Abstract
Eutrophication of shallow lakes often triggers a series of cascading ecological effects. Among these are shifts in the zooplankton community structure due to phytoplankton changes, or shifts in the fish community reducing size-selective feeding of planktivorous fish. In such conditions, larger zooplankton (e.g. Daphnia) can have a selective advantage. Re-oligotrophication can reverse such food-web interactions. Europe’s largest wetland system (the Danube Delta) went through a period of eutrophication and is now slowly recovering again. However, changes in the Daphnia populations triggered by eutrophication in this system have remained unstudied. We used different sampling strategies to screen 24 lakes (which differ in their ecological state) for the presence of Daphnia as well as for biotic and abiotic parameters potentially explaining Daphnia abundance. Daphnia densities were surprisingly low. We found D. magna ephippia in the sediment, but no D. magna in the water column. Microsatellite analyses on pelagic Daphnia populations confirmed the presence of the D. longispina complex and provided evidence for significant hybridisation events. FluoroProbe data showed that Daphnia was mainly present in lakes with a higher phytoplankton production. Our study provides insights into the spatial and temporal distribution of Daphnia in a very dynamic wetland system.
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References
Benzie, J., 2005. Cladocera: the genus Daphnia (including Daphniopsis), Vol. 21. Kenobi Productions, Backhuys Publishers, Ghent, Leiden.
Brede, N., A. Thielsch, C. Sandrock, P. Spaak, B. Keller, B. Streit & K. Schwenk, 2006. Microsatellite markers for European Daphnia. Molecular Ecology Notes 6: 536–539.
Brede, N., C. Sandrock, D. Straile, T. Jankowski, P. Spaak, B. Streit & K. Schwenk, 2009. The impact of human-made ecological changes on the genetic architecture of Daphnia species. Proceedings of the National Academy of Sciences of the United States of America 106: 4758–4763.
Brönmark, C. & L. A. Hansson, 2010. The Biology of Lakes and Ponds. Oxford University Press, New York.
Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and composition of plankton. Science 150: 28–35.
Brzeziński, T., J. Fronk, J. Trzcińska-Danielewicz & P. Dawidowicz, 2012. Interspecific hybridization in sympatric species of Daphnia inhabiting lakes in northeastern Poland. Oceanological and Hydrobiological Studies 41: 1–6.
Carpenter, S., J. F. Kitchell & J. Hodgson, 1985. Cascading trophic interactions and lake productivity. BioScience 35: 634–639.
Carpenter, S. R. & J. F. Kitchell, 1993. The Throphic Cascade in Lakes. Cambridge Univ. Press, Cambridge.
Catherine, A., N. Escoffier, A. Belhocine, A. B. Nasri, S. Hamlaoui, C. Yepremian, C. Bernard & M. Troussellier, 2012. On the use of the FluoroProbe(R), a phytoplankton quantification method based on fluorescence excitation spectra for large-scale surveys of lakes and reservoirs. Water Resource 46: 1771–1784.
Cottenie, K., E. Michels, N. Nuytten & L. DeMeester, 2003. Zooplankton metacommunity structure: regional vs. local processes in highly interconnected ponds. Ecology 84: 991–1000.
Cremer, H., A. Buijse, A. Lotter, W. Oosterberg & M. Staras, 2004. The palaeolimnological potential of diatom assemblages in floodplain lakes of the Danube Delta, Romania: a pilot study. Hydrobiologia 513: 7–26.
Cristofor, S., A. Vădineanu & G. Ignat, 1993. Importance of flood zones for nitrogen and phosphorus dynamics in the Danube Delta. Hydrobiologia 251: 143–148.
Damian-Georgescu, A., 1963. Fauna Republicii Populare Romane. Crustacea. Copepoda, fam. Cyclopidae (forme de apă dulce), Vol. 4. Academiei Republicii Populare Romane, București.
De Jong, Y. E. A., 2014. Fauna Europaea – all European animal species on the web. Biodiversity Data Journal 2: e4034. https://doi.org/10.3897/BDJ.2.e4034.
DeMott, W. R., 1986. The role of taste in food selection by freshwater zooplankton. Oecologia 69: 334–340.
Fink, P., C. Pflitsch & K. Marin, 2011. Dietary essential amino acids affect the reproduction of the keystone herbivore Daphnia pulex. PLoS ONE 6: e28498.
Galatchi, L.-D. & M. Tudor, 2006. Europe as a source of pollution – the main factor for the eutrophication of the Danube Delta and Black Sea Chemicals as Intentional and Accidental Global Environmental Threats. Springer, New York: 57–63.
Găldean, N. & D. M. Ruști, 2006. The Danube Delta ecosystems. In Tudorancea, C. & M. M. Tudorancea (eds), Danube Delta – Genesis and Biodiversity. Blackhuys Publishers, Leiden: 95–104.
Gâștescu, P., 2009. The Danube Delta biosphere reserve. Geography, biodiversity, protection, management. Revue Roumaine de Géographie 53: 139–152.
Ger, K. A., L.-A. Hansson & M. Lürling, 2014. Understanding cyanobacteria-zooplankton interactions in a more eutrophic world. Freshwater Biology 59: 1783–1798.
Gliwicz, Z. M., 2004. Zooplankton. In O’Sillivan, P. E. & C. S. Reynolds (eds), The Lakes Handbook, Vol. 1. Blackwell Science Ltd, Malden, MA: 461–516.
Hambright, K. D., N. G. Hairston, W. R. Schaffner & R. W. Howarth, 2007. Grazer control of nitrogen fixation: phytoplankton taxonomic composition and ecosystem functioning. Fundamental and Applied Limnology 170: 103–124.
Hülsmann, S., 2003. Recruitment patterns of Daphnia: a key for understanding midsummer declines? Hydrobiologia 491: 35–46.
Jensen, J. P., E. Jeppesen, K. Olrik & P. Kristensen, 1994. Impact of nutrients and physical factors on the shift from cyanobacterial to chlorophyte dominance in shallow Danish Lakes. Canadian Journal of Fisheries and Aquatic Sciences 51: 1692–1699.
Jeppesen, E., T. L. Lauridsen, S. F. Mitchell, K. Christoffersen & C. W. Burns, 2000. Trophic structure in the pelagial of 25 shallow New Zealand lakes: changes along nutrient and fish gradients. Journal of Plankton Research 22: 951–968.
Jombart, T., 2008. adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24: 1403–1405.
Jyrkänkallio-Mikkola, J., S. Meier, J. Heino, T. Laamanen, V. Pajunen, K. T. Tolonen, M. Tolkkinen & J. Soininen, 2017. Disentangling multi-scale environmental effects on stream microbial communities. Journal of Biogeography 44: 1512–1523.
Karabanov, D. P., E. I. Bekker, R. J. Shiel & A. A. Kotov, 2018. Invasion of a Holarctic planktonic cladoceran Daphnia galeata Sars (Crustacea: Cladocera) in the Lower Lakes of South Australia. Zootaxa 4402: 136–148.
Kerfoot, W. C. & A. Sih (eds), 1987. Predation: Direct and Indirect Impacts on Aquatic Communities. Univ. Press of New England, Hanover (NH).
Kreutzer, C. & W. Lampert, 1999. Exploitative competition in differently sized Daphnia species: a mechanistic explanation. Ecology 80: 2348–2357.
Lampert, W., 1987. Feeding and nutrition in Daphnia. In Peters, R. H. & R. De Bernardi (eds), “Daphnia”. Memorie dell’instituto di idrobiologia, Vol. 45. CNR Istituto italiano di idrobiologia, Pallanza: 107–141.
Lampert, W., 2011. Daphnia: development of a model organism in ecology and evolution. In Kinne, O. (ed.), Excellence in Ecology. Oldendorf, Luhe, International Ecology Institute.
Larsson, P. & S. I. Dodson, 1993. Invited review – chemical communication in planktonic animals. Archiv fur Hydrobiologie 129: 129–155.
Lass, S. & P. Spaak, 2003. Chemically induced anti-predator defences in plankton: a review. Hydrobiologia 491: 221–239.
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.
Legendre, P. & L. F. Legendre, 2012. Numerical Ecology, Vol. 24. Elsevier, Amsterdam.
Lubbock, J., 1857. An account of the two methods of reproduction in Daphnia, and of the structure of the ephippium. Philosophical Transactions of the Royal Society of London 147: 79–100.
Masclaux, H., A. Bec, M. J. Kainz, C. Desvilettes, L. Jouve & G. Bourdier, 2009. Combined effects of food quality and temperature on somatic growth and reproduction of two freshwater cladocerans. Limnology and Oceanography 54: 1323–1332.
Moldoveanu, M.-M. & L.-I. Florescu, 2013. Long-term analysis of cyanobacterial blooms in Lake Roşu (Danube Delta). Studii şi comunicări -Ştiinţele Naturii, Muzeul Olteniei Craiova 29: 252–259.
Monchamp, M.-E., I. Enache, P. Turko, F. Pomati, G. Rîșnoveanu & P. Spaak, 2017. Sedimentary and egg-bank DNA from 3 European lakes reveal concurrent changes in the composition and diversity of cyanobacterial and Daphnia communities. Hydrobiologia 800: 155–172.
Montero-Pau, J. & A. Gomez, 2008. Application of an inexpensive and high throughput genomic DNA extraction method for the molecular ecology of zooplanktonic diapausing eggs. Limnology and Oceanography Methods 6: 218–222.
Möst, M. H., 2013. Environmental change and its impact on hybridising Daphnia species complexes. Ph.D., ETH
Müller-Navarra, D. & W. Lampert, 1996. Seasonal patterns of food limitation in Daphnia galeata: separating food quantity and food quality effects. Journal of Plankton Research 18: 1137–1157.
Năstase, A. & I. Năvodaru, 2010. Researches of fish communities from Rosu-Puiu and Matita-Merhei lake-complexes in 2008. Sc Annals of Danube Delta Institute 16: 20–32.
Năvodaru, I., A. D. Buijse & M. Staras, 2000. Fish community structure in lakes of the Danube delta. In Oosterberg, W. (ed.), Ecological Gradients in the Danube Delta Lakes - RIZA rapport 2000015, 119–138.
Negrea, Ș., 1983. Fauna Republicii Socialiste România. Fascicula 12: Cladocera. Academiei Republicii Socialiste România, București.
Oksanen, J., R. Kindt, P. Legendre, B. O’Hara, M. H. H. Stevens, M. J. Oksanen & M. Suggests, 2007. The vegan package. Community Ecology Package 10: 631–637.
Oosterberg, W., M. Staras, L. Bogdan, A. D. Buijse, A. Constantinescu, J. Hanganu, B. W. Ibelings, G. A. M. Menting, I. Nãvodaru & L. Török, 2000. Ecological Gradients in the Danube Delta Lakes: Present State and Man-Induced Changes. RIZA the Netherlands, Danube Delta National Institute Romania and Danube Delta Biosphere Reserve Authority Romania, Lelystad.
Panin, N., 2003. The Danube Delta. Geomorphology and Holocene evolution: a synthesis [Le delta du Danube. Géomorphologie et évolution holocène: une synthèse]. Géomorphologie 9: 247–262.
Piepho, M., D. Martin-Creuzburg & A. Wacker, 2010. Simultaneous effects of light intensity and phosphorus supply on the sterol content of phytoplankton. PLoS ONE 5: e15828.
Pijanowska, J. & G. Stolpe, 1996. Summer diapause in Daphnia as a reaction to the presence of fish. Journal of Plankton Research 18: 1407–1412.
Postolache, C., 2006. The chemistry of the Danube Delta. In Tudorancea, C. & M. M. Tudorancea (eds), Danube Delta – Genesis and Biodiversity. Blackhuys Publishers, Leiden: 65–94.
R Core Team, 2013. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
Rellstab, C., B. Keller, S. Girardclos, F. Anselmetti & P. Spaak, 2011. Anthropogenic eutrophication shapes the past and present taxonomic composition of hybridizing Daphnia in unproductive lakes. Limnology and Oceanography 56: 292–302.
Ringelberg, J., 1991. A mechanism of predator-mediated induction of diel vertical migration in Daphnia hyalina. Journal of Plankton Research 13: 83–89.
Rîșnoveanu, G., C. Postolache & A. Vădineanu, 2004. Ecological significance of nitrogen cycling by tubificid communities in shallow eutrophic lakes of the Danube Delta. Hydrobiologia 524: 193–202.
Rudescu, L., 1960. Fauna Republicii Populare Române, Secțiunea Trochelminthes: Rotatoria, Vol. 2. Editura Academiei Române, Bucuresti.
Seda, J., A. Petrusek, J. Machacek & P. Smilauer, 2007. Spatial distribution of the Daphnia longispina species complex and other planktonic crustaceans in the heterogeneous environment of canyon-shaped reservoirs. Journal of Plankton Research 29: 619–628.
Seidendorf, B., M. Boersma & K. Schwenk, 2007. Evolutionary stoichiometry: the role of food quality for clonal differentiation and hybrid maintenance in a Daphnia species complex. Limnology and Oceanography 52: 385–394.
Sommer, U., Z. M. Gliwicz, W. Lampert & A. Duncan, 1986. The PEG-model of seasonal succession of planktonic events in fresh waters. Archiv fur Hydrobiologie 106: 433–471.
Spaak, P. & J. R. Hoekstra, 1995. Life history variation and the coexistence of a Daphnia hybrid with its parental species. Ecology 76: 553–564.
Spaak, P. & J. R. Hoekstra, 1997. Fish predation on a Daphnia hybrid species complex: a factor explaining species coexistence? Limnology and Oceanography 42: 753–762.
Spaak, P., J. Fox & N. Hairston, 2012. Modes and mechanisms of a Daphnia invasion. Proceedings of the Royal Society B Biological Sciences 279: 2936–2944.
Spandl, H., 1926. Wissenschaftliche Forschungsegebnisse aus dem Gebiete der unteren Donau und des Schwarzen Meeres. II Die Süßwaßer-Mikrofauna. Archiv für Hydrobiologie 16: 528–604.
StatSoft, I., 2011. STATISTICA (Data Analysis Software System), Version 10. [available on internet at www.statsoft.com] Tulsa, OK.
Tillmanns, A. R., A. E. Wilson, F. R. Pick & O. Sarnelle, 2008. Meta-analysis of cyanobacterial effects on zooplankton population growth rate: species-specific responses. Fundamental and Applied Limnology 171: 285–295.
Toonen, R. J. & S. Hughes, 2001. Increased throughput for fragment analysis on an ABI Prism® 377 automated sequencer using a membrane comb and STRand software. BioTechniques 31: 1320–1324.
Török, L., 2005. Seasonal succesion of phytoplankton from lakes of the Danube Delta. Acta Oecologica XII: 15–23.
Török, L., 2008. Phytoplankton blooms of the Danube Delta Biosphere Reserve. Contributii Botanice XLIII: 85–90.
Török, L., 2011. The trend of phytoplankton development in Danube Delta’s lakes. Sc Annals of Danube Delta Institute 17: 89–98.
Török, L. & A. Radu, 2007. The analysis of the records of zooplankton species from the Danube Delta Biosphere Reserve. Scientific Annals of DDI 13: 111–122.
Tudor, M., I. M. Tudor, O. Ibram, B. Alexandrov & N. Racovet, 2014. Evolution of zooplankton community structure in the Danube Delta region. Journal of Environmental Protection and Ecology 15: 506–516.
Tudorancea, M. M., 2006. Human presence in the Danube Delta. In Tudorancea, C. & M. M. Tudorancea (eds), Danube Delta – Genesis and Biodiversity. Blackhuys Publishers, Leiden: 399–410.
Vandekerkhove, J., S. Declerck, M. Vanhove, L. Brendonck, E. Jeppesen, J. M. Conde-Porcuna & L. De Meester, 2004. Use of ephippial morphology to assess richness of anomopods: potentials and pitfalls. Journal of Limnology 63: 75–84.
Wolf, H. G. & M. A. Mort, 1986. Interspecific hybridization underlies phenotypic variability in Daphnia populations. Oecologia 68: 507–511.
Xu, S., K. Spitze, M. S. Ackerman, Z. Ye, L. Bright, N. Keith, C. E. Jackson, J. R. Shaw & M. Lynch, 2015. Hybridization and the origin of contagious asexuality in Daphnia pulex. Molecular Biology and Evolution 32: 3215–3225.
Zaffagnini, F., 1988. Reproduction in Daphnia. In Peters, R. H. & R. de Bernardi (eds), Daphnia. Memorie dell’instituto di idrobiologia. CNR Istituto italiano di idrobiologia, Pallanza: 245–284.
Zinevici, V. & L. Parpală, 2007. Zooplanctonul din Delta Dunării și Avandeltă – Diversitate, Structură, Productivitate și Relații Trofice. ArsDocendi, București.
Acknowledgements
This work was supported by the Swiss Enlargement Contribution, Project IZERZ0 – 142165, “CyanoArchive”, in the framework of the Romanian-Swiss Research Program. We are thankful to Esther Keller who helped in the lab, Nadine Tardent who assisted with scoring the microsatellites and Darmina Niță for assisting with part of the statistics. We also thank Doru Simon Dobre, Aurel Damian, Vanea Dunaev, Laurentiu Butâlchin, Silviu Perijoc, Emilia Radu and Ciprian Birsan who helped with the fieldwork. We thank Georgia Lavinia Cosor for providing helpful information about surfaces and shore lengths of Danube Delta lakes areas and Christoph Tellenbach for helpful discussions. We also thank 3 anonymous reviewers for their helpful and constructive comments.
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Enache, I., Florescu, L.I., Moldoveanu, M. et al. Diversity and distribution of Daphnia across space and time in Danube Delta lakes explained by food quality and abundance. Hydrobiologia 842, 39–54 (2019). https://doi.org/10.1007/s10750-019-04025-y
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DOI: https://doi.org/10.1007/s10750-019-04025-y