Oecologia

, Volume 150, Issue 4, pp 668–681

Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming

Global change and conservation ecology

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.

Keywords

Microzooplankton Baltic Sea spring assemblages Climate change Plankton mesocosms Global change 

References

  1. Beaugrand G (2004) Monitoring marine plankton ecosystems. 1: description of an ecosystem approach based on plankton indicators. Mar Ecol Prog Ser 269:69–81Google Scholar
  2. Beaugrand G, Brander KM, Lindley JA, Souissi S, Reid PC (2003) Plankton effect on cod recruitment in the North Sea. Nature 426:661–664PubMedCrossRefGoogle Scholar
  3. 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 93–96Google Scholar
  4. 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 147:1017–1032CrossRefGoogle Scholar
  5. Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167Google Scholar
  6. 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 43:458–464Google Scholar
  7. Cushing DH (1975) Marine ecology and fisheries. Cambridge University Press, London, p 292Google Scholar
  8. Cushing DH (1989) A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified. J Plankton Res 11:1–13Google Scholar
  9. Fenchel T, Finlay BJ (1983) Respiration rates in heterotrophic, free-living protozoa. Microb Ecol 9:99–122CrossRefGoogle Scholar
  10. 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, MünchenGoogle Scholar
  11. 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 34:247–261Google Scholar
  12. Gifford DJ (1985) Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida). Mar Ecol Prog Ser 23:257–267Google Scholar
  13. 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 239:57–68Google Scholar
  14. Greve W, Reiners F (1995) Biocoenotic process patterns in the German Bight. Olsen and Olsen, Fredensborg, pp 67–72Google Scholar
  15. 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 58:274–288CrossRefGoogle Scholar
  16. Hays GC, Richardson AJ, Robinson C (2005) Climate change and marine plankton. Trends Ecol Evol 20:337–344PubMedCrossRefGoogle Scholar
  17. Hillebrand H, Duerselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424CrossRefGoogle Scholar
  18. IPCC (2001) Impacts, adaptations and vulnerability (UNEP and WHO). Climate Change 2001Google Scholar
  19. Irigoien X, Huisman J, Harris RP (2004) Global biodiversity patterns of marine phytoplankton and zooplankton. Nature 429:863–867PubMedCrossRefGoogle Scholar
  20. Irigoien X, Flynn KJ, Harris RP (2005) Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? J Plankton Res 27:313–321CrossRefGoogle Scholar
  21. 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 158:75–86Google Scholar
  22. 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 26:67–80CrossRefGoogle Scholar
  23. 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 1:45–57CrossRefGoogle Scholar
  24. Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33:265–277Google Scholar
  25. Kahl A (1932) Urtiere oder Protozoa I. Wimpertiere oder Ciliata (Infusoria). In: Dahl F (ed) Tierwelt Deutschlands und der angrenzenden Meeresteile 18:1–886Google Scholar
  26. Kivi K, Setaelae O (1995) Simultaneous measurement of food particle selection and clearance rates of planktonic oligotrich ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 119:1–3Google Scholar
  27. 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 38:893–905Google Scholar
  28. 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 136:1–3Google Scholar
  29. Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol Prog Ser 99:1–2Google Scholar
  30. Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507CrossRefGoogle Scholar
  31. Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288CrossRefGoogle Scholar
  32. 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 255:55–78Google Scholar
  33. 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 50:2567–2582CrossRefGoogle Scholar
  34. Montagnes DJS (1996) Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium. Mar Ecol Prog Ser 130:1–3Google Scholar
  35. Montagnes DJS, Lessard EJ (1999) Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms. Aquat Microb Ecol 20:167–181Google Scholar
  36. Montagnes DJS, Weisse T (2000) Fluctuating temperatures affect growth and production rates of planktonic ciliates. Aquat Microb Ecol 21:97–102Google Scholar
  37. 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 99:21–30CrossRefGoogle Scholar
  38. Mueller H (1989) The relative importance of different ciliate taxa in the pelagic food web of Lake Constance. Microb Ecol 18:261–273CrossRefGoogle Scholar
  39. Mueller H, Geller W (1993) Maximum growth rates of aquatic ciliated protozoa: the dependence on body size and temperature reconsidered. Arch Hydrobiol 126:315–327Google Scholar
  40. Mueller H, Schlegel A (1999) Responses of three freshwater planktonic ciliates with different feeding modes to cryptophyte and diatom prey. Aquat Microb Ecol 17:49–60Google Scholar
  41. Mueller H, Schone A, Pintocoelho RM, Schweizer A, Weisse T (1991) Seasonal succession of ciliates in Lake Constance. Microb Ecol 21:119–138CrossRefGoogle Scholar
  42. 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 221:77–91Google Scholar
  43. Nielsen TG, Kioerboe T, Bjoernsen PK (1990) Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar Ecol Prog Ser 62:1–2Google Scholar
  44. 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 158:249–266CrossRefGoogle Scholar
  45. Peters HP, Downing JA (1984) Empirical analysis of zooplankton filtering and feeding rates. Limnol Oceanogr 29:763–784CrossRefGoogle Scholar
  46. Posch T et al (1999) Predator-induced changes of bacterial size-structure and productivity studied on an experimental microbial community. Aquat Microb Ecol 18:235–246Google Scholar
  47. Putt M, Stoecker DK (1989) An experimentally determined carbon: volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34:1097–1103Google Scholar
  48. Scheffer M, Straile D, Van Nes EH, Hosper H (2001) Climatic warming causes regime shifts in lake food webs. Limnol Oceanogr 46:1780–1783CrossRefGoogle Scholar
  49. Setaelae O, Kivi K (2003) Planktonic ciliates in the Baltic Sea in summer: distribution, species association and estimated grazing impact. Aquat Microb Ecol 32:287–297Google Scholar
  50. Shannon C, Weaver W (1963) The mathematical theory of communication. University of Illinois Press, UrbanaGoogle Scholar
  51. Sherr BF, Sherr EB, McDaniel J (1992) Effect of protistan grazing on the frequency of dividing cells in bacterioplankton assemblages. Appl Environ Microbiol 58:2381–2385PubMedGoogle Scholar
  52. 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 22:43–56Google Scholar
  53. Smetacek V (1981) Annual cycle of protozooplankton in the Kiel Bight. Mar Biol 63:1–11CrossRefGoogle Scholar
  54. Smol JP et al (2005) Climate-driven regime shifts in the biological communities of arctic lakes. Proc Natl Acad Sci USA 102:4397–4402PubMedCrossRefGoogle Scholar
  55. Sommer U (1996) Plankton ecology: the past two decades of progress. Naturwissenschaften 63:293–301Google Scholar
  56. 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 142:274–283PubMedCrossRefGoogle Scholar
  57. 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)Google Scholar
  58. Stoecker DK, Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J Plankton Res 12:891–908Google Scholar
  59. 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 6:663–670CrossRefGoogle Scholar
  60. Strom SL, Brainard MA, Holmes JL, Olson MB (2001) Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters. Mar Biol 138:355–368CrossRefGoogle Scholar
  61. 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
  62. Sverdrup H (1953) On conditions for the vernal blooming of phytoplankton. J Cons Explor Mer 18:287–295Google Scholar
  63. Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168PubMedCrossRefGoogle Scholar
  64. 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 28:361–373CrossRefGoogle Scholar
  65. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Limnol 9:1–38Google Scholar
  66. Walther GR et al (2002) Ecological responses to recent climate change. Nature 416:389–395PubMedCrossRefGoogle Scholar
  67. Weisse T, Montagnes DJS (1998) Effect of temperature on inter- and intraspecific isolates of Urotricha (Prostomatida, Ciliophora). Aquat Microb Ecol 15:285–291Google Scholar
  68. Weisse T, Mueller H (1998) Planktonic protozoa and the microbial food web in Lake Constance. Arch Hydrobiol 53:223–254Google Scholar
  69. 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 26:167–179Google Scholar
  70. Wiltshire KH, Lampert W (1999) Urea excetion by Daphnia: a kairomone for colony formation in Scenedesmus? Limnol Oceanogr 44:1894–1903CrossRefGoogle Scholar
  71. Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgol Mar Res 58:269–273CrossRefGoogle Scholar
  72. Winder M, Schindler DE (2004) Climate change uncouples trophic interactions in an aquatic ecosystem. Ecology 85:2100–2106Google Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.IFM-GEOMAR Leibniz Institute of Marine SciencesKielGermany

Personalised recommendations