Abstract
This study aimed at simulating different degrees of winter warming and at assessing its potential effects on ciliate succession and grazing-related patterns. By using indoor mesocosms filled with unfiltered water from Kiel Bight, natural light and four different temperature regimes, phytoplankton spring blooms were induced and the thermal responses of ciliates were quantified. Two distinct ciliate assemblages, a pre-spring and a spring bloom assemblage, could be detected, while their formation was strongly temperature-dependent. Both assemblages were dominated by Strobilidiids; the pre-spring bloom phase was dominated by the small Strobilidiids Lohmaniella oviformis, and the spring bloom was mainly dominated by large Strobilidiids of the genus Strobilidium. The numerical response of ciliates to increasing food concentrations showed a strong acceleration by temperature. Grazing rates of ciliates and copepods were low during the pre-spring bloom period and high during the bloom ranging from 0.06 (Δ0°C) to 0.23 day−1 (Δ4°C) for ciliates and 0.09 (Δ0°C) to 1.62 day−1 (Δ4°C) for copepods. During the spring bloom ciliates and copepods showed a strong dietary overlap characterized by a wide food spectrum consisting mainly of Chrysochromulina sp., diatom chains and large, single-celled diatoms.
Similar content being viewed by others
References
Beaugrand G (2004) Monitoring marine plankton ecosystems. 1: description of an ecosystem approach based on plankton indicators. Mar Ecol Prog Ser 269:69–81
Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664
Behrends G (1996) Long-term investigation of seasonal mesozooplankton dynamics in Kiel Bight. In: Proceedings of the 13th Symposium of the Baltic Marine Biologists, pp 93–96
Berninger UG, Wickham S (2005) Resonse of microbial food web to manipulation of nutrients and grazers in the oligotrophic Gulf of Aqaba and northern Red Sea. Mar Biol 147:1017–1032
Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167
Christaki U, Dolan JR, Pelegri S, Rassoulzadegan F (1998) Consumption of picoplankton-size particles by marine ciliates: effects of physiological state of the ciliate and particle quality. Limnol Oceanogr 43:458–464
Cushing DH (1975) Marine ecology and fisheries. Cambridge University Press, London, p 292
Cushing DH (1989) A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J Plankton Res 11:1–13
Fenchel T, Finlay BJ (1983) Respiration rates in heterotrophic, free-living protozoa. Microb Ecol 9:99–122
Foissner W, Berger H, Kohmann F (1991, 1992, 1994, 1995) Taxonomische und ökologische Revision der Ciliaten des Saprobiensystems Band I–IV, Informationsberichte Bayerisches Landesamt für Wasserwirtschaft, München
Gaedke U, Wickham SA (2004) Ciliate dynamics in response to changing biotic and abiotic conditions in a large, deep lake (Lake Constance). Aquat Microb Ecol 34:247–261
Gifford DJ (1985) Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida). Mar Ecol Prog Ser 23:257–267
Granéli E, Turner JT (2002) Top-down regulation in ctenophore-copepod-ciliate-diatom-phytoflagellate communities in coastal waters: a mesocosm study. Mar Ecol Prog Ser 239:57–68
Greve W, Reiners F (1995) Biocoenotic process patterns in the German Bight. Olsen and Olsen, Fredensborg, pp 67–72
Greve W, Reiners F, Nast J, Hoffmann S (2004) Helgoland Roads meso- and macrozooplankton time-series 1974–2004: lessons from 30 years of single spot, high frequency sampling at the only off-shore island in the North Sea. Helgol Mar Res 58:274–288
Hays GC, Richardson AJ, Robinson C (2005) Climate change and marine plankton. Trends Ecol Evol 20:337–344
Hillebrand H, Duerselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424
IPCC (2001) Impacts, adaptations and vulnerability (UNEP and WHO). Climate Change 2001
Irigoien X, Huisman J, Harris RP (2004) Global biodiversity patterns of marine phytoplankton and zooplankton. Nature 429:863–867
Irigoien X, Flynn KJ, Harris RP (2005) Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? J Plankton Res 27:313–321
Jakobsen HH, Hansen PJ (1997) Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum—a comparative study. Mar Ecol Prog Ser 158:75–86
Johansson M, Gorokhova E, Larsson U (2004) Annual variability in ciliate community structure, potential prey and predators in the open northern Baltic Sea proper. J Plankton Res 26:67–80
John U, Tillmann U, Medlin LK (2002) A comparative approach to study inhibition of grazing and lipid composition of a toxic and non-toxic clone of Chrysochromulina polyepsis (Prymnesiophyceae). Harmful Algae 1:45–57
Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33:265–277
Kahl A (1932) Urtiere oder Protozoa I. Wimpertiere oder Ciliata (Infusoria). In: Dahl F (ed) Tierwelt Deutschlands und der angrenzenden Meeresteile 18:1–886
Kivi K, Setaelae O (1995) Simultaneous measurement of food particle selection and clearance rates of planktonic oligotrich ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 119:1–3
Kivi K, Kaitala S, Kuosa H, Kuparinen J, Leskinen E, Lignell R, Marcussen B, Tamminen T (1993) Nutrient limitation and grazing control of the Baltic plankton community during annual succession. Limnol Oceanogr 38:893–905
Kivi K, Kuosa H, Tanskanen S (1996) An experimental study on the role of crustacean and microprotozoan grazers in the planktonic food web. Mar Ecol Prog Ser 136:1–3
Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol Prog Ser 99:1–2
Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507
Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288
Leppaenen JM, Bruun JE (1988) Cycling of organic matter during the vernal growth period in the open northern Baltic proper. 4. Ciliate and mesozooplankton species composition, biomass, food intake, respiration, and production. Finn Mar Res 255:55–78
McGowan JA, Bograd SJ, Lynn RJ, Miller AJ (2003) The biological response to the 1977 regime shift in the California Current. Deep Sea Res Part II 50:2567–2582
Montagnes DJS (1996) Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium. Mar Ecol Prog Ser 130:1–3
Montagnes DJS, Lessard EJ (1999) Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms. Aquat Microb Ecol 20:167–181
Montagnes DJS, Weisse T (2000) Fluctuating temperatures affect growth and production rates of planktonic ciliates. Aquat Microb Ecol 21:97–102
Montagnes DJS, Lynn DH, Roff JC, Taylor WD (1988) The annual cycle of heterotrophic planktonic ciliates in the waters surrounding the Isles of Shoals, Gulf of Maine: an assessment of their trophic role. Mar Biol 99:21–30
Mueller H (1989) The relative importance of different ciliate taxa in the pelagic food web of Lake Constance. Microb Ecol 18:261–273
Mueller H, Geller W (1993) Maximum growth rates of aquatic ciliated protozoa: the dependence on body size and temperature reconsidered. Arch Hydrobiol 126:315–327
Mueller H, Schlegel A (1999) Responses of three freshwater planktonic ciliates with different feeding modes to cryptophyte and diatom prey. Aquat Microb Ecol 17:49–60
Mueller H, Schone A, Pintocoelho RM, Schweizer A, Weisse T (1991) Seasonal succession of ciliates in Lake Constance. Microb Ecol 21:119–138
Nejstgaard JC, Hygum BH, Naustvoll LJ, Bamstedt U (2001) Zooplankton growth, diet and reproductive success compared in simultaneous diatom- and flagellate-microzooplankton-dominated plankton blooms. Mar Ecol Prog Ser 221:77–91
Nielsen TG, Kioerboe T, Bjoernsen PK (1990) Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar Ecol Prog Ser 62:1–2
Olsson P, Graneli E, Carlsson P, Abreu P (1992) Structuring of a postspring phytoplankton community by manipulation of trophic interactions. J Exp Mar Biol Ecol 158:249–266
Peters HP, Downing JA (1984) Empirical analysis of zooplankton filtering and feeding rates. Limnol Oceanogr 29:763–784
Posch T et al (1999) Predator-induced changes of bacterial size-structure and productivity studied on an experimental microbial community. Aquat Microb Ecol 18:235–246
Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34:1097–1103
Scheffer M, Straile D, Van Nes EH, Hosper H (2001) Climatic warming causes regime shifts in lake food webs. Limnol Oceanogr 46:1780–1783
Setaelae O, Kivi K (2003) Planktonic ciliates in the Baltic Sea in summer: distribution, species association and estimated grazing impact. Aquat Microb Ecol 32:287–297
Shannon C, Weaver W (1963) The mathematical theory of communication. University of Illinois Press, Urbana
Sherr BF, Sherr EB, McDaniel J (1992) Effect of protistan grazing on the frequency of dividing cells in bacterioplankton assemblages. Appl Environ Microbiol 58:2381–2385
Simek K, Juergens K, Nedoma J, Comerma M, Armengol J (2000) Ecological role and bacterial grazing of Halteria spp.: small freshwater oligotrichs as dominant pelagic ciliate bacterivores. Aquat Microb Ecol 22:43–56
Smetacek V (1981) Annual cycle of protozooplankton in the Kiel Bight. Mar Biol 63:1–11
Smol JP et al (2005) Climate-driven regime shifts in the biological communities of arctic lakes. Proc Natl Acad Sci USA 102:4397–4402
Sommer U (1996) Plankton ecology: the past two decades of progress. Naturwissenschaften 63:293–301
Sommer U, Hansen T, Blum O, Holzner N, Vadstein O, Stibor H (2005) Copepod and microzooplankton grazing in mesocosms fertilised with different Si:N ratios: no overlap between food spectra and Si:N influence on zooplankton trophic level. Oecologia 142:274–283
Sommer U, Aberle N, Engel A, Hansen T, Lengfellner K, Sandow M, Wohlers J, Zoellner E, Riebesell U (2006) An indoor mesocosm system to study the effect of climate change on the late winter and spring succession of Baltic Sea phyto- and zooplankton. Oecologia (in press)
Stoecker DK, Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J Plankton Res 12:891–908
Straile D, Adrian R (2000) The North Atlantic Oscillation and plankton dynamics in two European lakes—two variations on a general theme. Global Change Biol 6:663–670
Strom SL, Brainard MA, Holmes JL, Olson MB (2001) Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Mar Biol 138:355–368
Strüder-Kypke MC, Kypke ER, Agatha S, Warwick J, Montagnes DJS (2002) Guide to UK coastal planktonic ciliates (http://www.liv.ac.uk/ciliate/site/index.htm). Copyright © 2002 David Montagnes, The University of Liverpool, Port Erin Marine Laboratory, Port Erin, Isle of Man, British Isles
Sverdrup H (1953) On conditions for the vernal blooming of phytoplankton. J Cons Explor Mer 18:287–295
Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168
Tirok K, Gaedke U (2006) Spring weather determines the relative importance of ciliates, rotifers and crustaceans for the initiation of the clear-water phase in a large, deep lake. J Plankton Res 28:361–373
Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Limnol 9:1–38
Walther GR et al (2002) Ecological responses to recent climate change. Nature 416:389–395
Weisse T, Montagnes DJS (1998) Effect of temperature on inter- and intraspecific isolates of Urotricha (Prostomatida, Ciliophora). Aquat Microb Ecol 15:285–291
Weisse T, Mueller H (1998) Planktonic protozoa and the microbial food web in Lake Constance. Arch Hydrobiol 53:223–254
Weisse T, Karstens N, Meyer VCL, Janke L, Lettner S, Teichgraber K (2001) Niche separation in common prostome freshwater ciliates: the effect of food and temperature. Aquat Microb Ecol 26:167–179
Wiltshire KH, Lampert W (1999) Urea excetion by Daphnia: a kairomone for colony formation in Scenedesmus? Limnol Oceanogr 44:1894–1903
Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgol Mar Res 58:269–273
Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106
Acknowledgments
We would like to thank Thomas Hansen, Sandra Schröder and Christine Rautenstrauch for the maintenance of the mesocosms and for their technical support. The participants of the Kiel Plankton Mesocosm Cluster are thanked for the joint experimental activities. We thank Karen Wiltshire and three anonymous reviewers for the valuable and constructive comments on an earlier version of the manuscript. This study was part of the project SO 145/23-1 within the DFG priority program 1162 AQUASHIFT, and we are grateful for the funding. This study complies with the current German law.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by Roland Brandl.
Priority programme of the German Research Foundation—contribution 4.
Rights and permissions
About this article
Cite this article
Aberle, N., Lengfellner, K. & Sommer, U. Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming. Oecologia 150, 668–681 (2007). https://doi.org/10.1007/s00442-006-0540-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00442-006-0540-y