Hydrobiologia

, Volume 753, Issue 1, pp 47–59 | Cite as

Size-based diel migration of zooplankton in Mediterranean shallow lakes assessed from in situ experiments with artificial plants

  • Ülkü Nihan Tavşanoğlu
  • Sandra Brucet
  • Eti Ester Levi
  • Tuba Bucak
  • Gizem Bezirci
  • Arda Özen
  • Liselotte S. Johansson
  • Erik Jeppesen
  • Meryem Beklioğlu
Primary Research Paper

Abstract

In warm lakes, fish aggregate within macrophytes, thereby weakening the role of these as a daytime refuge for zooplankton and altering the zooplankton size structure, predation pressure, and water clarity. To elucidate the role of macrophytes as a refuge for zooplankton and their effect on zooplankton size distribution, we established three sets of strandardized artificial plant beds in 11 lakes in Turkey with contrasting fish predation risk and turbidity. Zooplankton were sampled within and outside of each plant beds during day and night. Fish, collected overnight in multimesh-sized gillnets, were abundant both inside and outside the artificial plant beds, impoverishing the usefulness of plants as a daytime refuge for particularly large-bodied zooplankton. Zooplankton size diversity was negatively related to fish abundance. Diel vertical migration was the frequent anti-predator avoidance behavior, but reverse migration was also observed when Chaoborus was present. In contrast to the small-bodied taxa, large- and medium-sized taxa showed intraspecific size-based migration (i.e., individuals of different sizes had different migration patterns). Predators influenced the size structure and diel movement of zooplankton, but the response changed with the size of zooplankton and water clarity.

Keywords

Zooplankton community structure Migration Predation size diversity Water clarity 

Supplementary material

10750_2015_2192_MOESM1_ESM.docx (217 kb)
Supplementary material 1 (DOCX 218 kb)

References

  1. Basińska, A., N. Kuczyńska Kippen & K. Świdnicki, 2010. The body size distribution of Filinia longiseta (Ehrenberg) in different types of small water bodies in the Wielkoposka region. Limnetica 29: 171–182.Google Scholar
  2. Bayly, I. A. E., 1986. Aspects of diel vertical migration in zooplankton and its enigma variations. In De Deckker, P. & W. D. Williams (eds), Limnology in Australia. CSIRO, Melbourne: 349–368.CrossRefGoogle Scholar
  3. Blanck, A. & N. Lamouroux, 2007. Large-scale intraspecific variation in life-history traits of European freshwater fish. Journal of Biogeography 34: 862–875.CrossRefGoogle Scholar
  4. Bottrell, H. H., A. Duncan, Z. M. Gliwicz, E. Grygierek, A. Herzig, A. Hillbricht-Ilkowska, H. Kurasawa, P. Larsson & T. Weglenska, 1976. A review of some problems in zooplankton production studies. Norwegian Journal of Zoology 24: 419–456.Google Scholar
  5. Brooks, J. L. & S. I. Dodson, 1965. Predation, body size and composition of plankton. Science 150: 28–35.CrossRefPubMedGoogle Scholar
  6. Brucet, S., D. Boix, R. López-Flores, A. Badosa & X. D. Quintana, 2006. Size and species diversity of zooplankton communities in fluctuating Mediterranean salt marshes. Estuarine Coastal and Shelf Science 67: 424–432.CrossRefGoogle Scholar
  7. Brucet, S., D. Boix, X. D. Quintana, E. Jensen, L. W. Nathansen, C. Trochine, M. Meerhoff, S. Gascón & E. Jeppesen, 2010. Factors influencing zooplankton size structure at contrasting temperatures in coastal shallow lakes: implications for effects of climate change. Limnology and Oceanography 55: 1697–1711.CrossRefGoogle Scholar
  8. Brucet, S., S. Pédron, T. Mehner, T. L. Lauridsen, C. Argillier, I. J. Winfield, P. Volta, M. Emmrich, T. Hesthagen, K. Holmgren, L. Benejam, F. Kelly, T. Krause, A. Palm, M. Rask & E. Jeppesen, 2013. Fish diversity in European lakes: geographical predictors dominate over anthropogenic pressures. Freshwater Biology 58: 1779–1793.CrossRefGoogle Scholar
  9. Burks, R. L., E. Jeppesen & D. M. Lodge, 2001. Pelagic and benthic predators: impacts of odonate predation on Daphnia. Journal of the North American Benthological Society 20: 615–628.CrossRefGoogle Scholar
  10. Burks, R. L., D. M. Lodge, E. Jeppesen & T. L. Lauridsen, 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshwater Biology 47: 343–363.CrossRefGoogle Scholar
  11. Canfield, Jr., D. E., J. V. Shireman, D. E. Colle, W. T. Haller, C. E. Watkins & M. J. Maceina, 1984. Prediction of chlorophyll a concentrations in Florida lakes: importance of aquatic macrophytes. Canadian Journal of Fisheries and Aquatic Sciences 41: 497–501.CrossRefGoogle Scholar
  12. Carl, H. & P. R. Møller, 2012. Atlas over danske ferskvandsfisk (in Danish, Atlas of Danish freshwater fish), 1st ed. Natural History Museum of Denmark, Copenhagen.Google Scholar
  13. Connell, A. D., 1978. Reversed vertical migration of planktonic crustaceans in a eutrophic lake of high pH. Journal of the Limnological Society of Southern Africa 4: 101–104.CrossRefGoogle Scholar
  14. Dodson, S., 1990. Predicting diel vertical migration of zooplankton. Limnology and Oceanography 35: 1195–1200.CrossRefGoogle Scholar
  15. Dodson, S. I., R. Tollrian & W. Lampert, 1997. Daphnia swimming behaviour during vertical migration. Journal of Plankton Research 19: 969–978.CrossRefGoogle Scholar
  16. Dumont, H. J., 1972. A competition based approach of the reversed vertical migration in zooplankton and its implications, chiefly based on a study of the interactions of the rotifer Asplanchna priodonta (Gosse) with several crustacean entomostraca. International Review of Hydrobiology 57: 1–38.CrossRefGoogle Scholar
  17. Dumont, H. J., I. V. de Velde & S. Dumont, 1975. The dry weight estimate of biomass in a selection of Cladocera, Copepoda and Rotifera from the plankton, periphyton and benthos of continental waters. Oecologia 19: 75–97.CrossRefGoogle Scholar
  18. Froese, R. & D. Pauly (eds), 2011. FishBase. World Wide Web Electronic Publication. www.fishbase.org. Accessed June 2013.
  19. Geldiay, R. & S. Balık, 2002. Türkiye Tatlı Su Balıkları: Ders Kitabı. Ege University Fisheries and Aquatic Sciences Publication 46, İzmir: 532 pp.Google Scholar
  20. George, D. G. & I. J. Winfield, 2000. Factors influencing the spatial distribution of zooplankton and fish in Loch Ness, UK. Freshwater Biology 43: 557–570.CrossRefGoogle Scholar
  21. Gliwicz, M. Z., 1986. Predation and the evolution of vertical migration in zooplankton. Nature 320: 746–748.CrossRefGoogle Scholar
  22. Gliwicz, M. Z., A. Biernacka, J. Pijanowska & R. Korsak, 2000. Ontogenetic shifts in the migratory behavior of Chaoborus flavicans MEIGEN: field and experimental evidence. Archiv für Hydrobiologie 149: 193–212.Google Scholar
  23. Hansson, L.-A. & S. Hylander, 2009. Size-structured risk assessments govern Daphnia migration. Proceeding of Royal Society Bulletin 276: 331–336.CrossRefGoogle Scholar
  24. Horppila, J., P. Eloranta, A. Liljendahl-Nurminen, J. Niemistö & Z. Pekcan-Hekim, 2009. Refuge availability and sequence of predators determine the seasonal succession of crustacean zooplankton in a clay-turbid lake. Aquatic Ecology 43: 91–103.CrossRefGoogle Scholar
  25. Hurlbert, S. H., 1971. The Nonconcept of Species Diversity: a Critique and Alternative Parameters. Ecology 52: 577–586.CrossRefGoogle Scholar
  26. Iglesias, C., G. Goyemola, N. Mazzeo, M. Meerhoff, E. Rodo & E. Jeppesen, 2007. Horizontal dynamics of zooplankton in subtropical Lake Blance (Uruguay) hosting multiple zooplankton predators and aquatic plant refuges. Hydrobiologia 584: 179–189.CrossRefGoogle Scholar
  27. Iglesias, C., N. Mazzeo, F. Teixeira de Mello, G. Goyenola, C. Fosalba, S. García & E. Jeppesen, 2008. Field and experimental evidence of the effect of Jenynsia multidentata Jenyns (Cyprinodontiformes, Anablepidae) on the size distribution of zooplankton in subtropical lakes. Freshwater Biology 53: 1797–1807.CrossRefGoogle Scholar
  28. 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(343): 151–164.CrossRefGoogle Scholar
  29. Jeppesen, E., J. P. Jensen, C. Jensen, B. Faafeng, P. Brettum, D. Hessen, M. Søndergaard, T. Lauridsen & K. Christoffersen, 2003. The impact of nutrient state and lake depth on top-down control in the pelagic zone of lakes: study of 466 lakes from the temperate zone to the Arctic. Ecosystems 6: 313–325.CrossRefGoogle Scholar
  30. Jeppesen, E., M. Meerhoff, K. Holmgren, I. González-Bergonzoni, F. Teixeira-de Mello, S. A. J. Declerck, L. De Meester, M. Søndergaard, T. L. Lauridsen, R. Bjerring, J. M. Conde-Porcuna, N. Mazzeo, C. Iglesias, M. Reizenstein, H. Malmquist, L. Zhengwen, D. Balayla & L. Xavier, 2010a. Impacts of climate warming on lake fish community structure and potential ecosystem effects. Hydrobiologia 646: 73–90.CrossRefGoogle Scholar
  31. Jeppesen, E., B. Moss, H. Bennion, L. Carvalho, L. De Mesteer, H. Feuchtmayr, N. Friberg, M. O. Gessner, M. Hefting, T. L. Lauridsen, L. Liboriussen, H. J. Malquist, L. May, M. Meerhoff, J. S. Olafsson, M. B. Soons & J. T. A. Verhoeven, 2010b. Interaction of climate change and eutrophication. In Kernan, M., R. Battarbee & B. Moss (eds), Climate Change Impacts on Freshwater Ecosystems. Blackwell, London: 119–151.CrossRefGoogle Scholar
  32. Jespersen, A. M. & K. Christoffersen, 1987. Measurements of chlorophyll a from phytoplankton using ethanol as extraction solvent. Archiv fr Hydrobiologie 109: 445–454.Google Scholar
  33. Kvam, O. V. & O. T. Kleiven, 1995. Diel horizontal migration and swarm formation in Daphnia in response to Chaoborus. Hydrobiologia 307: 177–184.CrossRefGoogle Scholar
  34. Lagergren, R., K. Leberfinger & J. A. E. Stenson, 2008. Seasonal and ontogenetic variation in diel vertical migration of Chaoborus flavicans and its effect on depth-selection behavior of other zooplankton. Limnology and Oceanography 53: 1083–1092.CrossRefGoogle Scholar
  35. Lampert, W., 1989. The adaptive significance of diel vertical migration of zooplankton. Functional Ecology 3: 21–27.CrossRefGoogle Scholar
  36. Lauridsen, T. L. & I. Buenk, 1996. Diel changes in the horizontal distribution of zooplankton in the littoral zone of two shallow eutrophic lakes. Archiv für Hydrobiologie 137: 167–176.Google Scholar
  37. Lauridsen, T. L. & D. M. Lodge, 1996. Avoidance by Daphnia magna of fish and macrophytes: chemical cues and predator-mediated use of macrophyte habitat. Limnology and Oceanography 41: 794–798.CrossRefGoogle Scholar
  38. Lass, S. & P. Spaak, 2003. Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491: 221–239.CrossRefGoogle Scholar
  39. Lazzaro, X., M. Bouvy, R. A. Ribeiro-Filho, S. O. Vanildo, L. T. Sales, A. R. M. Vasconcelos & M. R. Mata, 2003. Do fish regulate phytoplankton in shallow northeast Brazilian reservoirs? Freshwater Biology 48: 649–668.CrossRefGoogle Scholar
  40. Liljendahl-Nurminen, A., J. Horppila, L. Uusitalo & J. Niemistö, 2008. Spatial variability in the abundance of pelagic invertebrate predators in relation to depth and turbidity. Aquatic Ecology 42: 25–33.CrossRefGoogle Scholar
  41. MacIsaac, H. J. & J. J. Gilbert, 1989. Competition between rotifers and cladocerans of different body sizes. Oecologia 81: 295–301.CrossRefGoogle Scholar
  42. Mackereth, F. G. H., J. Heron & J. F. Talling, 1978. Water Analysis: Some Revised Methods for Limnologists. Freshwater Biological Association 36, Ambleside.Google Scholar
  43. Malley, D. F., S. G. Lawrence, M. A. Maclver & W. J. Findlay, 1989. Range and variation in estimates of dry weight for planktonic Crustacea and Rotifera from temperate North American Lakes. Canadian Technical Report of Fisheries and Aquatic Sciences 1666: 1–49.Google Scholar
  44. McCauley, E., 1984. The estimation of the abundance and biomass of zooplankton in samples. In Downing, J. A. & F. H. Rigler (eds), A Manual on Methods for the Assessment of Secondary Productivity in Freshwaters. Blackwell, Oxford: 228–265.Google Scholar
  45. Meerhoff, M., C. Iglesias, F. Teixeira-de Mello, J. M. Clemente, E. Jensen, T. L. Lauridsen & E. Jeppesen, 2007. Effects of habitat complexity on the community structure and predator avoidance behaviour of littoral zooplankton in temperate versus subtropical shallow lakes. Freshwater Biology 52: 1009–1021.CrossRefGoogle Scholar
  46. Michaloudi, E., 2005. Dry weights of the zooplankton of Lake Mikri Prespa (Macedonia, Greece). Belgian Journal of Zoology 135(2): 223–227.Google Scholar
  47. Muluk, B. Ç. & M. Beklioğlu, 2005. Absence of typical diel vertical migration in Daphnia: varying role of water clarity, food, and dissolved oxygen in Lake Eymir, Turkey. Hydrobiologia 537: 125–133.CrossRefGoogle Scholar
  48. Ohman, M. D., B. W. Frost & E. B. Cohen, 1983. Reverse diel vertical migration: an escape from invertebrate predators. Science 220: 1404–1407.CrossRefPubMedGoogle Scholar
  49. Pekcan-Hekim, Z. & J. Lappalainen, 2006. Effects of clay turbidity and density of pikeperch (Sander lucioperca) larvae on predation by perch (Perca fluviatilis). Naturwissenschaften 93: 356–359.CrossRefPubMedGoogle Scholar
  50. Peel, M. C., B. L. Finlayson & T. A. McMahon, 2007. Updated world map of the Köppen-Geiger climate classification. Hydrology and Earth Systems Sciences 11: 1633–1644.CrossRefGoogle Scholar
  51. Quintana, X. D., S. Brucet, D. Boix, R. Lopez-Flores, S. Gascon, A. Baldosa, J. Sala, R. Moreno-Amich & J. J. Egozcue, 2008. A nonparametric method for the measurement of size diversity with emphasis on data standardization. Limnology and Oceanograpty: Methods 6: 75–86.CrossRefGoogle Scholar
  52. Rejas, D., L. De Meester, L. Ferrufino, M. Maldonado & F. Ollevier, 2007. Diel vertical migration of zooplankton in an Amazonian várzea lake (Laguna Bufeos, Bolivia). Studies on Neotropical Fauna and Envionment 42: 71–81.CrossRefGoogle Scholar
  53. Ruttner-Kolisko, A., 1977. Suggestions for biomass calculations of plankton rotifers. Archiv für Hydrobiologie-Beiheft Ergebnisse der Limnologie 8: 71–76.Google Scholar
  54. Saraoğlu, E., 2012. Impact of water level fluctuations and fish on macroinvertebrate community and periphyton growth in shallow lakes – a mesocosm approach. Dissertation, Middle East Technical University.Google Scholar
  55. Schou, M. O., C. Risholt, T. L. Lauridsen, M. Sondergaard, P. Grondkjaer, L. Jacobsen, S. Berg, C. Skov, S. Brucet & E. Jeppesen, 2009. Restoring lakes by using artificial plant beds: habitat selection of zooplankton in a clear and turbid shallow lake. Freshwater Biology 54: 1520–1531.CrossRefGoogle Scholar
  56. Taşdemir, A., M. R. Ustaoğlu, S. Balık & H. M. Sarı, 2008. Batı Karadeniz Bölgesindeki (Türkiye) Bazı Göllerin Diptera ve Ephemeroptera Faunası. Turkish Journal of Fisheries and Aquatic Sciences 2: 252–465.Google Scholar
  57. Tavşanoğlu, Ü. N., Aİ. Çakıroğlu, Ş. Erdoğan, M. Meerhoff, E. Jeppesen & M. Beklioğlu, 2012. Sediment, not plants, offer the preferred refuge for Daphnia against fish predation in Mediterranean shallow lakes: an experimental demonstration. Freshwater Biology 57: 795–802.CrossRefGoogle Scholar
  58. Teixeira-de Mello, F., M. Meerhoff, Z. Pekcan-Hekim & E. Jeppesen, 2009. Substantial differences in littoral fish community structure and dynamics in subtropical and temperate shallow lakes. Freshwater Biology 54: 1202–1215.CrossRefGoogle Scholar
  59. Thomson, G. A., E. O. Dinofrio & V. A. Alder, 2013. Structure, abundance and biomass size spectra of copepods and other zooplankton communities in upper waters of the Southwestern Atlantic Ocean during summer. Journal of Plankton Research 0: 1–20.Google Scholar
  60. Toksöz, A. & M. R. Ustaoğlu, 2005. Gölcük Gölü’nin (Bozdağ, Ödemiş) Profundan Makrobentik Faunası Üzerine Araştırmalar. Ege Journal of Fisheries and Aquatic Sciences 1–2: 173–175.Google Scholar
  61. Tollrian, R. & Dodson, I. 2009. Inducible defenses in Cladocera: constraints, cost, and multipredator environment. In Tollrien, R. & C. D. Harvell (eds), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton: 383 pp.Google Scholar
  62. Winder, M., M. Boersma & P. Spaak, 2003. On the cost of vertical migration: are feeding conditions really worse at greater depths? Freshwater Biology 48: 383–393.CrossRefGoogle Scholar
  63. Young, J. D. & H. P. Riessen, 2005. The interaction of Chaoborous size and vertical distribution determines predation effects on Daphnia. Freshwater Biology 50: 993–1006.CrossRefGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2015

Authors and Affiliations

  • Ülkü Nihan Tavşanoğlu
    • 1
  • Sandra Brucet
    • 2
    • 3
  • Eti Ester Levi
    • 1
  • Tuba Bucak
    • 1
  • Gizem Bezirci
    • 1
  • Arda Özen
    • 1
    • 4
  • Liselotte S. Johansson
    • 2
  • Erik Jeppesen
    • 2
    • 5
    • 6
  • Meryem Beklioğlu
    • 1
    • 7
  1. 1.Limnology Laboratory, Department of BiologyMiddle East Technical University06800 Çankaya, AnkaraTurkey
  2. 2.Department of Bioscience and the Arctic Centre (ARC)Aarhus University8600 SilkeborgDenmark
  3. 3.Department of Environmental SciencesUniversity of VicVicSpain
  4. 4.Department of Forest EngineeringÇankırı Karatekin University18200 ÇankırıTurkey
  5. 5.Sino-Danish Centre for Education and Research (SDC)BeijingChina
  6. 6.Greenland Climate Research Centre (GCRC)Greenland Institute of Natural Resources3900 NuukGreenland
  7. 7.Kemal Kurdaş Ecological Research and Training Stations, Lake EymirMiddle East Technical University06400 Çankaya, AnkaraTurkey

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