Skip to main content

Advertisement

SpringerLink
Log in

The influence of bioturbation and water column oxygenation on nutrient recycling in reservoir sediments

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

Abstract

Sediments are sinks of nutrients in reservoirs, but may also act as temporary nutrient sources to the water column, leading to eutrophication during the warm season. Several abiotic and biotic factors at the water–sediment interface are known to influence the role of sediments as temporary nutrient sources. This study aimed at quantifying the effects of two factors (i.e., oxygenation and bioturbation) on fluxes of nutrients from the water–sediment interface of the reservoir. An experimental approach was developed in the laboratory to test three fauna conditions (no fauna, presence of tubificid worms, and chironomids larvae) and three conditions of water column oxygenation (aerobic, fluctuating, and anaerobic conditions). Chironomid larvae significantly increased concentrations of N (NH4+ + NO3−) and PO43− released from sediments by 3.7-fold and by 17-fold, whereas tubificid worms had a lesser effect (twofold for N and threefold for PO43−). Anaerobic conditions increased N by 56-fold and PO43− by 102-fold compared to the aerobic treatment. Thus, anaerobic conditions produced greater N and P fluxes than fauna. Nevertheless, fauna and anoxic conditions at the water–sediment interface should not be neglected when quantifying the role of sediments on nutrient dynamics in lakes and reservoirs.

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

  • Agence de l’Eau Rhône Méditerranée Corse, 2015. Suivi des plans d’eau des bassins Rhône-Méditerranée et Corse en application de la Directive Cadre sur l’Eau (Sites de Référence, Réseau de Contrôle de Surveillance et Contrôle Opérationnel) Note synthétique d’interprétation des résultats Puyvalador (66 : Pyrénées-Orientales) Campagnes 2013.

  • Aller, R. C., 2001. Transport and Reaction in the Bioirrigated Zone The Benthic Boundary Layer: Transport Processes and Biogeochemistry. Oxford University Press, Oxford: 269.

    Google Scholar 

  • Anschutz, P., A. Ciutat, P. Lecroart, M. Gérino & A. Boudou, 2012. Effects of tubificid worm bioturbation on freshwater sediment biogeochemistry. Aquatic Geochemistry 18: 475–497.

    CAS  Google Scholar 

  • Balangoda, A., 2017. Effect of diurnal variation of dissolved oxygen in a eutrophic polymictic reservoir. American Journal of Environmental Sciences 13: 30–46.

    CAS  Google Scholar 

  • Baranov, V., J. Lewandowski, P. Romeijn, G. Singer & S. Krause, 2016. Effects of bioirrigation of non-biting midges (Diptera: Chironomidae) on lake sediment respiration. Scientific Reports 6: 27239.

    Google Scholar 

  • Berner, R. A., 1980. Early diagenesis: a theoretical approach. Princeton University Press, Princeton.

    Google Scholar 

  • Beutel, M. W., 2006. Inhibition of ammonia release from anoxic profundal sediments in lakes using hypolimnetic oxygenation. Ecological Engineering 28: 271–279.

    Google Scholar 

  • Biles, C., D. Paterson, R. Ford, M. Solan & D. Raffaelli, 2002. Bioturbation, ecosystem functioning and community structure. Hydrology and Earth System Sciences Discussions 6: 999–1005.

    Google Scholar 

  • Boström, B., J. M. Andersen, S. Fleischer & M. Jansson, 1988. Exchange of phosphorus across the sediment-water interface. In Persson, G. & M. Jansson (eds.), Phosphorus in Freshwater Ecosystems. Springer, Dordrecht: 229–244.

    Google Scholar 

  • Boulton, A. J., S. Findlay, P. Marmonier, E. H. Stanley & H. M. Valett, 1998. The functional significance of the hyporheic zone in streams and rivers. Annual Review of Ecology and Systematics 29: 59–81.

    Google Scholar 

  • Bowen, J. L., A. R. Babbin, P. J. Kearns & B. B. Ward, 2014. Connecting the dots: linking nitrogen cycle gene expression to nitrogen fluxes in marine sediment mesocosms. Frontiers in Microbiology. https://doi.org/10.3389/fmicb.2014.00429/abstract.

    Article  PubMed  PubMed Central  Google Scholar 

  • Breitburg, D. L., J. K. Craig, R. S. Fulford, K. A. Rose, W. R. Boynton, D. C. Brady, B. J. Ciotti, R. J. Diaz, K. D. Friedland, J. D. Hagy, D. R. Hart, A. H. Hines, E. D. Houde, S. E. Kolesar, S. W. Nixon, J. A. Rice, D. H. Secor & T. E. Targett, 2009. Nutrient enrichment and fisheries exploitation: interactive effects on estuarine living resources and their management. Hydrobiologia 629: 31–47.

    CAS  Google Scholar 

  • Cheng, X., Y. Zeng, Z. Guo & L. Zhu, 2014. Diffusion of nitrogen and phosphorus across the sediment-water interface and in seawater at aquaculture areas of Daya Bay, China. International Journal of Environmental Research and Public Health 11: 1557–1572.

    PubMed  PubMed Central  Google Scholar 

  • Dahm, C. N., E. H. Trotter & J. R. Sedell, 1987. Role of anaerobic zones and processes in stream ecosystem productivity. Chemical Quality of Water and the Hydrologic Cycle 251: 157–178.

    Google Scholar 

  • Ekeroth, N., S. Blomqvist & P. Hall, 2016. Nutrient fluxes from reduced Baltic Sea sediment: effects of oxygenation and macrobenthos. Marine Ecology Progress Series 544: 77–92.

    CAS  Google Scholar 

  • Council, European, 2000. Directive 2000/60/EC of the European Parliament and of the Council of 23 October 2000 establishing a framework for Community action in the field of water policy. OJ L 327: 1–73.

    Google Scholar 

  • Findlay, D. & S. Kasian, 1987. Phytoplankton community responses to nutrient addition in Lake 226, Experimental Lakes Area, northwestern Ontario. Canadian Journal of Fisheries and Aquatic Sciences 44: s35–s46.

    Google Scholar 

  • Foley, B., I. D. Jones, S. C. Maberly & B. Rippey, 2012. Long-term changes in oxygen depletion in a small temperate lake: effects of climate change and eutrophication: oxygen depletion in a small lake. Freshwater Biology 57: 278–289.

    CAS  Google Scholar 

  • Forsberg, C., 1989. Importance of sediments in understanding nutrient cyclings in lakes. Hydrobiologia 176: 263–277.

    Google Scholar 

  • Fukuhara, H. & M. Sakamoto, 1987. Enhancement of inorganic nitrogen and phosphate release from lake sediment by tubificid worms and chironomid larvae. Oikos 48: 312–320.

    Google Scholar 

  • Galloway, J. N., F. J. Dentener, D. G. Capone, E. W. Boyer, R. W. Howarth, S. P. Seitzinger, G. P. Asner, C. Cleveland, P. Green, E. Holland, et al., 2004. Nitrogen cycles: past, present, and future. Biogeochemistry 70: 153–226.

    CAS  Google Scholar 

  • Granéli, W., 1979. The influence of Chironomus plumosus larvae on the exchange of dissolved substances between sediment and water. Hydrobiologia 66: 149–159.

    Google Scholar 

  • Hansen, K., S. Mouridsen & E. Kristensen, 1998. The impact of Chironomus plumosus larvae on organic matter decay and nutrient (N, P) exchange in a shallow eutrophic lake sediment following a phytoplankton sedimentation. Hydrobiologia 364: 65–74.

    Google Scholar 

  • Hedin, L. O., J. C. von Fischer, N. E. Ostrom, B. P. Kennedy, M. G. Brown & G. P. Robertson, 1998. Thermodynamic constraints on nitrogen transformations and other biogeochemical processes at soil–stream interfaces. Ecology 79: 684–703.

    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.

    Google Scholar 

  • House, W. A. & F. H. Denison, 2002. Total phosphorus content of river sediments in relationship to calcium, iron and organic matter concentrations. Science of The Total Environment 282–283: 341–351.

    PubMed  Google Scholar 

  • Hupfer, M., S. Jordan, C. Herzog, C. Ebeling, R. Ladwig, M. Rothe & J. Lewandowski, 2019. Chironomid larvae enhance phosphorus burial in lake sediments: insights from long-term and short-term experiments. Science of The Total Environment 663: 254–264.

    CAS  PubMed  Google Scholar 

  • Jensen, H., P. Kristensen, E. Jeppesen & A. Skytthe, 1992. Iron/phosphorus ratio in surface sediment as an indicator of phosphate release from aerobic sediments in shallow lakes. Hydrobiologia 235–236: 731–743.

    Google Scholar 

  • Jeppesen, E., M. Sondergaard, J. P. Jensen, K. E. Havens, O. Anneville, L. Carvalho, M. F. Coveney, R. Deneke, M. T. Dokulil, B. Foy, D. Gerdeaux, S. E. Hampton, S. Hilt, K. Kangur, J. Kohler, E. H. H. R. Lammens, T. L. Lauridsen, M. Manca, M. R. Miracle, B. Moss, P. Noges, G. Persson, G. Phillips, R. Portielje, S. Romo, C. L. Schelske, D. Straile, I. Tatrai, E. Willen & M. Winder, 2005. Lake responses to reduced nutrient loading—an analysis of contemporary long-term data from 35 case studies. Freshwater Biology 50: 1747–1771.

    CAS  Google Scholar 

  • Klein, S., 2006. Sediment porewater exchange and solute release during ebullition. Marine Chemistry 102: 60–71.

    CAS  Google Scholar 

  • Krantzberg, G., 1985. The influence of bioturbation on physical, chemical and biological parameters in aquatic environments: a review. Environmental Pollution Series A, Ecological and Biological 39: 99–122.

    CAS  Google Scholar 

  • Kristensen, E., 2000. Organic matter diagenesis at the oxic/anoxic interface in coastal marine sediments, with emphasis on the role of burrowing animals. Hydrobiologia 426: 1–24.

    CAS  Google Scholar 

  • Kristensen, E., G. Penha-Lopes, M. Delefosse, T. Valdemarsen, C. Quintana & G. Banta, 2012. What is bioturbation? The need for a precise definition for fauna in aquatic sciences. Marine Ecology Progress Series 446: 285–302.

    Google Scholar 

  • Lavery, P. S., C. E. Oldham & M. Ghisalberti, 2001. The use of Fick’s First Law for predicting porewater nutrient fluxes under diffusive conditions. Hydrological Processes 15: 2435–2451.

    Google Scholar 

  • Leuchs, H., 1986. Die Schlaengelaktivität von Chironomuslarven (Diptera) aus flachen und tiefen Gewässern und die resultierenden Wasserzirkulationen in Abhängigkeit von Temperatur und Sauerstoffangebot. Archiv für Hydrobiologie 108: 281–299.

    Google Scholar 

  • Lewandowski, J. & M. Hupfer, 2005. Effect of macrozoobenthos on two-dimensional small-scale heterogeneity of pore water phosphorus concentrations in lake sediments: a laboratory study. Limnology and Oceanography 50: 1106–1118.

    CAS  Google Scholar 

  • Lewandowski, J., C. Laskov & M. Hupfer, 2007. The relationship between Chironomus plumosus burrows and the spatial distribution of pore-water phosphate, iron and ammonium in lake sediments. Freshwater Biology 52: 331–343.

    CAS  Google Scholar 

  • Meinikmann, K., M. Hupfer & J. Lewandowski, 2015. Phosphorus in groundwater discharge—a potential source for lake eutrophication. Journal of Hydrology 524: 214–226.

    CAS  Google Scholar 

  • Mermillod-Blondin, F. & R. Rosenberg, 2006. Ecosystem engineering: the impact of bioturbation on biogeochemical processes in marine and freshwater benthic habitats. Aquatic Sciences 68: 434–442.

    CAS  Google Scholar 

  • Mermillod-Blondin, F., G. Fauvet, A. Chalamet & M. C. des Châtelliers, 2001. A comparison of two ultrasonic methods for detaching biofilms from natural substrata. International Review of Hydrobiology 86: 349–360.

    CAS  Google Scholar 

  • Mermillod-Blondin, F., R. Rosenberg, F. François-Carcaillet, K. Norling & L. Mauclaire, 2004. Influence of bioturbation by three benthic infaunal species on microbial communities and biogeochemical processes in marine sediment. Aquatic Microbial Ecology 36: 271–284.

    Google Scholar 

  • Mermillod-Blondin, F., G. Nogaro, T. Datry, F. Malard & J. Gibert, 2005. Do tubificid worms influence the fate of organic matter and pollutants in stormwater sediments? Environmental Pollution 134: 57–69.

    CAS  PubMed  Google Scholar 

  • Mermillod-Blondin, F., G. Nogaro, F. Vallier & J. Gibert, 2008. Laboratory study highlights the key influences of stormwater sediment thickness and bioturbation by tubificid worms on dynamics of nutrients and pollutants in stormwater retention systems. Chemosphere 72: 213–223.

    CAS  PubMed  Google Scholar 

  • Moraes, P. C., M. Zilius, S. Benelli & M. Bartoli, 2018. Nitrification and denitrification in estuarine sediments with tube-dwelling benthic animals. Hydrobiologia 819: 217–230.

    Google Scholar 

  • Mortimer, C. H., 1941. The exchange of dissolved substances between mud and water in lakes. Journal of Ecology 29: 280–329.

    CAS  Google Scholar 

  • Murniati, E., D. Gross, H. Herlina, K. Hancke & A. Lorke, 2017. Effects of bioirrigation on the spatial and temporal dynamics of oxygen above the sediment–water interface. Freshwater Science 36: 784–795.

    Google Scholar 

  • Ni, Z. & S. Wang, 2015. Historical accumulation and environmental risk of nitrogen and phosphorus in sediments of Erhai Lake, Southwest China. Ecological Engineering 79: 42–53.

    Google Scholar 

  • Nogaro, G., A. M. Harris & A. D. Steinman, 2016. Alum application, invertebrate bioturbation, and sediment characteristics interact to affect phosphorus exchange in eutrophic ecosystems. Freshwater Science 35: 597–610.

    Google Scholar 

  • Pelegri, S. & T. H. Blackburn, 1996. Nitrogen cycling in lake sediments bioturbated by Chironomus plumosus larvae, under different degrees of oxygenation. Hydrobiologia 325: 231–238.

    CAS  Google Scholar 

  • Penn, M. R., M. T. Auer, S. M. Doerr, C. T. Driscoll, C. M. Brooks & S. W. Effler, 2000. Seasonality in phosphorus release rates from the sediments of a hypereutrophic lake under a matrix of pH and redox conditions. Canadian Journal of Fisheries and Aquatic Sciences 57: 1033–1041.

    CAS  Google Scholar 

  • Pigneret, M., F. Mermillod-Blondin, L. Volatier, C. Romestaing, E. Maire, J. Adrien, L. Guillard, D. Roussel & F. Hervant, 2016. Urban pollution of sediments: impact on the physiology and burrowing activity of tubificid worms and consequences on biogeochemical processes. Science of The Total Environment 568: 196–207.

    CAS  PubMed  Google Scholar 

  • Qin, L., Q. Zeng, W. Zhang, X. Li, A. D. Steinman & X. Du, 2016. Estimating internal P loading in a deep water reservoir of northern China using three different methods. Environmental Science and Pollution Research 23: 18512–18523.

    CAS  PubMed  Google Scholar 

  • Rapin, A., M. Grybos, M. Rabiet, B. Mourier & V. Deluchat, 2019. Phosphorus mobility in dam reservoir affected by redox oscillations: an experimental study. Journal of Environmental Sciences 77: 250–263.

    Google Scholar 

  • Saaltink, R. M., E. Honingh, S. C. Dekker, J. Griffioen, M. C. van Riel, P. F. M. Verdonschot, J. P. M. Vink, J. C. Winterwerp & M. J. Wassen, 2018. Respiration and aeration by bioturbating Tubificidae alter biogeochemical processes in aquatic sediment. Aquatic Sciences 81: 13.

    Google Scholar 

  • Schindler, D. W., 1974. Eutrophication and recovery in experimental lakes: implications for lake management. Science 184: 897–899.

    CAS  PubMed  Google Scholar 

  • Smith, V. H., 2003. Eutrophication of freshwater and coastal marine ecosystems a global problem. Environmental Science and Pollution Research 10: 126–139.

    CAS  PubMed  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.

    Google Scholar 

  • Stief, P. & D. De Beer, 2006. Probing the microenvironment of freshwater sediment macrofauna: implications of deposit-feeding and bioirrigation for nitrogen cycling. Limnology and Oceanography 51: 2538–2548.

    Google Scholar 

  • Svensson, J. & L. Leonardson, 1996. Effects of bioturbation by tube-dwelling chironomid larvae on oxygen uptake and denitrification in eutrophic lake sediments. Freshwater Biology 35: 289–300.

    Google Scholar 

  • Svensson, J. M., A. Enrich-Prast & L. Leonardson, 2001. Nitrification and denitrification in a eutrophic lake sediment bioturbated by oligochaetes. Aquatic Microbial Ecology 23: 177–186.

    Google Scholar 

  • Tessenow, U., 1972. Lösungs-, diffusions-und sorptionsprozesse in der oberschicht von Seesedimenten. Arch. Hydrobiol. Suppl 38: 353–398.

    Google Scholar 

  • US EPA, 1991. Methods for measuring the acute toxicity of effluents and receiving waters to freshwater and marine organisms. EPA/600/4-90/027.

  • Vitousek, P. M., J. D. Aber, R. W. Howarth, G. E. Likens, P. A. Matson, D. W. Schindler, W. H. Schlesinger & D. G. Tilman, 1997. Human alteration of the global nitrogen cycle: sources and consequences. Ecological Applications 7: 737–750.

    Google Scholar 

  • Vörösmarty, C. J., M. Meybeck, B. Fekete, K. Sharma, P. Green & J. P. M. Syvitski, 2003. Anthropogenic sediment retention: major global impact from registered river impoundments. Global and Planetary Change 39: 169–190.

    Google Scholar 

  • Wetzel, R. G., 2001a. The phosphorus cycle Limnology: lake and river ecosystems. Academic Press, San Diego: 239–288.

    Google Scholar 

  • Wetzel, R. G., 2001b. Oxygen limnology: lake and river ecosystems. Academic Press, San Diego: 239–288.

    Google Scholar 

  • Wetzel, R. G., 2001c. The nitrogen cycle limnology: lake and river ecosystems. Academic Press, San Diego: 205–237.

    Google Scholar 

  • Wood, L. W., 1975. Role of oligochaetes in the circulation of water and solutes across the mud-water interface. SIL Proceedings 1922–2010(19): 1530–1533.

    Google Scholar 

  • Wu, Z., Y. Liu, Z. Liang, S. Wu & H. Guo, 2017. Internal cycling, not external loading, decides the nutrient limitation in eutrophic lake: a dynamic model with temporal Bayesian hierarchical inference. Water Research 116: 231–240.

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank the ANRT (Association Nationale Recherche Technologie) and EDF (Electricité de France) for Edwige Gautreau’s Ph.D. Grant (convention bourse CIFRE- EDF: No. 0733/2016). This study was funded by a partnership between EDF and CNRS (CNRS No. 149389) and by Lyon Metropole though the equipment acquisition on Sedaqua Platform (Contrat Plan Etat Région). This work was performed within the framework of the EUR H2O’Lyon (ANR-17-EURE-0018) of Université de Lyon (UdL), within the program “Investissements d’Avenir” operated by the French National Research Agency (ANR). We are grateful to Félix Vallier, Athos Environnement (Antoine Thouvenot, David Foltier, and Benjamin Legrand), Pierre Rossignol, Laurent Simon, Michel Lafont, and Pierre Marmonier for their support and advice during field and laboratory work. We also wish to thank Jörg Lewandowski and one anonymous referee for their pertinent comments which significantly improved a previous draft of this manuscript.

Funding

This study was funded by the partnership EDF-CNRS (CNRS no. 149389) and Lyon Metropole within the framework of Sedaqua Platform (Contrat Plan Etat Région).

Author information

Authors and Affiliations

  1. Univ Lyon, Université Claude Bernard Lyon 1, CNRS, ENTPE, UMR5023, Écologie des Hydrosystèmes Naturels et Anthropisés, 69622, Villeurbanne, France

    Edwige Gautreau, Laurence Volatier & Florian Mermillod-Blondin

  2. EDF R&D, Laboratoire National d’Hydraulique et Environnement, 6 quai Watier, BP49, 78401, Chatou, France

    Edwige Gautreau, Géraldine Nogaro & Emma Gouze

Authors
  1. Edwige Gautreau
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Laurence Volatier
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Géraldine Nogaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Emma Gouze
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Florian Mermillod-Blondin
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Edwige Gautreau.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Additional information

Handling editor: Andrew Dzialowski

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gautreau, E., Volatier, L., Nogaro, G. et al. The influence of bioturbation and water column oxygenation on nutrient recycling in reservoir sediments. Hydrobiologia 847, 1027–1040 (2020). https://doi.org/10.1007/s10750-019-04166-0

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-019-04166-0

Keywords

Search

Navigation