Skip to main content
SpringerLink
Log in

Interclonal variation in diel horizontal migration behaviour of the water flea Daphnia magna—searching for a signature of adaptive evolution

  • CLADOCERA
  • Published:
Hydrobiologia Aims and scope Submit manuscript

Abstract

In shallow temperate lakes, zooplankton populations may exhibit diel horizontal migration (DHM) and move towards macrophytes during the day to avoid fish. Using a natural Daphnia magna population, we undertook an experimental investigation aimed to describe the genetic variation for DHM and to study whether an adaptive micro-evolutionary response occurred to changes in macrophyte coverage and fish predation pressure through time. Twenty-seven D. magna clones were hatched from ephippia in the sediment of shallow Lake Ring, Denmark. This lake was eutrophied during the 20th century and was subject to restoration measures in the 1970s. The DHM behaviour of the clones was observed both in the presence and absence of fish kairomone. Significant interclonal variation in DHM behaviour occurred in both treatments. To study the micro-evolutionary response of the Lake Ring D. magna population, two approaches were used. First, we compared the DHM behaviour of clones derived from ephippia collected at different depths. A comparison was conducted between clones resurrected from the period of eutrophication (1960–1980) and from the period of recovery (1986–2000). A significant treatment (presence and absence of fish kairomone) × period interaction effect was identified, suggesting a significant micro-evolutionary response for DHM behaviour. The D. magna clones exhibited a significantly stronger horizontal migration response during the period of eutrophication than in the recovery phase. Second, clonal means, representing the influence of the genotype on the trait, were correlated with environmental conditions (macrophyte cover, fish predation pressure and Secchi depth). The results of this analysis also suggest that a micro-evolutionary response by Daphnia has occurred in reaction to changes in fish predation pressure. In periods with high fish predation pressure, Daphnia migrated more strongly towards the plants.

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

  • Amsinck, S., E. Jeppesen & F. Landkildehus, 2005. Relationships between environmental variables and zooplankton subfossils in the surface sediments of 36 shallow coastal brackish lakes with special emphasis on the role of fish. Journal of Paleolimnology 33: 39–51.

    Article  Google Scholar 

  • Appleby, P. G. & F. Oldfield, 1978. The calculation of 210Pb dates assuming a constant rate of supply of unsupported 210Pb to the sediment. Catena 5: 1–8.

    Article  CAS  Google Scholar 

  • Appleby, P. G., P. J. Nolan, D. W. Gifford, M. J. Godfrey, F. Oldfield, N. J. Anderson & R. W. Battarbee, 1986. 210Pb dating by low background gamma-counting. Hydrobiologia 141: 21–27.

    Article  Google Scholar 

  • Benzie, J. A. H., 2005. Cladocera: the genus Daphnia (including Daphniopsis). Backhuys Publishers, Leiden.

    Google Scholar 

  • Berg, S., E. Jeppesen, M. Søndergaard & E. Mortensen, 1994. Environmental effects of introducing whitefish, Coregonus lavaretus (L.) in Lake Ring. Hydrobiologia 275/376: 71–79.

    Article  Google Scholar 

  • Boersma, M., P. Spaak & L. De Meester, 1998. Predator-mediated plasticity in morphology, life history and behavior of Daphnia: the uncoupling of responses. American Naturalist 152: 237–248.

    Article  PubMed  CAS  Google Scholar 

  • Boersma, M., L. De Meester & P. Spaak, 1999. Environmental stress and local adaptation in Daphnia magna. Limnology and Oceanography 44: 393–402.

    Google Scholar 

  • Brendonck, L. & L. De Meester, 2003. Egg banks in freshwater zooplankton: evolutionary and ecological archives in the sediment. Hydrobiologia 491: 65–84.

    Article  Google Scholar 

  • Brooks, J. L., 1957. The systematics of North American Daphnia. Conneticut Academy of Arts and Science. New Haven, USA.

    Google Scholar 

  • Burks, R. L., E. Jeppesen & D. M. Lodge, 2000. Chemicals from macrophytes and fishes suppress Daphnia growth and alter life history traits. Oikos 88: 139–147.

    Article  CAS  Google Scholar 

  • Burks, R. L., E. Jeppesen & D. M. Lodge, 2001. Littoral zone structure as Daphnia refugia against fish predators. Limnology and Oceanography 46: 230–237.

    Google Scholar 

  • Burks, R. L., D. M. Lodge & E. Jeppesen, 2002. Diel horizontal migration of zooplankton: costs and benefits of inhabiting the littoral. Freshwater Biology 47: 343–365.

    Article  Google Scholar 

  • Cerbin, S., D. J. Baylayla & W. J. Van de Bund, 2003. Small-scale distribution and diel vertical migration of zooplankton in a shallow lake (Lake Naardermeer, The Netherlands). Hydrobiologia 491: 111–117.

    Article  Google Scholar 

  • Cousyn, C., L. De Meester, J. K. Colbourne, L. Brendonck, D. Verschuren & F. Volckaert, 2001. Rapid evolution of predator-induced avoidance behavior in a natural zooplankton population. Proceedings of the National Academy of Science 98: 6256–6260.

    Article  CAS  Google Scholar 

  • Cushing, D. H., 1951. The vertical migration of planktonic Crustacea. Biological Reviews of the Cambridge Philosophical Society 26: 158–192.

    Google Scholar 

  • Davies, J., 1985. Evidence for a diurnal horizontal migration in Daphnia hyalina lacustris Sars. Hydrobiologia 120: 103–105.

    Article  Google Scholar 

  • De Meester, L., 1993. Genotype, fish-mediated chemicals and phototaxis in Daphnia. Ecology 74: 1467–1474.

    Article  Google Scholar 

  • De Meester, L. & H. De Jager, 1993. Hatching of Daphnia sexual eggs. I. Intraspecific differences in the hatching responses of D. magna eggs. Freshwater Biology 30: 219–226.

    Article  Google Scholar 

  • De Meester, L., L. J. Weider & Tollrian, 1995. Alternative antipredator defenses and genetic polymorphism in a pelagic predator-prey system. Nature 378: 483–485.

    Article  Google Scholar 

  • De Meester, L., 1996a. Evolutionary potential and local genetic differentiation in a phenotypically plastic trait of a cyclical parthenogen, Daphnia magna. Evolution 50: 1293–1298.

    Article  Google Scholar 

  • De Meester, L., 1996b. Local genetic differentiation and adaptation in freshwater zooplankton populations: patterns and processes. Ecoscience 3: 385–399.

    Google Scholar 

  • De Meester, L., P. Dawidowicz, E. Van Gool & C. J. Loose, 1999. Ecology and evolution of predator-induced behavior in zooplankton: depth selection behavior and diel vertical migration. In R. Tollrian & C. D. Harvell (eds), The Ecology and Evolution of Inducible Defenses. Princeton University Press, Princeton, 160–176.

    Google Scholar 

  • Endler, J. A., 1986. Natural selection in the wild. Princeton University Press, Princeton, New Jersey.

    Google Scholar 

  • Falconer, D. C. & T. F. C. Mackay, 1996. Introduction to quantitative genetics, IVth ed. Longman, London.

    Google Scholar 

  • Flößner, D., 2000. Die Haplopoda und Cladocera (ohne Bosminidae) Mitteleuropas. Backhuys Publishers, Leiden, The Netherlands.

    Google Scholar 

  • Gliwicz, Z. M. & J. Pijanowska, 1986. The role of predation in zooplankton succession. In Sommer U. (ed.), Plankton Ecology: Succession in Plankton Communities. Springer-Verlag, Heidelberg.

    Google Scholar 

  • Hairston, N. G., Jr., W. Lampert, C. E. Cáceres, C. L. Holtmeier, L. J. Weider, U. Gaedke, J. M. Fisher, J. A. Fox & D. M. Post, 1999. Rapid evolution revealed by dormant eggs. Nature 15: 446.

    Article  Google Scholar 

  • Haney, J. F., 1988. Diel patterns of zooplankton behavior. Bulletin of Marine Science 43: 583–603.

    Google Scholar 

  • Haney, J. F., 1993. Environmental control of diel vertical migration behaviour. Archiv für Hydrobiologie Beiheifte Ergebnisse der Limnologie 39: 1–17.

    Google Scholar 

  • Hebert, P. D. N., 1995. The Daphnia of North-America: an illustrated fauna (on CD-rom). CyberNatural Software, Guelphe, Ontario, Canada.

    Google Scholar 

  • Jeppesen, E., 1998. The ecology of shallow lakes—trophic interactions of the pelagical. Doctor’s dissertation, National Environmental Report No. 247, 37–39.

  • Jeppesen, E., J. P. Jensen, M. Søndergaard, T. Lauridsen & F. Landkildehus, 2000. Trophic structure, species richness and biodiversity in Danish lakes: changes along a phosphorus gradient. Freshwater Biology 45: 201–213.

    Article  CAS  Google Scholar 

  • Jeppesen, E., P. Leavitt, L. De Meester & J. P. Jensen, 2001. Functional ecology and palaeolimnology: using cladoceran remains to reconstruct anthropogenic impact. Trends in Ecology and Evolution 16: 191–198.

    Article  PubMed  Google Scholar 

  • Jeppesen, E., J. P. Jensen, S. Amsinck, F. Landkildehus, T. Lauridsen & S. F. Mitchell, 2002. Reconstructing the historical changes in Daphnia mean size and planktivorous fish abundance in lakes from the size of Daphnia ephippia in the sediment. Journal of paleolimnology 27: 133–143.

    Article  Google Scholar 

  • Johansson, L. S., S. L. Amsinck, R. Bjerring & E. Jeppesen, 2005. Mid- to late-Holocene land-use change and development at Lake Dallund, Denmark: trophic structure inferred from cladoceran subfossils. The Holocene, 15: 1–9.

    Article  Google Scholar 

  • Kerfoot, W. C., J. A. Robbins & L. J. Weider, 1999. A new approach to historical reconstruction: combining descriptive and experimental paleolimnology. Limnology and Oceanography 44: 1232–1247.

    Google Scholar 

  • Kvam, O. V. & O. T. Kleiven, 1995. Diel horizontal migration and swarm formation in Daphnia in response to Chaoborus. Hydrobiologia 307: 177–184.

    Article  Google Scholar 

  • Lampert, W., 1987. Predictability in lake ecosystems: the role of biotic interactions. In Schultze E. D & H. Zwölfer (eds), Ecological Studies. Springer-Verlag, Berlin Heidelberg, 333–346.

    Google Scholar 

  • 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: 161–176.

    Google Scholar 

  • 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.

    Article  Google Scholar 

  • Lauridsen, T. L., L. Pedersen, E. Jeppesen & M. Søndergaard, 1996. The importance of macrophyte bed size for cladoceran composition and horizontal migration in a shallow lake. Journal of Plankton Research 18: 2283–2294.

    Article  Google Scholar 

  • Lynch, M., 1984. The limits to life history in Daphnia. Evolution 38:465–482.

    Article  Google Scholar 

  • Pennak, R. W., 1966. Structure of zooplankton populations in the littoral macrophyte zone some Colorado lakes. Transactions of the American Microscopical Society 85: 329–349.

    Article  Google Scholar 

  • Pulido, F. & P. Berthold, 2004. Microevolutionary response to climate change. Birds and Climate change in Ecological Research 35: 151–183.

    Article  Google Scholar 

  • Ringelberg, J., 1991. Enhancement of the phototactic reaction in Daphnia hyalina by a chemical mediated by juvenile perch (Perca fluviatilis). Journal of Plankton Research 13: 17–25.

    Article  Google Scholar 

  • Ringelberg, J., 1999. The photobehaviour of Daphnia spp. as a model to explain diel vertical migration in zooplankton. Biological Reviews of the Cambridge Philosophical Society 74: 397–423.

    Article  Google Scholar 

  • Scheffer, M., S. H. Hosper, M.-L. Meijer, Moss B. & E. Jeppesen, 1993. Alternative equilibria in shallow lakes. Trends in Ecology and Evolution 8:275–279.

    Article  Google Scholar 

  • Schlaepfer, M., M. C. Runge & P. W. Sherman, 2002. Ecological and evolutionary traps. Trends in Ecology and Evolution 17: 474–480.

    Article  Google Scholar 

  • Schwartz, S. S. & P. Hebert, 1987. Methods for activation of the resting eggs of Daphnia. Freshwater Biology 17: 373–379.

    Article  Google Scholar 

  • Sokal, R. & F. J. Rohlf, 1995. Biometry, 3rd ed. Freeman, New York.

    Google Scholar 

  • Statsoft, 1994. STATISTICA for the windows operating system. Inc. Tulsa, UK.

  • Stockwell, C. A., A. P. Hendry & M. T. Kinnison, 2003. Contemporary evolution meets conservation biology. Trends in Ecology and Evolution 18: 94–101.

    Article  Google Scholar 

  • Timms, R. M. & B. Moss, 1984. Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing in the presence of zooplanktivorous fish, in a freshwater wetland ecosystem. Limnology and Oceanography 29: 472–486.

    Google Scholar 

  • Van De Meutter, F., R. Stoks & L. De Meester, 2005. Spatial avoidance of littoral and pelagic invertebrate predators by Daphnia. Oecologia 142: 489–499.

    Article  PubMed  Google Scholar 

  • Van Gool, E. & J. Ringelberg, 1995. Swimming of Daphnia galeata x hyalina in response to changing light intensities: influence of food availability and predator kairomone. Marine and Freshwater Behaviour and Physiology 26: 259–265.

    Article  Google Scholar 

  • Weider, L. J., 1984. Spatial heterogeneity of Daphnia genotypes: vertical migration and habitat partitioning. Limnology and Oceanography 29: 225–235.

    Article  Google Scholar 

Download references

Acknowledgements

Special thanks go to Liselotte Sander Johansson and Rikke Bjerring Hansen for identification of cladoceran remains and to Anne Mette Poulsen for manuscript editing. We also thank three anonymous reviewers for constructive comments. This study was financially supported by the project OT/00/14 of the K. U. Leuven research fund and by the EU IP project EUROLIMPACS (GOCE-CT-2003-505540). H. M. is a fellow of the Institute for the Promotion of Innovation through Science and Technology in Flanders. E. J. and S. L. A. were also supported by the Danish lake restoration project CLEAR.

Author information

Authors and Affiliations

  1. Laboratory of Aquatic Ecology, Katholieke Universiteit Leuven, Ch. Debériotstraat 32, Leuven, 3000, Belgium

    Helen Michels & Luc De Meester

  2. Department of Freshwater Ecology, National Environmental Research Institute, Vejlsøvej 25, Silkeborg, 8600, Denmark

    Susanne Lildal Amsinck & Erik Jeppesen

  3. Department of Plant Biology, University of Aarhus, Ole Worms Allé, Building 135, Aarhus C, 8000, Denmark

    Erik Jeppesen

Authors
  1. Helen Michels
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Susanne Lildal Amsinck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Erik Jeppesen
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Luc De Meester
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Helen Michels.

Additional information

Guest editor: Piet Spaak

Cladocera: Proceedings of the 7th International Symposium on Cladocera

Rights and permissions

Reprints and permissions

About this article

Cite this article

Michels, H., Amsinck, S.L., Jeppesen, E. et al. Interclonal variation in diel horizontal migration behaviour of the water flea Daphnia magna—searching for a signature of adaptive evolution. Hydrobiologia 594, 117–129 (2007). https://doi.org/10.1007/s10750-007-9086-1

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10750-007-9086-1

Keywords

Search

Navigation