. Aquatic Sciences 73: 1–14.

    Article  CAS  Google Scholar 

  • Boustany, R. G., T. C. Michot & R. F. Moss, 2010. Effects of salinity and light on biomass and growth of Vallisneria americana from Lower St. Johns River, FL, USA. Wetlands Ecology and Management 18: 203–217.

    Article  CAS  Google Scholar 

  • Bower, C. F. & T. T. Holm-Hansen, 1980. A salicylate-hypochlorite method for determining ammonia in seawater. Canadian Journal of Fisheries and Aquatic Sciences 37: 794–798.

    Article  CAS  Google Scholar 

  • Brouwer, E. & J. G. M. Roelofs, 2001. Degraded softwater lakes: possibilities for restoration. Restoration Ecology 9: 155–166.

    Article  Google Scholar 

  • Bruni, I., R. Gentili, F. De Mattia, P. Cortis, G. Rossi & M. Labra, 2013. A multi-level analysis to evaluate the extinction risk of and conservation strategy for the aquatic fern Marsilea quadrifolia L. in Europe. Aquatic Botany 111: 35–42.

    Article  Google Scholar 

  • Cai, X., L. Yao, G. Gao, Y. Xie, J. Yang, X. Tang & M. Zhang, 2016. Responses in root physiological characteristics of Vallisneria natans (Hydrocharitaceae) to increasing nutrient loadings. Knowledge and Management of Aquatic Ecosystems 417: 4.

    Article  Google Scholar 

  • Drava, G., E. Roccotiello, V. Minganti, A. Manfredi & L. Cornara, 2012. Effects of cadmium and arsenic on Pteris vittata under hydroponic conditions. Environmental Toxicology and Chemistry 31: 1375–1380.

    Article  CAS  PubMed  Google Scholar 

  • Gulati, R. D., L. M. D. Pires & E. van Donk, 2008. Lake restoration studies: Failures, bottlenecks and prospects of new eco-technological measures. Limnologica 38: 233–247.

    Article  CAS  Google Scholar 

  • Guillitte, O., 1995. Bioreceptivity: a new concept for building ecology studies. Science of the Total Environment 167: 215–220.

    Article  CAS  Google Scholar 

  • Hodge, A., 2004. The plastic plant: root responses to heterogeneous supplies of nutrients. New Phytologist 16: 24–29.

    Google Scholar 

  • Hoffmann, M., U. Reader & A. Melzer, 2015. Influence of environmental conditions on the regenerative capacity and the survivability of Elodea nuttallii fragments. Journal of Limnology 74: 12–20.

    Google Scholar 

  • Husák, S. & H. Oťaheľová, 1986. Contribution to the ecology of Marsilea quadrifolia L. Folia Geobotanica et Phytotaxonomica 21: 86–89.

    Article  Google Scholar 

  • Hussner, A., T. Mettler-Altmann, A. P. M. Weber & K. Sand-Jensen, 2016. Acclimation of photosynthesis to supersaturated CO2 in aquatic plant bicarbonate users. Freshwater Biology. doi:10.1111/fwb.12812.

    Google Scholar 

  • Lenth, R., 2015. lsmeans: least-squares means. R package version 2.20-23. http://CRAN.R-project.org/package=lsmeans.

  • Keruzoré, A. A., N. J. Willby & D. J. Gilvear, 2013. The role of lateral connectivity in the maintenance of macrophyte diversity and production in large rivers. Aquatic Conservation: Marine and Freshwater Ecosystems 23: 301–315.

    Article  Google Scholar 

  • Kozlowski, G. & S. Vallelian, 2009. Eutrophication and endangered aquatic plants: An experimental study on Baldellia ranunculoides (L.) parl. (Alismataceae). Hydrobiologia 635: 181–187.

    Article  CAS  Google Scholar 

  • Mascaró, O., T. Valdemarsen, M. Holmer, M. Pérez & J. Romero, 2009. Experimental manipulation of sediment organic content and water column aeration reduces Zostera marina (eelgrass) growth and survival. Journal of Experimental Marine Biology and Ecology 373: 26–34.

    Article  Google Scholar 

  • Nienhuis, P. H., J. P. Bakker, A. P. Grootjans, R. D. Gulati & V. N. De Jonge, 2002. The state of the art of aquatic and semi-aquatic ecological restoration projects in the Netherlands. Hydrobiologia 478: 219–233.

    Article  Google Scholar 

  • Pierobon, E., R. Bolpagni, M. Bartoli & P. Viaroli, 2010. Net primary production and seasonal CO2 and CH4 fluxes in a Trapa natans L. meadow. Journal of Limnology 69: 225–234.

    Article  Google Scholar 

  • Pinardi, M., M. Bartoli, D. Longhi, U. Marzocchi, A. Laini, C. Ribaudo & P. Viaroli, 2009. Benthic metabolism and denitrification in a river reach: a comparison between vegetated and bare sediments. Journal of Limnology 68: 133–145.

    Article  Google Scholar 

  • Pinheiro, J., D. Bates, S. DebRoy, D. Sarkar & R Core Team, 2016. Nlme: linear and nonlinear mixed effects models. R package version 3.1-126, http://CRAN.R-project.org/package=nlme.

  • Pulido, C., E. C. H. E. T. Lucassen, O. Pedersen & J. G. M. Roelofs, 2011. Influence of quantity and lability of sediment organic matter on the biomass of two isoetids, Littorella uniflora and Echinodorus repens. Freshwater Biology 56: 939–951.

    Article  Google Scholar 

  • Pulido, C., J. L. Riera, E. Ballestreros, E. Chappuis & E. Gacia, 2015. Predicting aquatic macrophyte occurrence in soft-water oligotrophic lakes (Pyrenees mountain range). Journal of Limnology 74: 143–154.

    Google Scholar 

  • R Development Core Team, 2015. A language and environment for statistical computing. R Foundation for Statistical Computing, Wien.

    Google Scholar 

  • Raun, A. L., J. Borum & K. Sand-Jensen, 2010. Influence of sediment organic enrichment and water alkalinity on growth of aquatic isoetid and elodeid plants. Freshwater Biology 55: 1891–1904.

    Article  Google Scholar 

  • Ribaudo, C., M. Bartoli, E. Racchetti, D. Longhi & P. Viaroli, 2011. Seasonal fluxes of O2, DIC and CH4 in sediments with Vallisneria spiralis: indications for radial oxygen loss. Aquatic Botany 94: 134–142.

    Article  CAS  Google Scholar 

  • Sand-Jensen, K., 1997. Macrophytes as biological engineers in the ecology of Danish streams. In Sand-Jensen, K. & O. Pedersen (eds), Freshwater biology: priorities and development in Danish research. Gad Publisher, København: 74–101.

    Google Scholar 

  • Sand-Jensen, K. & C. L. Møller, 2015. Reduced root anchorage of freshwater plants in sandy sediments enriched with fine organic matter. Freshwater Biology 59: 427–437.

    Article  Google Scholar 

  • Sand-Jensen, K., C. Prahl & H. Stokholm, 1982. Oxygen release from roots of submerged aquatic macrophytes. Oikos 38: 349–354.

    Article  Google Scholar 

  • Sand-Jensen, K., C. L. Møller & J. Borum, 2015. High resistance of oligotrophic isoetid plants to oxic and anoxic dark exposure. Freshwater Biology 60: 1044–1051.

    Article  CAS  Google Scholar 

  • Scheffer, M., S. Szabo, A. Gragnani, E. H. Van Nees, S. Rinaldi, N. Kautsky, J. Norberg, R. M. Roijackers & R. J. Franken, 2003. Floating plant dominance as a stable state. Proceedings of the National Academy of Sciences 100: 4040–4045.

    Article  CAS  Google Scholar 

  • Schneider, B., E. R. Cunha, M. Marchese & S. M. Thomaz, 2015. Explanatory variables associated with diversity and composition of aquatic macrophytes in a large subtropical river floodplain. Aquatic Botany 121: 67–75.

    Article  Google Scholar 

  • Shields, E. C. & K. A. Moore, 2016. Effects of sediment and salinity on the growth and competitive abilities of three submersed macrophytes. Aquatic Botany 132: 24–29.

    Article  CAS  Google Scholar 

  • Silveira, M. J. & S. M. Thomaz, 2015. Growth of a native versus an invasive submerged aquatic macrophyte differs in relation to mud and organic matter concentrations in sediment. Aquatic Botany 124: 85–91.

    Article  Google Scholar 

  • Silveira, M. J., V. C. Harthman, T. S. Michelan & L. A. Souza, 2016. Anatomical development of roots of native and non-native submerged aquatic macrophytes in different sediment types. Aquatic Botany 133: 24–27.

    Article  Google Scholar 

  • Smolders, A. P. J., E. C. H. E. T. Lucassen & J. G. M. Roelofs, 2002. The isoetid environment biogeochemistry and threats. Aquatic Botany 73: 325–350.

    Article  CAS  Google Scholar 

  • Soana, E. 2013. Radial oxygen loss from roots of Vallisneria spiralis L.: biogeochemical implications in eutrophic aquatic ecosystems. Parma: PhD thesis.

  • Soana, E. & M. Bartoli, 2013. Seasonal variation of radial oxygen loss in Vallisneria spiralis L.: an adaptation to sediment redox? Aquatic Botany 104: 228–232.

    Article  Google Scholar 

  • Soana, E. & M. Bartoli, 2014. Seasonal regulation of nitrification in a rooted macrophyte (Vallisneria spiralis L.) meadow under eutrophic conditions. Aquatic Ecology 48: 11–21.

    Article  CAS  Google Scholar 

  • Soana, E., M. Naldi & M. Bartoli, 2012. Effects of increasing organic matter loads on pore-water features of vegetated (Vallisneria spiralis L.) and plant-free sediments. Ecological Engineering 47: 141–145.

    Article  Google Scholar 

  • Søndergaard, M., E. Jeppesen, T. L. Lauridsen, C. Skov, E. H. Van Nees, R. Roijackers, E. Lammens & R. Portielje, 2007. Lake restoration: successes, failures and long-term effects. Journal of Applied Ecology 44: 1095–1105.

    Article  Google Scholar 

  • Stehlik, I., J. P. Caspersen, L. Wirth & R. Holderegger, 2007. Floral free fall in the Swiss lowlands: Environmental determinants of local plant extinction in a peri-urban landscape. Journal of Ecology 95: 734–744.

    Article  Google Scholar 

  • Valdemarsen, T., E. Kristensen & M. Holmer, 2009. Metabolic threshold and sulphide-buffering in diffusion controlled marine sediments impacted by continuous organic enrichment. Biogeochemistry 95: 335–353.

    Article  CAS  Google Scholar 

  • Valderrama, J. C., 1977. Methods used by the hydrographic Department of the National Board of Fisheries, Sweden. In Grasshof, K. (ed.), Report of the Baltic intercalibration workshop. Interim Commission for the Protection of the Environment of the Baltic Sea, Goteborg: 13–40.

    Google Scholar 

  • Wang, J. & D. Yu, 2007. Influence of sediment fertility on morphological variability of Vallisneria spiralis L. Aquatic Botany 122: 94–99.

    Google Scholar 

  • Xiao, K., D. Yu & J. Wang, 2006. Habitat selection in spatially heterogeneous environments: A test of foraging behaviour in the clonal submerged macrophyte Vallisneria spiralis. Freshwater Biology 51: 1552–1559.

    Article  Google Scholar 

  • Yuan, G., H. Fu, J. Zhong, Q. Lou, L. Ni & T. Cao, 2016. Growth and C/N metabolism of three submersed macrophytes in response to water depths. Environmental and Experimental Botany 68: 44–50.

    Google Scholar 

  • Zhang, M., T. Cao, L. Ni, P. Xie & Z. Li, 2010. Carbon, nitrogen and antioxidant enzyme responses of Potamogeton crispus to both low light and high nutrient stresses. Environmental and Experimental Botany 68: 44–50.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to thank Dr. E. Soana and Dr. M. Bartoli for their suggestions on and contributions to the experiment design. Special thanks goes to Prof. P. Viaroli for his valuable comments on an early version of the present manuscript. We also express our gratitude to Dr. A. Laini for his fundamental support in the statistical analyses. We thank the Parchi del Ducato and Dr. N. Toscani for the field support. We thank the Associate editor and three anonymous reviewers for their excellent comments on the draft of this article. Dr. R. Bolpagni was partially supported by the University of Parma (Grant No. 377-03102014).

Author information

Authors and Affiliations

  1. Department of Life Sciences, Parma University, Parco Area Delle Scienze 11A, 43124, Parma, Italy

    R. Bolpagni & F. Pino

Authors
  1. R. Bolpagni
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. Pino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to R. Bolpagni.

Additional information

Handling editor: André Padial

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 42 kb)

10750_2016_3064_MOESM2_ESM.tif

Supplementary material 2 (TIFF 388 kb). Illustrative images of two shoots of Marsilea quadrifolia showing fronds and knots

Supplementary material 3 (DOC 45 kb)

Supplementary material 4 (DOC 442 kb)

Supplementary material 5 (DOC 405 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Bolpagni, R., Pino, F. Sediment nutrient drivers of the growth dynamics of the rare fern Marsilea quadrifolia . Hydrobiologia 792, 303–314 (2017). https://doi.org/10.1007/s10750-016-3064-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-016-3064-4

Keywords

Search

Navigation