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Water level and fish-mediated cascading effects on the microbial community in eutrophic warm shallow lakes: a mesocosm experiment

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Abstract

Information on the effects of water level changes on microbial planktonic communities in lakes is limited but vital for understanding ecosystem dynamics in Mediterranean lakes subjected to major intra- and inter-annual variations in water level. We performed an in situ mesocosm experiment in an eutrophic Turkish lake at two different depths crossed with presence/absence of fish in order to explore the effects of water level variations and the role of top-down regulation at contrasting depths. Strong effects of fish were found on zooplankton, weakening through the food chain to ciliates, HNF and bacterioplankton, whereas the effect of water level variations was overall modest. Presence of fish resulted in lower biomass of zooplankton and higher biomasses of phytoplankton, ciliates and total plankton. The cascading effects of fish were strongest in the shallow mesocosms as evidenced by a lower zooplankton contribution to total plankton biomass and lower zooplankton:ciliate and HNF:bacteria biomass ratios. Our results suggest that a lowering of the water level in warm shallow lakes will enhance the contribution of bacteria, HNF and ciliates to the plankton biomass, likely due to increased density of submerged macrophytes (less phytoplankton); this effect will, however, be less pronounced in the presence of fish.

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References

  • Andersen, T. & D. O. Hessen, 1991. Carbon, nitrogen and phosphorus content of freshwater zooplankton. Limnology and Oceanography 36: 807–814.

    Article  CAS  Google Scholar 

  • Auer, B., U. Elzer & H. Arndt, 2004. Comparison of pelagic food webs in lakes along a trophic gradient and with seasonal aspects: influence of resource and predation. Journal of Plankton Research 26: 697–709.

    Article  Google Scholar 

  • Beklioğlu, M. & C. O. Tan, 2008. Restoration of a shallow Mediterranean lake by biomanipulation complicated by drought. Fundamental and Applied Limnology 171: 105–118.

    Article  Google Scholar 

  • Beklioğlu, M., Ö. İnce & İ. Tüzün, 2003. Restoration of eutrophic Lake Eymir, Turkey, by biomanipulation undertaken following a major external nutrient control I. Hydrobiologia 489: 93–105.

    Article  Google Scholar 

  • Beklioğlu, M., G. Altinayar & C. O. Tan, 2006. Water level control over submerged macrophyte development in five shallow lakes of Mediterranean Turkey. Archiv für Hydrobiologie 166: 535–556.

    Article  Google Scholar 

  • Beklioğlu, M., S. Romo, I. Kagalou, X. Quintana & E. Becares, 2007. State of the art in the functioning of shallow Mediterranean lakes: workshop conclusions. Hydrobiologia 584: 317–326.

    Article  Google Scholar 

  • Biddanda, B., M. Ogdahl & J. Cotner, 2001. Dominance of bacterial metabolism in oligotrophic relative to eutrophic waters. Limnology and Oceanography 46: 730–739.

    Article  Google Scholar 

  • Borsheim, K. Y. & G. Bratback, 1987. Cell volume to carbon conversion factors for bacterivorous Monas sp. enriched from seawater. Marine Ecology Progress Series 36: 171–175.

    Article  Google Scholar 

  • Bratbak, G. & I. Dundas, 1984. Bacterial dry matter content and biomass estimations. Applied and Environmental Microbiology 48: 755–757.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Bucak, T., E. Saraoğlu, E. E. Levi, Ü. N. Tavşanoğlu, Aİ. Çakiroğlu, E. Jeppesen & M. Beklioğlu, 2012. The influence of water level on macrophyte growth and trophic interactions in eutrophic Mediterranean shallow lakes: a mesocosm experiment with and without fish. Freshwater Biology 57: 1631–1642.

    Article  Google Scholar 

  • Carrick, H. J., G. L. Fahnenstiel, E. F. Stoermer & R. G. Wetzel, 1991. The importance of zooplankton–protozoan trophic couplings in Lake Michigan. Limnology and Oceanography 36: 1335–1345.

    Article  Google Scholar 

  • Christoffersen, K., B. Riemann, A. Klysner & M. Søndergaard, 1993. Potential role of natural populations of zooplankton on plankton community structure in eutrophic lake water. Limnology and Oceanography 38: 561–573.

    Article  Google Scholar 

  • Coops, H., M. Beklioğlu & T. L. Crisman, 2003. The role of water-level fluctuations in shallow lake ecosystems: workshop conclusions. Hydrobiologia 506: 23–27.

    Article  Google Scholar 

  • Cotner, J. B. & B. A. Biddanda, 2002. Small players, large role: microbial influence on biogeochemical processes in pelagic aquatic ecosystem. Ecosystems 5: 105–121.

    Article  CAS  Google Scholar 

  • Farjalla, V. F., D. A. Azevedo, F. A. Esteves, R. L. Bozelli, F. Roland & A. Enrich-Prast, 2006. Influence of hydrological pulse on bacterial growth and DOC uptake in a clear-water Amazonian lake. Microbial Ecology 52: 334–344.

    Article  PubMed  Google Scholar 

  • Foissner, W. & H. Berger, 1996. A user-friendly guide to the ciliates (Protozoa, Ciliophora) commonly used by hydrobiologists as bioindicators in rivers, lakes, and waste waters, with notes on their ecology. Freshwater Biology 35: 375–482.

    Google Scholar 

  • Foissner, W., H. Berger & J. Schaumburg, 1999. Identification and Ecology of Limnetic Plankton Ciliates. Informations berichte des Bayer. Landesamtes für Wasserwirtschaft. 3, 793 pp.

  • Fonte, E. S., L. S. Carneiro, A. Caliman, R. L. Bozelli, F. D. A. Esteves & V. F. Farjalla, 2011. Effects of resources and food web structure on bacterioplankton production in a tropical humic lagoon. Journal of Plankton Research 33: 1596–1605.

    Article  Google Scholar 

  • Gaedke, U. & D. Straile, 1994. Seasonal changes of the quantitative importance of protozoans in a large lake: an ecosystem approach using mass-balanced carbon flow diagrams. Marine Microbial Food Webs 8: 163–188.

    Google Scholar 

  • Gafny, S., A. Gasith & M. Goren, 1992. Effect of water level fluctuation on shore spawning of Mirogrex terraesanctae (Steinitz), Cyprinidae in Lake Kinneret, Israel. Journal of Fish Biology 41: 863–871.

    Article  Google Scholar 

  • Gasol, J. M. & C. M. Duarte, 2000. Comparative analyses in aquatic microbial ecology: how far do they go? FEMS Microbiology Ecology 31: 99–106.

    Article  PubMed  CAS  Google Scholar 

  • Havens, K. E., B. Sharfstein, M. A. Brady, T. L. East, M. C. Harwell, R. P. Maki & A. J. Rodusky, 2004. Recovery of submerged plants from high water stress in a large subtropical Lake in Florida, USA. Aquatic Botany 78: 67–82.

    Article  Google Scholar 

  • Jeppesen, E., Ma Søndergaard, Mo Søndergaard, K. Christoffersen, K. Jürgens, J. Theil-Nielsen & L. Schlüter, 2002. Cascading trophic interactions in the littoral zone: an enclosure experiment in shallow Lake Stigsholm, Denmark. Archiv für Hydrobiologie 153: 533–555.

    Google Scholar 

  • Jeppesen, E., B. Kronvang, M. Meerhoff, M. Søndergaard, K. M. Hansen, H. E. Andersen, T. L. Lauridsen, L. Liboriussen, M. Beklioğlu, A. Özen & J. E. Olesen, 2009. Climate change effects on runoff, catchment phosphorus loading and lake ecological state, and potential adaptations. Journal of Environmental Quality 38: 1930–1941.

    Article  PubMed  CAS  Google Scholar 

  • Jeppesen, E., B. Kronvang, J. E. Olesen, M. Søndergaard, C. C. Hoffmann, H. E. Andersen, T. L. Lauridsen, L. Liboriussen, S. Larsen, M. Beklioğlu, M. Meerhoff, A. Özen & K. Özkan, 2011. Climate change effect on nitrogen loading from catchment in Europe: implications for nitrogen retention and ecological state of lakes and adaptations. Hydrobiologia 663: 1–21.

    Article  CAS  Google Scholar 

  • Jürgens, K. & E. Jeppesen, 2000. The impact of metazooplankton on the structure of the microbial food web in a shallow, hypertrophic lake. Journal of Plankton Research 22: 1047–1070.

    Article  Google Scholar 

  • Jürgens, K., H. Arndt & K. O. Rothhaupt, 1994. Zooplankton-mediated changes of bacterial community structure. Microbial Ecology 27: 27–42.

    Article  PubMed  Google Scholar 

  • Leira, M. & M. Cantonati, 2008. Effects of water-level fluctuations on lakes: an annotated bibliography. Hydrobiologia 613: 171–184.

    Article  Google Scholar 

  • Markosova, R. & J. Jezek, 1993. Bacterioplankton interactions with daphnia and algae in experimental enclosures. Hydrobiologia 264: 85–99.

    Article  Google Scholar 

  • Müller-Solger, A., M. T. Brett, C. Luecke, J. J. Elser & C. R. Goldman, 1997. The effects of planktivorous fish (golden shiners) on the ciliate community of a mesotrophic lake. Journal of Plankton Research 12: 1815–1828.

    Article  Google Scholar 

  • Muylaert, K., K. Van der Gucht, N. Vloemans, L. De Meester, M. Gillis & W. Vyverman, 2002. Relationship between bacterial community composition and bottom-up versus top-down variables in four eutrophic shallow lakes. Applied Environmental Microbiology 68: 4740–4750.

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Naselli-Flores, L., 2003. Man-made lakes in Mediterranean semi-arid climate: the strange case of Dr Deep Lake and Mr Shallow Lake. Hydrobiologia 506: 13–21.

    Article  Google Scholar 

  • Nishimura, Y., T. Ohtsuka, K. Yoshiyama, D. Nakai, F. Shibahara & M. Maehata, 2011. Cascading effects of larval Crucian carp introduction on phytoplankton and microbial communities in a paddy field: top-down and bottom-up controls. Ecological Research 26: 615–626.

    Article  Google Scholar 

  • Nixdorf, B. & H. Arndt, 1993. Seasonal dynamics of plankton component including the microbial web in Lake Müggelsee. Internationale Revue gesamten Hydrobiologie 78: 403–410.

    Article  Google Scholar 

  • Nõges, P., T. Nõges & A. Laas, 2010. Climate-related changes of phytoplankton seasonalityin large shallow Lake Võrtsjärv, Estonia. Aquatic Ecosystem Health & Management 13: 154–163.

    Article  Google Scholar 

  • Pace, M. L. & J. J. Cole, 1994. Comparative and experimental approaches to top down and bottom up regulation of bacteria. Microbial Ecology 28: 181–193.

    Article  PubMed  CAS  Google Scholar 

  • Pace, M. L. & E. Funke, 1991. Regulation of planktonic microbial communities by nutrients and herbivores. Ecology 73: 904–914.

    Article  Google Scholar 

  • Porter, K. G. & Y. S. Feig, 1980. The use of DAPI for identifying and counting aquatic microflora. Limnology and Oceanography 25: 943–948.

    Article  Google Scholar 

  • Putt, M. & D. K. Stoecker, 1989. An experimentally determined carbon:carbon:volume ratio for marine oligotrichous ciliates from estuarine and coastal waters. Limnology and Oceanography 34: 1097–1103.

    Article  Google Scholar 

  • Reynolds, C. S., 1984. The Ecology of Freshwater Phytoplankton. Cambridge University Press, Cambridge: 384.

    Google Scholar 

  • Riemann, B., 1985. Potential importance of fish predation and zooplankton grazing on natural populations of freshwater bacteria. Applied and Environmental Microbiology 50: 187–193.

    PubMed  CAS  PubMed Central  Google Scholar 

  • Roozen, F. C. J. M., M. Lürling, H. Vlek, E. A. J. V. P. Kraan, B. W. Ibelings & M. Scheffer, 2007. Resuspension of algal cells by benthivorous fish boosts phytoplankton biomass and alters community structure in shallow lakes. Freshwater Biology 52: 977–987.

    Article  CAS  Google Scholar 

  • Özen, A., B. Karapinar, I. Küçük, E. Jeppesen & M. Beklioğlu, 2010. Drought-induced changes in nutrient concentrations and retention in two shallow Mediterranean lakes subjected to different degrees of management. Hydrobiologia 646: 61–72.

    Article  Google Scholar 

  • Özkan, K., E. Jeppesen, L. S. Johansson & M. Beklioğlu, 2010. The response of periphyton and submerged macrophytes to nitrogen and phosphorus loadings in shallow warm lakes: a mesocosm experiment. Freshwater Biology 55: 463–475.

    Article  Google Scholar 

  • Saad, J. F., M. R. Schiaffino, A. Vinocur, I. O’Farrell, G. Tell & I. Izaguirre, 2013. Microbial planktonic communities of freshwater environments from Tierra del Fuego: dominant trophic strategies in lakes with contrasting features. Journal of Plankton Research 35: 1220–1233.

    Article  CAS  Google Scholar 

  • Stanley, E. H., M. D. Johnson & A. K. Ward, 2003. Evaluating the influence of macrophytes on algal and bacterial production in multiple habitats of a freshwater wetland. Limnology and Oceanography 48: 1101–1111.

    Article  CAS  Google Scholar 

  • Tan, C. & M. Beklioğlu, 2006. Modelling complex nonlinear responses of shallow lakes to fish and hydrology using artificial neural networks. Ecological Modelling 196: 183–194.

    Article  Google Scholar 

  • Tzaras, A., F. R. Pick, A. Mazumder & D. R. S. Lean, 1999. Effects of nutrients, planktivorous fish and water column depth on components of the microbial food web. Aquatic Microbial Ecology 19: 67–80.

    Article  Google Scholar 

  • Utermöhl, H., 1958. Zur Vervollkommnung der quantitativen Phytoplankton Methodik. Mitteilungen-Internationale Vereinigung Theoretische und Angewandte Limnologie 9: 1–38.

    Google Scholar 

  • Vanni, M. J., 2002. Nutrient cycling by animals in freshwater ecosystems. Annual Review of Ecology and Systematics 33: 341–370.

    Article  Google Scholar 

  • Vanni, M. J. & C. D. Layne, 1997. Nutrient recycling and herbivory as mechanisms in the “top-down” effect of fish on algae in lakes. Ecology 78: 21–40.

    Google Scholar 

  • Weisse, T., 1991. The annual cycle of heterotrophic freshwater nanoflagellates: role of bottom-up versus top-down control. Journal of Plankton Research 13: 167–185.

    Article  Google Scholar 

  • Wetzel, R. G. & M. Søndergaard, 1998. Role of submerged macrophytes for the microbial community and dynamics of dissolved organic carbon in aquatic ecosystems. In Jeppesen, E., M. Søndergaard, M. Søndergaard & K. Christoffersen (eds), The Structuring Role of Submerged Macrophytes in Lakes. Springer, New York: 133–148.

    Chapter  Google Scholar 

  • Wickham, S. A., 1998. The direct and indirect impact of Daphnia and Cyclops on a freshwater microbial food web. Journal of Plankton Research 20: 739–755.

    Article  Google Scholar 

  • Wilcock, R. J., P. D. Champion, J. W. Nagels & G. F. Croker, 1999. The influence of aquatic macrophytes on the hydraulic and physico-chemical properties of a New Zealand lowland stream. Hydrobiologia 416: 203–214.

    Article  CAS  Google Scholar 

  • Yamazaki, M., T. Ohtsuka, Y. Kusuoka, M. Maehata, H. Obayashi, K. Imai, F. Shibahara & M. Kimura, 2010. The impact of nigorobuna crucian carp larvae/fry stocking and rice-straw application on the community structure of aquatic organisms in Japanese rice fields. Fisheries Science 76: 207–217.

    Article  CAS  Google Scholar 

  • Zhang, Y., X. Liu, M. Wang & B. Qin, 2013. Compositional differences of chromophoric dissolved organic matter derived from phytoplankton and macrophytes. Organic Geochemistry 55: 26–37.

    Article  Google Scholar 

  • Zingel, P. & T. Nõges, 2008. Protozoan grazing in shallow macrophyte and plankton lakes. Fundamental and Applied Limnology 171: 15–25.

    Article  Google Scholar 

  • Zöllner, E., B. Santer, M. Boersma, H. G. Hoppe & K. Jürgens, 2003. Cascading predation effects of Daphnia and copepods on microbial foodweb components. Freshwater Biology 48: 2174–2193.

    Article  Google Scholar 

  • Zöllner, E., H. G. Hoppe, U. Sommer & K. Jürgens, 2009. Effect of zooplankton mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnology and Oceanography 54: 262–275.

    Article  Google Scholar 

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Acknowledgments

This study and Arda Özen were supported by a Middle East Technical University grant from the METU-BAP programme of Turkey (BAP-07-02-2009), the METU-DPT ÖYP programme of Turkey (BAP-08-11-DP T-2002-K120510) and by TUBITAK-ÇAYDAĞ (Project nos: 105Y332, 109Y181 and 110Y125). During the writing phase, support was given by FP7-ENV-2009-1, REFRESH (Adaptive strategies to Mitigate the Impacts of Climate Change on European Freshwater Ecosystems, Contract No: 244121) and 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 (http://www.mars-project.eu). TB was supported by the TÜBİTAK 2211 Scholarship programme during her graduate study; JC is supported by the TÜBİTAK 2215 Scholarship programme; EEL, ÜNT and AİC were also supported by TÜBITAK ÇAYDAĞ (Project nos: 105Y332 and 110Y125), and EJ was supported by CLEAR (a Villum Kann Rasmussen Centre of Excellence project) and by The Research Council for Nature and Universe, Denmark (272-08-0406), CIRCE and CRES. We also want to thank Gizem Bezirci, Merve Tepe, Betül Acar, Nergis İrem Ertan, Mert Elverici and Soner Oruç for their great efforts during the fieldwork. We thank Anne Mette Poulsen for valuable editorial assistance. This study was a part of the PhD dissertation of Arda Özen at the Middle East Technical University.

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Authors and Affiliations

  1. Department of Forest Engineering, Cankiri Karatekin University, 18200, Çankırı, Turkey

    Arda Özen

  2. Department of Biology, Faculty of Science, Atatürk University, 25400, Erzurum, Turkey

    Arda Özen

  3. Limnology Laboratory, Department of Biology, Middle East Technical University, Üniversiteler Mahallesi, Dumlupınar Bulvarı, Çankaya, 06800, Ankara, Turkey

    Arda Özen, Tuba Bucak, Ülkü Nihan Tavşanoğlu, Ayşe İdil Çakıroğlu, Eti Ester Levi, Jan Coppens & Meryem Beklioğlu

  4. Department of Bioscience and the Arctic Centre (ARC), Aarhus University, Vejlsøvej 25, 8600, Silkeborg, Denmark

    Erik Jeppesen

  5. Greenland Climate Research Centre (GCRC), Greenland Institute of Natural Resources, Kivioq 2, P.O. Box 570, 3900, Nuuk, Greenland

    Erik Jeppesen

  6. Sino-Danish Centre for Education and Research (SDC), Beijing, China

    Erik Jeppesen

  7. Kemal Kurdaş Ecological Research and Training Stations, Lake Eymir, Middle East Technical University, Oran Mahallesi, Çankaya, 06400, Ankara, Turkey

    Meryem Beklioğlu

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  1. Arda Özen
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  2. Tuba Bucak
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  3. Ülkü Nihan Tavşanoğlu
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  6. Jan Coppens
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  7. Erik Jeppesen
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  8. Meryem Beklioğlu
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Correspondence to Arda Özen or Meryem Beklioğlu.

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Özen, A., Bucak, T., Tavşanoğlu, Ü.N. et al. Water level and fish-mediated cascading effects on the microbial community in eutrophic warm shallow lakes: a mesocosm experiment. Hydrobiologia 740, 25–35 (2014). https://doi.org/10.1007/s10750-014-1934-1

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