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Macrophyte-induced thermal stratification in a shallow urban lake promotes conditions suitable for nitrogen-fixing cyanobacteria

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Abstract

Densely vegetated shallow lakes often experience low water column nutrient levels and reduced phytoplankton growth, but in some cases a high phytoplankton biomass can co-exist with submerged macrophytes. The conditions that favour phytoplankton blooms within areas colonized by submerged macrophytes remain largely unexplored. We investigated changes in water quality variables and phytoplankton community composition data in relation to macrophyte-induced thermal stratification in a shallow urban lake. The results indicate that submerged macrophytes may favour internal loadings of phosphorus and low DIN:TP ratios, in periods when macrophyte-induced thermal stratification of the water column is common. Blooms of nitrogen-fixing cyanobacteria occurred under the strongly stratified conditions triggered by the high macrophyte biomass and elevated canopy, even though nitrogen limitation was apparent during the whole growing season. These findings suggest that submerged macrophytes can promote blooms of nitrogen-fixing cyanobacteria once they are sufficiently tall and dense to induce stable water column conditions.

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References

  • Andersen, M. R., K. Sand-Jensen, R. Iestyn Woolway & I. D. Jones, 2017. Profound daily vertical stratification and mixing in a small, shallow, wind-exposed lake with submerged macrophytes. Aquatic Sciences 79: 395–406.

    Article  CAS  Google Scholar 

  • Anderson, M. J. & D. C. I. Walsh, 2013. PERMANOVA, ANOSIM, and the Mantel test in the face of heterogeneous dispersions: what null hypothesis are you testing? Ecological Monographs 83: 557–574.

    Article  Google Scholar 

  • Anderson, M. J., K. E. Ellingsen & B. H. McArdle, 2006. Multivariate dispersion as a measure of beta diversity. Ecology Letters 9: 683–693.

    Article  PubMed  Google Scholar 

  • Barko, J. W. & W. F. James, 1998. Effects of submerged aquatic macrophytes on nutrient dynamics, sedimentation, and resuspension. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The structuring role of submerged macrophytes in lakes. Springer, New York: 197–214.

    Chapter  Google Scholar 

  • Blair, R. C. & J. J. Higgins, 1980. A Comparison of the power of Wilcoxon’s rank-sum statistic to that of Student’s t statistic under various nonnormal distributions. Journal of Educational Statistics 5: 309–335.

    Article  Google Scholar 

  • Bolduan, B. R., G. C. Van Eeckhout, H. W. Quade & J. E. Gannon, 1994. Potamogeton crispus—the other invader. Lake and Reservoir Management 10: 113–125.

    Article  Google Scholar 

  • Boros, G., M. Søndergaard, P. Takács, Á. Vári & I. Tátrai, 2011. Influence of submerged macrophytes, temperature, and nutrient loading on the development of redox potential around the sediment–water interface in lakes. Hydrobiologia 665: 117–127.

    Article  CAS  Google Scholar 

  • Borum, J., O. Pedersen, T. M. Greve, T. A. Frankovich, J. C. Zieman, J. W. Fourqurean & C. J. Madden, 2005. The potential role of plant oxygen and sulphide dynamics in die-off events of the tropical seagrass, Thalassia testudinum. Journal of Ecology 93: 148–158.

    Article  CAS  Google Scholar 

  • Branco, B., T. Torgersen, J. R. Bean, G. Grenier & D. Arbige, 2005. A new water column profiler for shallow aquatic systems. Limnology and Oceanography: Methods 3: 190–202.

    Article  CAS  Google Scholar 

  • Caraco, N., J. Cole, S. Findlay & C. Wigand, 2006. Vascular plants as engineers of oxygen in aquatic systems. BioScience 56: 219.

    Article  Google Scholar 

  • Carey, C. C., B. W. Ibelings, E. P. Hoffmann, D. P. Hamilton & J. D. Brookes, 2012. Eco-physiological adaptations that favour freshwater cyanobacteria in a changing climate. Water Research 46: 1394–1407.

    Article  CAS  PubMed  Google Scholar 

  • Carpenter, S. R., 1981. Submersed vegetation: an internal factor in lake ecosystem succession. The American Naturalist 118: 372–383.

    Article  Google Scholar 

  • Chambers, P. A., 1982. Light, temperature and the induction of dormancy in Potamogeton crispus and Potamogeton obtusifolius. Ph.D. thesis. University of St. Andrews.

  • Chambers, P. A., E. E. Prepas, M. L. Bothwell & H. R. Hamilton, 1989. Roots versus shoots in nutrient uptake by aquatic macrophytes in flowing waters. Canadian Journal of Fisheries and Aquatic Sciences 46: 435–439.

    Article  Google Scholar 

  • Chimney, M. J., L. Wenkert & K. C. Pietro, 2006. Patterns of vertical stratification in a subtropical constructed wetland in south Florida (USA). Ecological Engineering 27: 322–330.

    Article  Google Scholar 

  • Clarke, K. R., 1993. Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18: 117–143.

    Article  Google Scholar 

  • Coops, H., E. H. van Nes, M. S. van den Berg & G. D. Butijn, 2002. Promoting low-canopy macrophytes to compromise conservation and recreational navigation in a shallow lake. Aquatic Ecology 36: 483–492.

    Article  Google Scholar 

  • de Tezanos Pinto, P. & E. Litchman, 2010. Interactive effects of N: P ratios and light on nitrogen-fixer abundance. Oikos 119: 567–575.

    Article  Google Scholar 

  • Downing, J. A., S. B. Watson & E. McCauley, 2001. Predicting cyanobacteria dominance in lakes. Canadian Journal of Fisheries and Aquatic Sciences 58: 1905–1908.

    Article  Google Scholar 

  • Ferber, L. R., S. N. Levine, A. Lini & G. P. Livingston, 2004. Do cyanobacteria dominate in eutrophic lakes because they fix atmospheric nitrogen? Freshwater Biology 49: 690–708.

    Article  CAS  Google Scholar 

  • Fonseca, B. M. & C. E. D. M. Bicudo, 2010. How important can the presence/absence of macrophytes be in determining phytoplankton strategies in two tropical shallow reservoirs with different trophic status? Journal of Plankton Research 32: 31–46.

    Article  Google Scholar 

  • Goodwin, K., N. Caraco & J. Cole, 2008. Temporal dynamics of dissolved oxygen in a floating-leaved macrophyte bed. Freshwater Biology 53: 1632–1641.

    Article  CAS  Google Scholar 

  • Havens, K. E., R. T. James, T. L. East & V. H. Smith, 2003. N: P ratios, light limitation, and cyanobacterial dominance in a subtropical lake impacted by non-point source nutrient pollution. Environmental Pollution 122: 379–390.

    Article  CAS  PubMed  Google Scholar 

  • Herb, W. R. & H. G. Stefan, 2005. Model for wind-driven vertical mixing in a shallow lake with submersed macrophytes. Journal of Hydraulic Engineering 131: 488–496.

    Article  Google Scholar 

  • Hickey, C. W. & M. M. Gibbs, 2009. Lake sediment phosphorus release management-decision support and risk assessment framework. New Zealand Journal of Marine and Freshwater Research 43: 819–856.

    Article  CAS  Google Scholar 

  • Hölker, F., M. J. Vanni, J. J. Kuiper, C. Meile, H.-P. Grossart, P. Stief, R. Adrian, A. Lorke, O. Dellwig, A. Brand, M. Hupfer, W. M. Mooij, G. Nützmann & J. Lewandowski, 2015. Tube-dwelling invertebrates: tiny ecosystem engineers have large effects in lake ecosystems. Ecological Monographs 85: 333–351.

    Article  Google Scholar 

  • Holmroos, H., J. Horppila, J. Niemistö, L. Nurminen & S. Hietanen, 2014. Dynamics of dissolved nutrients among different macrophyte stands in a shallow lake. Limnology 16: 31–39.

    Article  Google Scholar 

  • Horppila, J. & L. Nurminen, 2003. Effects of submerged macrophytes on sediment resuspension and internal phosphorus loading in Lake Hiidenvesi (southern Finland). Water Research 37: 4468–4474.

    Article  CAS  PubMed  Google Scholar 

  • Huisman, J., J. Sharples, J. M. Stroom, P. M. Visser, W. E. A. Kardinaal, J. M. H. Verspagen & B. Sommeijer, 2004. Changes in turbulent mixing shift competition for light between phytoplankton species. Ecology 85: 2960–2970.

    Article  Google Scholar 

  • Imberger, J., 2004. A lake diagnostic system for managing lakes and reservoirs. Water Resources Impact 6: 7–10.

    Google Scholar 

  • Imberger, J. & R. Head, 1994. Measurement of turbulent properties in a natural system. Proceedings of Symposium on Fundamentals and Advancements in Hydraulic Measurements and Experimentation. Buffalo, New York: 1–20.

  • Jensen, H. S. & F. O. Andersen, 1992. Importance of temperature, nitrate, and pH for phosphate release from aerobic sediments of four shallow, eutrophic lakes. Limnology and Oceanography 37: 577–589.

    Article  Google Scholar 

  • Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen, L. J. Pedersen & L. Jensen, 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342: 151–164.

    Article  Google Scholar 

  • Jeppesen, E., M. Søndergaard, M. Meerhoff, T. L. Lauridsen & J. P. Jensen, 2007. Shallow lake restoration by nutrient loading reduction—some recent findings and challenges ahead. Hydrobiologia 584: 239–252.

    Article  CAS  Google Scholar 

  • Lamers, L. P. M., L. L. Govers, I. I. C. J. M. Janssen, J. J. M. Geurts, M. E. W. Van der Welle, M. M. Van Katwijk, T. Van der Heide, J. G. M. Roelofs & A. J. P. Smolders, 2013. Sulfide as a soil phytotoxin—a review. Frontiers in Plant Science 4: 268.

    Article  PubMed  PubMed Central  Google Scholar 

  • Lemoine, D. G., F. Mermillod-Blondin, M. H. Barrat-Segretain, C. Massé & E. Malet, 2012. The ability of aquatic macrophytes to increase root porosity and radial oxygen loss determines their resistance to sediment anoxia. Aquatic Ecology 46: 191–200.

    Article  CAS  Google Scholar 

  • Leoni, B., C. L. Marti, E. Forasacco, M. Mattavelli, V. Soler, P. Fumagalli, J. Imberger, S. Rezzonico & L. Garibaldi, 2016. The contribution of Potamogeton crispus to the phosphorus budget of an urban shallow lake: Lake Monger, Western Australia. Limnology 17: 175–182.

    Article  CAS  Google Scholar 

  • Lund, M. A. & J. A. Davis, 2000. Seasonal dynamics of plankton communities and water chemistry in a eutrophic wetland (Lake Monger, Western Australia): implications for biomanipulation. Marine & Freshwater Research 51: 321–332.

    Article  CAS  Google Scholar 

  • Madsen, T. V. & K. Sand-Jensen, 1991. Photosynthetic carbon assimilation in aquatic macrophytes. Aquatic Botany 41: 5–40.

    Article  CAS  Google Scholar 

  • Mi, W. J., D. W. Zhu, Y. Y. Zhou, H. D. Zhou, T. W. Yang & D. P. Hamilton, 2007. Influence of Potamogeton crispus growth on nutrients in the sediment and water of Lake Tangxunhu. Hydrobiologia 603: 139–146.

    Article  Google Scholar 

  • Muylaert, K., C. Pérez-Martínez, P. Sánchez-Castillo, T. L. Lauridsen, M. Vanderstukken, S. A. J. Declerck, K. Van Der Gucht, Á. J.-M. Conde-Porcuna, Á. E. Jeppesen, Á. L. De Meester & Á. W. Vyverman, 2010. Influence of nutrients, submerged macrophytes and zooplankton grazing on phytoplankton biomass and diversity along a latitudinal gradient in Europe. Hydrobiologia 653: 79–90.

    Article  CAS  Google Scholar 

  • Nowlin, W. H., J. L. Evarts & M. J. Vanni, 2005. Release rates and potential fates of nitrogen and phosphorus from sediments in a eutrophic reservoir. Freshwater Biology 50: 301–322.

    Article  CAS  Google Scholar 

  • Nurminen, L. & J. Horppila, 2009. Life form dependent impacts of macrophyte vegetation on the ratio of resuspended nutrients. Water Research 43: 3217–3226.

    Article  CAS  PubMed  Google Scholar 

  • O’Neil, J. M., T. W. Davis, M. A. Burford & C. J. Gobler, 2012. The rise of harmful cyanobacteria blooms: the potential roles of eutrophication and climate change. Harmful Algae 14: 313–334.

    Article  Google Scholar 

  • Oksanen, J., F. G. Blanchet, R. Kindt, P. Legendre, P. R. Minchin, R. B. O’Hara, G. L. Simpson, P. Solymos, M. H. H. Stevens, & H. Wagner, 2016. Vegan: community ecology package. R Package version 2.3-5.

  • Padisák, J. & C. S. Reynolds, 2003. Shallow lakes: the absolute, the relative, the functional and the pragmatic. Hydrobiologia 506–509: 1–11.

    Article  Google Scholar 

  • Paerl, H. W., N. S. Hall & E. S. Calandrino, 2011. Controlling harmful cyanobacterial blooms in a world experiencing anthropogenic and climatic-induced change. Science of the Total Environment 409: 1739–1745.

    Article  CAS  PubMed  Google Scholar 

  • Pakdel, F. M., L. Sim, J. Beardall & J. Davis, 2013. Allelopathic inhibition of microalgae by the freshwater stonewort, Chara australis, and a submerged angiosperm, Potamogeton crispus. Aquatic Botany 110: 24–30.

    Article  Google Scholar 

  • Pettersson, L. H. & D. Pozdnyakov, 2013. Qualification, species variety, and consequences of harmful algal blooms (HABs). Monitoring of Harmful Algal Blooms. Springer, Berlin Heidelberg: 1–24.

    Chapter  Google Scholar 

  • Phillips, G., N. Willby & B. Moss, 2016. Submerged macrophyte decline in shallow lakes: what have we learnt in the last forty years? Aquatic Botany 135: 37–45.

    Article  Google Scholar 

  • Pierce, D., 1997. Contaminant cycling in Lake Monger and its implications for lake management. Honours thesis. University of Western Australia.

  • Qiu, S. & A. McComb, 2000. Properties of sediment phosphorus in seven wetlands of the Swan Coastal Plain, South-Western Australia. Wetlands 20: 267–279.

    Article  Google Scholar 

  • Reddy, K. R., M. M. Fisher & D. Ivanoff, 1996. Resuspension and diffusive flux of nitrogen and phosphorus in a hypereutrophic lake. Journal of Environmental Quality 25: 363–371.

    Article  CAS  Google Scholar 

  • Reynolds, C. S., 2006. The Ecology of Phytoplankton. Cambridge University Press, Cambridge.

    Book  Google Scholar 

  • Rice, E. W., R. B. Baird, A. D. Eaton & L. S. Clesceri, 2012. Standard methods for the examination of water and wastewater. American Public Health Association, American Water Works Association, Water Environment Federation, Washington, DC.

    Google Scholar 

  • Rogers, K. H. & C. M. Breen, 1980. Growth and reproduction of Potamogeton crispus in a South African lake. The Journal of Ecology 68: 561–571.

    Article  CAS  Google Scholar 

  • Rogers, K. H. & C. M. Breen, 1982. Decomposition of Potamogeton crispus L.: the effects of drying on the pattern of mass and nutrient loss. Aquatic Botany 12: 1–12.

    Article  CAS  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. Rinaldi, A. Gragnani, L. R. Mur & E. H. van Nes, 1997. On the dominance of filamentous cyanobacteria in shallow, turbid lakes. Ecology 78: 272.

    Article  Google Scholar 

  • Schindler, D. W., 1977. Evolution of phosphorus limitation in lakes. Science (New York, N.Y.) 195: 260–262.

    Article  CAS  Google Scholar 

  • Schriver, P., J. Bogestrand, E. Jeppesen & M. Søndergaard, 1995. Impact of submerged macrophytes on fish-zooplanl phytoplankton interactions: large-scale enclosure experiments in a shallow eutrophic lake. Freshwater Biology 33: 255–270.

    Article  Google Scholar 

  • Sherman, B. S., I. T. Webster, G. J. Jones & R. L. Oliver, 1998. Transitions between Aulacoseira and Anabaena dominance in a turbid river weir pool. Limnology and Oceanography 43: 1902–1915.

    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 

  • Soana, E., M. Naldi, S. Bonaglia, E. Racchetti, G. Castaldelli, V. Brüchert, P. Viaroli & M. Bartoli, 2015. Benthic nitrogen metabolism in a macrophyte meadow (Vallisneria spiralis L.) under increasing sedimentary organic matter loads. Biogeochemistry 124: 387–404.

    Article  CAS  Google Scholar 

  • Søndergaard, M. & B. Moss, 1998. Impact of submerged macrophytes on phytoplankton in shallow freshwater lakes. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 115–133.

    Chapter  Google Scholar 

  • Søndergaard, M., J. P. Jensen & E. Jeppesen, 2003. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506–509: 135–145.

    Article  Google Scholar 

  • Takamura, N., Y. Kadono, M. Fukushima, M. Nakagawa & B.-H. O. Kim, 2003. Effects of aquatic macrophytes on water quality and phytoplankton communities in shallow lakes. Ecological Research 18: 381–395.

    Article  CAS  Google Scholar 

  • Tobiessen, P. & P. D. Snow, 1984. Temperature and light effects on the growth of Potamogeton crispus in Collins Lake, New York State. Canadian Journal of Botany 62: 2822–2826.

    Article  Google Scholar 

  • Unrein, F., I. O’Farrell, I. Izaguirre, R. Sinistro, M. dos Santos Afonso & G. Tell, 2010. Phytoplankton response to pH rise in a N-limited floodplain lake: relevance of N2-fixing heterocystous cyanobacteria. Aquatic Sciences 72: 179–190.

    Article  CAS  Google Scholar 

  • Van den Berg, M. S., H. Coops, M. L. Meijer, M. Scheffer & J. Simons, 1998. Clear water associated with a dense Chara vegetation in the shallow and turbid Lake Veluwemeer, The Netherlands. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 339–352.

    Chapter  Google Scholar 

  • van Donk, E. & W. J. van de Bund, 2002. Impact of submerged macrophytes including charophytes on phyto- and zooplankton communities: allelopathy versus other mechanisms. Aquatic Botany 72: 261–274.

    Article  Google Scholar 

  • Vilas, M. P., Marti, C. L., Adams, M. P., Oldham, C. E. & M. R. Hipsey. Invasive macrophytes control the spatial and temporal patterns of temperature and dissolved oxygen in a shallow lake: A proposed mechanism of macrophyte loss. Frontiers in Plant Science (In review)

  • Watts, C. J., 2000. Seasonal phosphorus release from exposed, re-inundated littoral sediments of two Australian reservoirs. Hydrobiologia 431: 27–39.

    Article  CAS  Google Scholar 

  • Welsh, R. P. H. & P. Denny, 1979. The Translocation of 32P in two submerged aquatic angiosperm species. New Phytologist 82: 645–656.

    Article  CAS  Google Scholar 

  • Wilcoxon, F., 1945. Individual comparisons by ranking method. Biometrics Bulletin 1: 80–83.

    Article  Google Scholar 

  • Wilhelm, S. & R. Adrian, 2008. Impact of summer warming on the thermal characteristics of a polymictic lake and consequences for oxygen, nutrients and phytoplankton. Freshwater Biology 53: 226–237.

    Article  CAS  Google Scholar 

  • Wood, S. A., M. J. Prentice, K. Smith & D. P. Hamilton, 2010. Low dissolved inorganic nitrogen and increased heterocyte frequency: precursors to Anabaena planktonica blooms in a temperate, eutrophic reservoir. Journal of Plankton Research 32: 1315–1325.

    Article  CAS  Google Scholar 

  • Wu, J., S. Cheng, W. Liang, F. He & Z. Wu, 2009. Effects of sediment anoxia and light on turion germination and early growth of Potamogeton crispus. Hydrobiologia 628: 111–119.

    Article  Google Scholar 

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Acknowledgements

Gregory Attwater, Roger Head, Carol Lam, Angus Stewart and Lee Goodyear are thanked for their support on the acquisition and processing of field data. Chris Brower and Alice Gedaria are also acknowledged for assisting in the laboratory analysis. Maria P. Vilas would like to acknowledge the valuable contribution of Professor Jörg Imberger in the first steps of this research. She also acknowledges the Town of Cambridge, Centre for Water Research and SIRF scholarships. Clelia L. Marti is the recipient of a grant provided by the Town of Cambridge for the project “Lake Monger – understating of its functioning”.

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  1. School of Agriculture and Environment, The University of Western Australia, Crawley, WA, 6009, Australia

    M. P. Vilas & M. R. Hipsey

  2. Sustainable Engineering Group, Faculty of Science and Engineering, Curtin University, Bentley, WA, 6102, Australia

    C. L. Marti

  3. School of Civil, Environmental and Mining Engineering, The University of Western Australia, Crawley, WA, 6009, Australia

    C. E. Oldham

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  1. M. P. Vilas
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Vilas, M.P., Marti, C.L., Oldham, C.E. et al. Macrophyte-induced thermal stratification in a shallow urban lake promotes conditions suitable for nitrogen-fixing cyanobacteria. Hydrobiologia 806, 411–426 (2018). https://doi.org/10.1007/s10750-017-3376-z

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