, Volume 794, Issue 1, pp 49–57 | Cite as

Biomanipulation-induced reduction of sediment phosphorus release in a tropical shallow lake

  • Xiufeng Zhang
  • Yali Tang
  • Erik Jeppesen
  • Zhengwen Liu
Primary Research Paper


Biomanipulation via fish regulation combined with submerged plant introduction is an effective measure to restore eutrophic shallow lakes. Improved water quality and clarity promote growth of benthic algae, which with submerged plants may limit sediment phosphorus (P) release, thereby reinforce lake recovery. Our study sought to evaluate the effect of such a biomanipulation on water quality, benthic algal development and sediment P release in a shallow, tropical lake by (1) comparing porewater and lake water quality, light intensity and benthic algal development in restored and unrestored sections; (2) conducting a 32P radiotracer experiment to track P release from sediment cores sampled from both sections. The biomanipulation led to lower total P, total dissolved P, and soluble reactive P concentrations in lake water, lower phytoplankton biomass, and increased light intensity at sediment surface, stimulating benthic algal development. Moreover, sediment 32P release was lower in the restored than unrestored section. Concurrently, dissolved oxygen levels in upper layers of the sediment cores were higher in the restored section. Our study indicates that the biomanipulation improved water quality and enhanced growth of benthic algae, thereby reducing sediment P release, which may be one of the main mechanisms to create successful restoration.


Biomanipulation Submerged plant Fish manipulation Restoration Induced benthic algae Eutrophication Shallow lakes 



We thank Anne Mette Poulsen for valuable editorial work and Henning Skovgaard Jensen for constructive comments of this manuscript. The study was sponsored by the National Natural Science Foundation of China (No. 31570456 and 31000219) and the Natural Science Foundation of Guangdong Province (No. 2016A030313103) and was completed while the first author was a visiting associate professor at Cornell University. EJ was supported by the MARS project (Managing Aquatic ecosystems and water Resources under multiple Stress) funded under the 7th EU Framework Programme, Theme 6 (Environment including Climate Change), Contract No.: 603378 (, and the Danish project CLEAR (a Villum Kann Rasmussen Centre of Excellence project).


  1. APHA, 1992. Standard methods: for examination of water and wastewater, 18th ed. American Public Health Association.Google Scholar
  2. Barbour, M. T., J. Gerritsen, B. D. Snyder & J. B. Stribling, 1999. Rapid bioassessment protocols for use in streams and wadeable rivers USEPA, Washington.Google Scholar
  3. 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.CrossRefGoogle Scholar
  4. Blindow, I., G. Andersson, A. Hargeby & S. Johansson, 1993. Long-term pattern of alternative stable states in two shallow eutrophic lakes. Freshwater Biology 30: 159–167.CrossRefGoogle Scholar
  5. Brenner, M., T. J. Whitmore, M. A. Lasi, J. E. Cable & P. H. Cable, 1999. A multi-proxy trophic state reconstruction for shallow Orange Lake, Florida, USA: possible influence of macrophytes on limnetic nutrient concentrations. Journal of Paleolimnology 21: 215–233.CrossRefGoogle Scholar
  6. Carignan, R. & J. Kalff, 1980. Phosphorus sources for aquatic weeds: water or sediments? Science 207: 987–989.CrossRefPubMedGoogle Scholar
  7. Carlton, R. G. & R. G. Wetzel, 1988. Phosphorus flux from lake sediments: effects of epipelic algal oxygen production. Limnology and Oceanography 33: 562–570.CrossRefGoogle Scholar
  8. Carpenter, S. R., D. L. Christensen, J. J. Cole, K. L. Cottingham, X. He, J. R. Hodgson, J. F. Kitchell, S. E. Knight, M. L. Pace, D. M. Post, D. E. Schindler & N. Voichick, 1995. Biological control of eutrophication in lakes. Environmental Science & Technology 29: 784–786.CrossRefGoogle Scholar
  9. Christensen, K. K., F. O. Andersen & H. S. Jensen, 1997. Comparison of iron, manganese and phosphorus retention in freshwater litorral sediment with growth of Litorella uniflora and benthic microalgae. Biogeochemistry 38: 149–171.CrossRefGoogle Scholar
  10. Dalsgaard, T., 2003. Benthic primary production and nutrient cycling in sediments with benthic microalgae and transient accumulation of macroalgae. Limnology and Oceanography 48: 2138–2150.CrossRefGoogle Scholar
  11. Dodds, W. K., 2003. The role of periphyton in phosphorus retention in shallow freshwater aquatic systems. Journal of Phycology 39: 840–849.CrossRefGoogle Scholar
  12. Drenner, R. W. & K. D. Hambright, 1999. Biomanipulation of fish assemblages as a lake restoration technique. Archiv für Hydrobiologie 146: 129–165.CrossRefGoogle Scholar
  13. Gao, J., Z. Liu & E. Jeppesen, 2014. Fish community assemblages changed but biomass remained similar after lake restoration by biomanipulation in a Chinese tropical eutrophic lake. Hydrobiologia 724: 127–140.CrossRefGoogle Scholar
  14. Graham, J. M., P. Arancibia-Avila & L. E. Graham, 1996. Physiological ecology of a species of the filamentous green alga Mougeotia under acidic conditions: light and temperature effects on photosynthesis and respiration. Limnology and Oceanography 41: 253–261.CrossRefGoogle Scholar
  15. Hansson, L. A., 1989. The influence of a periphytic biolayer on phosphorus exchange between substrate and water. Archiv für Hydrobiologie 115: 21–26.Google Scholar
  16. Hansson, L. A., 1990. Quantifying the impact of periphytic algae on nutrient availability for phytoplankton. Freshwater Biology 24: 265–273.CrossRefGoogle Scholar
  17. Holdren, G. C. & D. E. Armstrong, 1986. Interstitial ion concentrations as an indicator of phosphorus release and mineral formation in lake sediments. In Sediments and Water Interactions. Springer, New York: 133–147Google Scholar
  18. Hu, H. J. & Y. X. Wei, 2006. The Freshwater Algae of China: Systematics, Taxonomy and Ecology. Science Press, Beijing.Google Scholar
  19. Hupfer, M. & A. Dollan, 2003. Immobilisation of phosphorus by iron-coated roots of submerged macrophytes. Hydrobiologia 506: 635–640.CrossRefGoogle Scholar
  20. Jaynes, M. L. & S. R. Carpenter, 1986. Effects of vascular and nonvascular macrophytes on sediment redox and solute dynamics. Ecology 67: 875–882.CrossRefGoogle Scholar
  21. Jensen, H. S., O. L. Nielsen, M. S. Koch & I. de Vicente, 2009. Phosphorus release with carbonate dissolution coupled to sulfide oxidation in Florida Bay seagrass sediments. Limnology and Oceanography 54: 1753–1764.CrossRefGoogle Scholar
  22. Jensen, M., Z. W. Liu, X. F. Zhang, K. Reitzel & H. S. Jensen. 2016. The effect of biomanipulation on phosphorus exchange between sediment and water in shallow, tropical Huizhou West Lake, China. Limnologica (Accepted)Google Scholar
  23. 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.CrossRefGoogle Scholar
  24. Jeppesen, E., M. Søndergaard, T. L. Lauridsen, T. A. Davidson, Z. W. Liu, N. Mazzeo, C. Trochine, K. Özkan, H. S. Jensen, D. Trolle, F. Starling, X. Lazzaro, L. S. Johansson, R. Bjerring, L. Liboriussen, S. E. Larsen, F. Landkildehus, S. Egemose & M. Meerhoff, 2012. Biomanipulation as a restoration tool to combat eutrophication: recent advances and future challenges. Advances in Ecological Research 47: 411–488.CrossRefGoogle Scholar
  25. Jespersen, A. M. & K. Christoffersen, 1987. Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Archiv für Hydrobiologie 109: 445–454.Google Scholar
  26. Jin, X. C., Q. J. Xu & C. Z. Yan, 2006. Restoration scheme for macrophytes in a hypertrophic water body, Wuli Lake, China. Lakes & Reservoirs: Research and Management 11: 21–27.CrossRefGoogle Scholar
  27. Kalnejais, L. H., W. R. Martin & M. H. Bothner, 2015. Porewater dynamics of silver, lead and copper in coastal sediments and implications for benthic metal fluxes. Science of the Total Environment 517: 178–194.CrossRefPubMedGoogle Scholar
  28. Liboriussen, L. & E. Jeppesen, 2003. Temporal dynamics in epipelic, pelagic and epiphytic algal production in a clear and a turbid shallow lake. Freshwater Biology 48: 418–431.CrossRefGoogle Scholar
  29. Liu, Z., P. Zhong, X. Zhang, J. Ning, S. E. Larsen & E. Jeppesen. Successful restoration of a tropical shallow eutrophic lake by biomanipulation: strong bottom-up but weak top-down effects recorded (Submitted)Google Scholar
  30. Lorenz, R. C., M. E. Monaco & C. E. Herdendorf, 1991. Minimum light requirements for substrate colonization by Cladophora glomerata. Journal of Great Lakes Research 17: 536–542.CrossRefGoogle Scholar
  31. Lubarsky, H. V., C. Hubas, M. Chocholek, F. Larson, W. Manz, D. M. Paterson & S. U. Gerbersdorf, 2010. The stabilisation potential of individual and mixed assemblages of natural bacteria and microalgae. PLoS ONE 5: e13794.CrossRefPubMedPubMedCentralGoogle Scholar
  32. McCormick, P. V. & M. B. O’Dell, 1996. Quantifying periphyton responses to phosphorus in the Florida Everglades: a synoptic-experimental approach. Journal of the North American Benthological Society 15: 450–468.CrossRefGoogle Scholar
  33. Pérez-Martínez, C., P. Sánchez-Castillo & M. Z. Jiménez-Pérez, 2010. Utilization of immobilized benthic algal species for N and P removal. Journal of Applied Phycology 22: 277–282.CrossRefGoogle Scholar
  34. Qiu, D. R., Z. B. Wu, B. Y. Liu, J. Q. Deng, G. P. Fu & F. He, 2001. The restoration of aquatic macrophytes for improving water quality in a hypertrophic shallow lake in Hubei Province, China. Ecological Engineering 18: 147–156.CrossRefGoogle Scholar
  35. Rooney, N., J. Kalff & C. Habel, 2003. The role of submerged macrophyte beds in phosphorus and sediment accumulation in Lake Memphremagog, Quebec, Canada. Limnology and Oceanography 48: 1927–1937.CrossRefGoogle Scholar
  36. Schindler, D. W., 1977. Evolution of phosphorus limitation in lakes. Science 195(4275): 260–262.CrossRefPubMedGoogle Scholar
  37. Schindler, D. W., 2006. Recent advances in the understanding and management of eutrophication. Limnology and Oceanography 51: 356–363.CrossRefGoogle Scholar
  38. Shilla, D. A., T. Asaeda, S. Kian, R. Lalith & J. Manatunge, 2006. Phosphorus concentration in sediment, water and tissues of three submerged macrophytes of Myall Lake, Australia. Wetlands Ecology and Management 14: 549–558.CrossRefGoogle Scholar
  39. Søndergaard, M., J. P. Jensen & E. Jeppesen, 2003. Role of sediment and internal loading of phosphorus in shallow lakes. Hydrobiologia 506: 135–145.CrossRefGoogle Scholar
  40. Søndergaard, M., R. Bjerring & E. Jeppesen, 2013. Persistent internal phosphorus loading during summer in shallow eutrophic lakes. Hydrobiologia 710: 95–107.CrossRefGoogle Scholar
  41. Spears, B. M., L. Carvalho, R. Perkins & D. M. Paterson, 2008. Effects of light on sediment nutrient flux and water column nutrient stoichiometry in a shallow lake. Water Research 42: 977–986.CrossRefPubMedGoogle Scholar
  42. Steinman, A. D. & C. D. McIntire, 1987. Effects of irradiance on the community structure and biomass of algal assemblages in laboratory streams. Canadian journal of fisheries and aquatic sciences 44: 1640–1648.CrossRefGoogle Scholar
  43. Stevenson, R. J. & E. F. Stoermer, 1982. Luxury consumption of phosphorus by benthic algae. Biological Science 32: 682–683.Google Scholar
  44. Tolhurst, T. J., M. Consalvey & D. M. Paterson, 2008. Changes in cohesive sediment properties associated with the growth of a diatom biofilm. Hydrobiologia 596: 225–239.CrossRefGoogle Scholar
  45. Tyler, A. C., K. J. McGlathery & I. C. Anderson, 2003. Benthic algae control sediment – water column fluxes of organic and inorganic nitrogen compounds in a temperate lagoon. Limnology and Oceanography 48: 2125–2137.CrossRefGoogle Scholar
  46. Vadeboncoeur, Y., E. Jeppesen, M. Zanden, H. H. Schierup, K. Christoffersen & D. M. Lodge, 2003. From Greenland to green lakes: cultural eutrophication and the loss of benthic pathways in lakes. Limnology and Oceanography 48: 1408–1418.CrossRefGoogle Scholar
  47. van der Molen, D. T. & P. C. M. Boers, 1994. Influence of internal loading on phosphorus concentration in shallow lakes before and after reduction of the external loading. Hydrobiologia 275(276): 379–389.CrossRefGoogle Scholar
  48. van Luijn, F., D. T. van der Molen, W. J. Luttmer & P. C. M. Boers, 1995. Influence of benthic diatoms on the nutrient release from sediments of shallow lakes recovering from eutrophication. Water Science and Technology 32: 89–97.CrossRefGoogle Scholar
  49. Wang, S. R., X. C. Jin, H. C. Zhang, X. N. Zhou & F. C. Wu, 2007. Effects of Hydrilla verticillata on Phosphorus Retention and Release in Sediments. Water Air Soil Pollution 181: 329–339.CrossRefGoogle Scholar
  50. Wetzel, R. G., 2001. Limnology: Lake and River Ecosystems. Academic Press, San Diego.Google Scholar
  51. Wiencke, C., 2011. Biology of Polar Benthic Algae. Walter de Gruyter, Berlin.Google Scholar
  52. Zhang, X., Z. Liu, R. D. Gulati & E. Jeppesen, 2013. The effect of benthic algae on phosphorus exchange between sediment and overlying water in shallow lakes: a microcosm study using 32P as a tracer. Hydrobiologia 710: 109–116.CrossRefGoogle Scholar
  53. Zhang, X., Z. Liu, E. Jeppesen & W. D. Taylor, 2014. Effects of deposit-feeding tubificid worms and filter-feeding bivalves on benthic-pelagic coupling: implications for the restoration of eutrophic shallow lakes. Water Research 50: 135–146.CrossRefPubMedGoogle Scholar
  54. Zhang, X., Z. Liu, E. Jeppesen, W. D. Taylor & L. G. Rudstam, 2016. Effects of benthic-feeding common carp and filter-feeding silver carp on benthic-pelagic coupling: implications for shallow lake management. Ecological Engineering 88: 256–264.CrossRefGoogle Scholar
  55. Yu, J., Z. Liu, K. Li, F. Chen, B. Guan, Y. Hu, P. Zhong, Y. Tang, X. Zhao, H. He, H. Zeng & E. Jeppesen, 2016. Restoration of shallow lakes in subtropical and tropical China: response of nutrients and water clarity to biomanipulation by fish removal and submerged plant transplantation. Water. doi: 10.3390/w8100438.Google Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Xiufeng Zhang
    • 1
    • 2
  • Yali Tang
    • 1
  • Erik Jeppesen
    • 3
    • 4
  • Zhengwen Liu
    • 1
    • 4
    • 5
  1. 1.Department of Ecology and Institute of HydrobiologyJinan UniversityGuangzhouChina
  2. 2.Cornell Biological Field Station, Department of Natural ResourcesCornell UniversityBridgeportUSA
  3. 3.Department of Bioscience & Arctic Research Centre (ARC)Aarhus UniversitySilkeborgDenmark
  4. 4.Sino-Danish Centre for Education and Research (SDC)The University of Chinese AcademyBeijingChina
  5. 5.State Key Laboratory of Lake Science and Environment, Institute of Geography and LimnologyChinese Academy of SciencesNanjingChina

Personalised recommendations