Advertisement

Marine Biology

, Volume 158, Issue 7, pp 1551–1580 | Cite as

The role of ciliates, heterotrophic dinoflagellates and copepods in structuring spring plankton communities at Helgoland Roads, North Sea

  • Martin G. J. Löder
  • Cédric Meunier
  • Karen H. Wiltshire
  • Maarten Boersma
  • Nicole Aberle
Original Paper

Abstract

Mesocosm experiments coupled with dilution grazing experiments were carried out during the phytoplankton spring bloom 2009. The interactions between phytoplankton, microzooplankton and copepods were investigated using natural plankton communities obtained from Helgoland Roads (54°11.3′N; 7°54.0′E), North Sea. In the absence of mesozooplankton grazers, the microzooplankton rapidly responded to different prey availabilities; this was most pronounced for ciliates such as strombidiids and strobilids. The occurrence of ciliates was strongly dependent on specific prey and abrupt losses in their relative importance with the disappearance of their prey were observed. Thecate and athecate dinoflagellates had a broader food spectrum and slower reaction times compared with ciliates. In general, high microzooplankton potential grazing impacts with an average consumption of 120% of the phytoplankton production (Pp) were measured. Thus, the decline in phytoplankton biomass could be mainly attributed to an intense grazing by microzooplankton. Copepods were less important phytoplankton grazers consuming on average only 47% of Pp. Microzooplankton in turn contributed a substantial part to the copepods’ diets especially with decreasing quality of phytoplankton food due to nutrient limitation over the course of the bloom. Copepod grazing rates exceeded microzooplankton growth, suggesting their strong top-down control potential on microzooplankton in the field. Selective grazing by microzooplankton was an important factor for stabilising a bloom of less-preferred diatom species in our mesocosms with specific species (Thalassiosira spp., Rhizosolenia spp. and Chaetoceros spp.) dominating the bloom. This study demonstrates the importance of microzooplankton grazers for structuring and controlling phytoplankton spring blooms in temperate waters and the important role of copepods as top-down regulators of microzooplankton.

Keywords

Phytoplankton Dinoflagellate Spring Bloom Grazing Rate Grazing Impact 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

Notes

Acknowledgments

This study was part of a PhD thesis within the Food Web Project at the Alfred Wegener Institute for Polar and Marine Research and we are grateful for the funding. Special thanks to Prof. Ulrich Sommer, Thomas Hansen and Sebastian Meyer at the IFM-GEOMAR (Kiel) for providing us the “Copacabana” light control programme and who helped us in words and deeds. Many thanks to the technical department of the BAH for all the perfect “short notice” solutions and to Arne Malzahn for his technical support. Special thanks also to the “Copepod Hunter” Katherina Schoo for catching and sorting out all the copepods for our experiments. Furthermore, thanks to the crews of the research vessels Uthörn and Aade, Kristine Carstens, Silvia Peters and the whole team of the AWI Food Web Project. Last but not least many thanks for the comments of three anonymous reviewers which helped us a lot for improving this manuscript.

References

  1. Aberle N, Lengfellner K, Sommer U (2007) Spring bloom succession, grazing impact and herbivore selectivity of ciliate communities in response to winter warming. Oecologia 150:668–681PubMedGoogle Scholar
  2. Arndt H (1993) Rotifers as predators on components of the microbial web (bacteria, heterotrophic flagellates, ciliates)—a review. Hydrobiologia 255:231–246Google Scholar
  3. Azam F, Fenchel T, Field JG, Gray JS, Meyer-Reil LA, Thingstad F (1983) The ecological role of water-column microbes in the sea. Mar Ecol Prog Ser 10:257–263Google Scholar
  4. Båmstedt U, Gifford DJ, Irigoien X, Atkinson A, Roman M (2000) Feeding. In: Harris R, Wiebe P, Lenz J, Skjoldal HR, Huntley M (eds) ICES zooplankton methodology manual. Academic Press, London, pp 297–399Google Scholar
  5. Bec A, Martin-Creuzburg D, von Elert E (2006) Trophic upgrading of autotrophic picoplankton by the heterotrophic nanoflagellate Paraphysomonas sp. Limnol Oceanogr 51:1699–1707Google Scholar
  6. Brock TD (1981) Calculating solar radiation for ecological studies. Ecolog Model 14:1–19Google Scholar
  7. Broglio E, Jónasdóttir SH, Calbet A, Jakobsen HH, Saiz E (2003) Effect of heterotrophic versus autotrophic food on feeding and reproduction of the calanoid copepod Acartia tonsa: relationship with prey fatty acid composition. Aquat Microb Ecol 31:267–278Google Scholar
  8. Brussaard CPD, Riegman R, Noordeloos AAM, Cadee GC, Witte H, Kop AJ, Nieuwland G, Vanduyl FC, Bak RPM (1995) Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web. Mar Ecol Prog Ser 123:259–271Google Scholar
  9. Calbet A (2001) Mesozooplankton grazing effect on primary production: a global comparative analysis in marine ecosystems. Limnol Oceanogr 46:1824–1830Google Scholar
  10. Calbet A, Landry MR (2004) Phytoplankton growth, microzooplankton grazing, and carbon cycling in marine systems. Limnol Oceanogr 49:51–57Google Scholar
  11. Calbet A, Saiz E (2005) The ciliate-copepod link in marine ecosystems. Aquat Microb Ecol 38:157–167Google Scholar
  12. Carey PG (1992) Marine interstitial ciliates: an illustrated key. Chapman & Hall, LondonGoogle Scholar
  13. Caron DA (2000) Protistan herbivory and bacterivory. In: Paul J (ed) Methods in microbiology, vol 30. Academic Press, San Diego, pp 289–315Google Scholar
  14. Chesson J (1978) Measuring preference in selective predation. Ecol 59:211–215CrossRefGoogle Scholar
  15. Chesson J (1983) The estimation and analysis of preference and its relationship to foraging models. Ecol 64:1297–1304Google Scholar
  16. 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
  17. Cowles TJ, Olson RJ, Chisholm SW (1988) Food selection by copepods—discrimination on the basis of food quality. Mar Biol 100:41–49Google Scholar
  18. Crawford DW, Stoecker DK (1996) Carbon content, dark respiration and mortality of the mixotrophic planktonic ciliate Strombidium capitatum. Mar Biol 126:415–422Google Scholar
  19. Dagg MJ, Vidal J, Whitledge TE, Iverson RL, Goering JJ (1982) The feeding, respiration, and excretion of zooplankton in the Bering Sea during a spring bloom. Deep-Sea Res Part I: Oceanogr Res Pap 29:45–63Google Scholar
  20. Dam HG (1986) Short-term feeding of Temora longicornis Müller in the laboratory and the field. J Exp Mar Biol Ecol 99:149–161Google Scholar
  21. Dam HG, Peterson WT (1993) Seasonal contrasts in the diel vertical distribution, feeding-behavior, and grazing impact of the copepod Temora longicornis in Long-Island Sound. J Mar Res 51:561–594Google Scholar
  22. Dam HG, Miller CA, Jonasdottir SH (1993) The trophic role of mesozooplankton at 47°N, 20°W during the North Atlantic Bloom Experiment. Deep-Sea Res Part II: Top Stud Oceanogr 40:197–212Google Scholar
  23. Daro MH (1985) Field-study of selectivity, efficiency and daily variation in the feeding of the marine copepod Temora longicornis, in the Southern Bight of the North Sea. Bull Mar Sci 37:764–764Google Scholar
  24. Dodge JD (1982) Marine dinoflagellates of the British Isles. Her Majesty’s Stationery Office, LondonGoogle Scholar
  25. Dolan JR, McKeon K (2005) The reliability of grazing rate estimates from dilution experiments: have we over-estimated rates of organic carbon consumption by microzooplankton? Ocean Sci 1:1–7Google Scholar
  26. Dolan JR, Gallegos CL, Moigis A (2000) Dilution effects on microzooplankton in dilution grazing experiments. Mar Ecol Prog Ser 200:127–139Google Scholar
  27. Du Yoo Y, Jeong HJ, Kim MS, Kang NS, Song JY, Shin W, Kim KY, Lee K (2009) Feeding by phototrophic red-tide dinoflagellates on the ubiquitous marine diatom Skeletonema costatum. J Eukaryot Microbiol 56:413–420PubMedGoogle Scholar
  28. Fenchel T (1980) Relation between particle size selection and clearance in suspension-feeding ciliates. Limnol Oceanogr 25:733–738Google Scholar
  29. Fenchel T, Finlay BJ (1983) Respiration rates in heterotrophic, free-living protozoa. Microb Ecol 9:99–122PubMedGoogle Scholar
  30. Fileman E, Smith T, Harris R (2007) Grazing by Calanus helgolandicus and Para-Pseudocalanus spp. on phytoplankton and protozooplankton during the spring bloom in the Celtic Sea. J Exp Mar Biol Ecol 348:70–84Google Scholar
  31. First MR, Miller HL, Lavrentyev PJ, Pinckney JL, Burd AB (2009) Effects of microzooplankton growth and trophic interactions on herbivory in coastal and offshore environments. Aquat Microb Ecol 54:255–267Google Scholar
  32. Flynn KJ (2008) Attack is not the best form of defense: Lessons from harmful algal bloom dynamics. Harmful Algae 8:129–139Google Scholar
  33. Fonda Umani S, Tirelli V, Beran A, Guardiani B (2005) Relations between microzooplankton and mesozooplankton: Competition versus predation on natural assemblages of the Gulf of Trieste (Northern Adriatic Sea). J Plankton Res 27:973–986Google Scholar
  34. Frost BW (1972) Effects of size and concentration of food particles on the feeding behaviour of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815Google Scholar
  35. Gaines G, Elbrächter M (1987) Heterotrophic nutrition. In: Taylor FJR (ed) The biology of dinoflagellates. Blackwell, Oxford, pp 224–268Google Scholar
  36. Gallegos CL (1989) Microzooplankton grazing on phytoplankton in the Rhode River, Maryland: Nonlinear feeding kinetics. Mar Ecol Prog Ser 57:23–33Google Scholar
  37. Gentsch E, Kreibich T, Hagen W, Niehoff B (2009) Dietary shifts in the copepod Temora longicornis during spring: evidence from stable isotope signatures, fatty acid biomarkers and feeding experiments. J Plankton Res 31:45–60Google Scholar
  38. Gifford DJ (1985) Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida). Mar Ecol Prog Ser 23:257–267Google Scholar
  39. Gifford DJ, Dagg MJ (1988) Feeding of the estuarine copepod Acartia tonsa dana: Carnivory vs. herbivory in natural microplankton assemblages. Bull Mar Sci 43:458–468Google Scholar
  40. Grasshoff K, Kremling K, Ehrhardt M (eds) (1999) Methods of seawater analysis, 3rd edn. Wiley-VCH Verlag, WeinheimGoogle Scholar
  41. Greve W, Reiners F, Nast J, Hoffmann S (2004) Helgoland Roads meso- and macrozooplankton time-series 1974 to 2004: lessons from 30 years of single spot, high frequency sampling at the only off-shore island of the North Sea. Helgol Mar Res 58:274–288Google Scholar
  42. Guillard RRL, Ryther JH (1962) Studies of marine planktonic diatoms. I. Cyclotella nana Hustedt and Detonula confervacea (Cleve) Gran. Can J Microbiol 8:229–239Google Scholar
  43. Hamels I, Mussche H, Sabbe K, Muylaert K, Vyverman W (2004) Evidence for constant and highly specific active food selection by benthic ciliates in mixed diatoms assemblages. Limnol Oceanogr 49:58–68Google Scholar
  44. Hansen PJ (1992) Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale. Mar Biol 114:327–334Google Scholar
  45. Hansen FC, Reckermann M, Klein Breteler WCM, Riegman R (1993) Phaeocystis blooming enhanced by copepod predation on protozoa—evidence from incubation experiments. Mar Ecol Prog Ser 102:51–57Google Scholar
  46. Heinbokel JF (1978) Studies on the functional role of tintinnids in the southern California Bight. I. Grazing and growth rates in laboratory cultures. Mar Biol 47:177–189Google Scholar
  47. Hickel W, Mangelsdorf P, Berg J (1993) The human impact in the German Bight: eutrophication during three decades (1962–1991). Helgol Meeresunters 47:243–263Google Scholar
  48. Hillebrand H, Dürselen C-D, Kirschtel D, Pollingher U, Zohary T (1999) Biovolume calculation for pelagic and benthic microalgae. J Phycol 35:403–424Google Scholar
  49. Hoppenrath M, Elbrächter M, Drebes G (2009) Marine phytoplankton: Selected microphytoplankton species from the North Sea around Helgoland and Sylt. Kleine Senckenberg-Reihe 49. E. Schweizerbart’sche Verlagsbuchhandlung (Nägele u. Obermiller), StuttgartGoogle Scholar
  50. Irigoien X, Flynn KJ, Harris RP (2005) Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? J Plankton Res 27:313–321Google Scholar
  51. Jackson KM, Berger J (1985) Survivorship curves of ciliate protozoa under starvation conditions and at low bacterial levels. Protistologica 21:17–24Google Scholar
  52. Jacobson DM, Anderson DM (1986) Thecate heterotrophic dinoflagellates: feeding behavior and mechanisms. J Phycol 22:249–258Google Scholar
  53. Jakobsen HH, Halvorsen E, Hansen BW, Visser AW (2005) Effects of prey motility and concentration on feeding in Acartia tonsa and Temora longicornis: the importance of feeding modes. J Plankton Res 27(8):775–785Google Scholar
  54. Jensen TC, Hessen DO (2007) Does excess dietary carbon affect respiration of Daphnia? Oecologia 152:191–200PubMedGoogle Scholar
  55. Jeong HJ (1999) The ecological role of heterotrophic dinoflagellates in marine plankton community. J Eukaryot Microbiol 46:390–396Google Scholar
  56. 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 26:67–80Google Scholar
  57. Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33:265–277Google Scholar
  58. Kahl A (1932) Urtiere oder Protozoa. I Wimpertiere. 3 Spirotricha. In: Dahl F (ed) Die Tierwelt Deutschlands und der angrenzenden Meeresteile, vol 25. Gustav Fischer, JenaGoogle Scholar
  59. Kim YO, Ha S, Taniguchi A (2008) Morphology and in situ sedimentation of the cysts of a planktonic oligotrich ciliate, Strombidium capitatum. Aquat Microb Ecol 53:173–179Google Scholar
  60. Klein Breteler WCM, Schogt N, Baas M, Schouten S, Kraay GW (1999) Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids. Mar Biol 135:191–198Google Scholar
  61. Kleppel GS (1993) On the diets of calanoid copepods. Mar Ecol Prog Ser 99:183–195Google Scholar
  62. Kleppel GS, Holliday DV, Pieper RE (1991) Trophic interactions between copepods and microplankton: a question about the role of diatoms. Limnol Oceanogr 36:172–178Google Scholar
  63. Köhler W, Schachtel G, Voleske P (1995) Biostatistik: Einführung in die Biometrie für Biologen und Agrarwissenschaftler, 2 edn edn. Springer, BerlinGoogle Scholar
  64. Koski M, Dutz J, Klein Breteler WCM (2005) Selective grazing of temora longicornis in different stages of a Phaeocystis globosa bloom—a mesocosm study. Harmful Algae 4(5):915–927Google Scholar
  65. Landry MR (1993) Estimating rates of growth and grazing mortality of phytoplankton by the dilution method. In: Kemp PF, Sherr BF, Sherr EB, Cole JJ (eds) Handbook of methods in aquatic microbial ecology. Lewis Publishers, Boca Raton, pp 715–722Google Scholar
  66. Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507Google Scholar
  67. Landry MR, Calbet A (2005) Reality checks on microbial food web interactions in dilution experiments: responses to the comments of Dolan and McKeon. Ocean Science 1:39–44Google Scholar
  68. Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288Google Scholar
  69. Landry MR, Kirshtein J, Constantinou J (1995) A refined dilution technique for measuring the community grazing impact of microzooplankton, with experimental tests in the central equatorial Pacific. Mar Ecol Prog Ser 120:53–63Google Scholar
  70. Löder MGJ (2010) The role of heterotrophic dinoflagellate and ciliate grazers in the food web at Helgoland Roads, North Sea. Dissertation, Jacobs University BremenGoogle Scholar
  71. Löder MGJ, Aberle N, Klaas C, Kraberg AC, Wiltshire KH (2010) Conserving original in situ diversity in microzooplankton grazing set-ups. Mar Biodivers Rec 3:e28Google Scholar
  72. Löder MGJ, Kraberg AC, Aberle N, Peters S, Wiltshire KH (2011) Dinoflagellates and ciliates at Helgoland Roads, North Sea. Helgol Mar Res (in Press)Google Scholar
  73. Maar M, Nielsen TG, Gooding S, Tonnesson K, Tiselius P, Zervoudaki S, Christou E, Sell A, Richardson K (2004) Trophodynamic function of copepods, appendicularians and protozooplankton in the late summer zooplankton community in the Skagerrak. Mar Biol 144:917–933Google Scholar
  74. Malzahn AM, Hantzsche F, Schoo KL, Boersma M, Aberle N (2010) Differential effects of nutrient-limited primary production on primary, secondary or tertiary consumers. Oecologia 162:35–48PubMedGoogle Scholar
  75. Martin-Creuzburg D, Bec A, von Elert E (2005) Trophic upgrading of picocyanobacterial carbon by ciliates for nutrition of Daphnia magna. Aquat Microb Ecol 41:271–280Google Scholar
  76. Mauchline J (1998) The biology of calanoid copepods. In: Advances in marine biology, vol 33. Academic Press, LondonGoogle Scholar
  77. McCauley E (1984) The estimation of the abundance and biomass of zooplankton in samples. In: Downing JA, Rigler FH (eds) A manual on methods for the assessment of secondary productivity in freshwater, IBP Handbook no. 17, 2nd edn. Blackwell Scientific Publications, Oxford, pp 228–265Google Scholar
  78. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579Google Scholar
  79. Menden-Deuer S, Lessard EJ, Satterberg J, Grünbaum D (2005) Growth rates and starvation survival of three species of the pallium-feeding, thecate dinoflagellate genus Protoperidinium. Aquat Microb Ecol 41:145–152Google Scholar
  80. Moigis AG (2006) The clearance rate of microzooplankton as the key element for describing estimated non-linear dilution plots demonstrated by a model. Mar Biol 149:743–762Google Scholar
  81. Montagnes DJS (2003) Planctonic ciliate project internet homepage. http://www.liv.ac.uk/ciliate/intro.htm. Accessed 19 December 2007
  82. 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
  83. Müller 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
  84. Müller H, Weisse T (1994) Laboratory and field observations on the scuticociliate Histiobalantium from the pelagic zone of Lake Constance, FRG. J Plankton Res 16:391–401Google Scholar
  85. Naustvoll LJ (2000a) Prey size spectra and food preferences in thecate heterotrophic dinoflagellates. Phycologia 39:187–198Google Scholar
  86. Naustvoll LJ (2000b) Prey size spectra in naked heterotrophic dinoflagellates. Phycologia 39:448–455Google Scholar
  87. Nejstgaard JC, Gismervik I, Solberg PT (1997) Feeding and reproduction by Calanus finmarchicus, and microzooplankton grazing during mesocosm blooms of diatoms and the coccolithophore Emiliania huxleyi. Mar Ecol Prog Ser 147:197–217Google Scholar
  88. Nejstgaard JC, Naustvoll L-J, Sazhin A (2001) Correcting for underestimation of microzooplankton grazing in bottle incubation experiments with mesozooplankton. Mar Ecol Prog Ser 221:59–75Google Scholar
  89. O’Connors HB, Biggs DC, Ninivaggi DV (1980) Particle-size-dependent maximum grazing rates for Temora longicornis fed natural particle assemblages. Mar Biol 56(1):65–70Google Scholar
  90. Paffenhöfer G-A (1988) Feeding rates and behavior of zooplankton. Bull Mar Sci 43:430–445Google Scholar
  91. Park GS, Marshall HG (2000) The trophic contributions of rotifers in tidal freshwater and estuarine habitats. Estuar Coast Shelf Sci 51:729–742Google Scholar
  92. Paterson HL, Knott B, Koslow AJ, Waite AM (2008) The grazing impact of microzooplankton off south west Western Australia: as measured by the dilution technique. J Plankton Res 30:379–392Google Scholar
  93. Poole HH, Atkins WRG (1929) Photo-electric measurements of submarine illumination throughout the year. J Mar Biol Assoc UK 16:297–324Google Scholar
  94. 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
  95. Quinlan EL, Jett CH, Phlips EJ (2009) Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary, USA. Hydrobiologia 632:127–137Google Scholar
  96. Riegman R, Kuipers BR, Noordeloos AAM, Witte HJ (1993) Size-differential control of phytoplankton and the structure of plankton communities. Neth J Sea Res 31:255–265Google Scholar
  97. Schoo KL (2010) Stoichiometric constraints in primary producers affect secondary consumers. Dissertation, Christian-Albrechts-Universität, KielGoogle Scholar
  98. Sherr EB, Sherr BF (2002) Significance of predation by protists in aquatic microbial food webs. Antonie Van Leeuwenhoek Int J Gen Mol Microb 81:293–308Google Scholar
  99. Sherr EB, Sherr BF (2007) Heterotrophic dinoflagellates: a significant component of microzooplankton biomass and major grazers of diatoms in the sea. Mar Ecol Prog Ser 352:187–197Google Scholar
  100. Sherr EB, Sherr BF (2009) Capacity of herbivorous protists to control initiation and development of mass phytoplankton blooms. Aquat Microb Ecol 57:253–262Google Scholar
  101. Sherr EB, Sherr BF, Paffenhöfer G-A (1986) Phagotrophic protozoa as food for metazoans: a “missing” trophic link in marine pelagic food webs? Mar Microb Food Webs 1:61–80Google Scholar
  102. Sime-Ngando T, Demers S, Juniper SK (1999) Protozoan bacterivory in the ice and the water column of a cold temperate lagoon. Microb Ecol 37:95–106PubMedGoogle Scholar
  103. Smetacek V (1981) The annual cycle of proto-zooplankton in the Kiel Bight. Mar Biol 63:1–11Google Scholar
  104. Sommer U, Sommer F (2006) Cladocerans versus copepods: The cause of contrasting top-down controls on freshwater and marine phytoplankton. Oecologia 147:183–194PubMedGoogle Scholar
  105. Sommer U, Sommer F, Santer B, Zöllner E, Jürgens K, Jamieson C, Boersma M, Gocke K (2003) Daphnia versus copepod impact on summer phytoplankton: Functional compensation at both trophic levels. Oecologia 135:639–647PubMedGoogle Scholar
  106. Sommer F, Saage A, Santer B, Hansen T, Sommer U (2005a) Linking foraging strategies of marine calanoid copepods to patterns of nitrogen stable isotope signatures in a mesocosm study. Mar Ecol Prog Ser 286:99–106Google Scholar
  107. Sommer U, Hansen T, Blum O, Holzner N, Vadstein O, Stibor H (2005b) 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 142:274–283PubMedGoogle Scholar
  108. Sommer U, Aberle N, Engel A, Hansen T, Lengfellner K, Sandow M, Wohlers J, Zöllner E, Riebesell U (2007) 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 150:655–667PubMedGoogle Scholar
  109. Spittler P (1973) Feeding experiments with tintinnids. Oikos (Suppl.) 15:128–132Google Scholar
  110. Stoecker DK, Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J Plankton Res 12:891–908Google Scholar
  111. Stoecker DK, Silver MW (1990) Replacement and aging of chloroplasts in Strombidium capitatum (Ciliophora, Oligotrichida). Mar Biol 107:491–502Google Scholar
  112. Stoecker D, Guillard RRL, Kavee RM (1981) Selective predation by Favella ehrenbergii (Tintinnia) on and among dinoflagellates. Biolog Bull 160:136–145Google Scholar
  113. Strom SL, Morello TA (1998) Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates. J Plankton Res 20:571–584Google Scholar
  114. Tackx MLM, Bakker C, Francke JW, Vink M (1989) Size and phytoplankton selection by Oosterschelde zooplankton. Neth J Sea Res 23:35–43Google Scholar
  115. Tackx MLM, Bakker C, Vanrijswijk P (1990) Zooplankton grazing pressure in the Oosterschelde (the Netherlands). Neth J Sea Res 25:405–415Google Scholar
  116. Tang KW, Taal M (2005) Trophic modification of food quality by heterotrophic protists: species-specific effects on copepod egg production and egg hatching. J Exp Mar Biol Ecol 318:85–98Google Scholar
  117. Teixeira IG, Figueiras FG (2009) Feeding behaviour and non-linear responses in dilution experiments in a coastal upwelling system. Aquat Microb Ecol 55:53–63Google Scholar
  118. Throndsen J (1978) Preservation and storage. In: Sournia A (ed) Phytoplankton manual. UNESCO, Paris, pp 69–74Google Scholar
  119. Tillmann U (2004) Interactions between planktonic microalgae and protozoan grazers. J Eukaryot Microbiol 51:156–168PubMedGoogle Scholar
  120. Tiselius P (1989) Contribution of aloricate ciliates to the diet of Acartia clausi and Centropages hamatus in coastal waters. Mar Ecol Prog Ser 56:49–56Google Scholar
  121. Tomas CR (1996) Identifying marine diatoms and dinoflagellates. Academic Press Inc., San DiegoGoogle Scholar
  122. Tyler JE (1968) The secchi disc. Limnol Oceanogr 13:1–6Google Scholar
  123. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Plankton-Methodik. Mitt Int Ver theor angew Limnol 9:1–38Google Scholar
  124. Vanderploeg H, Scavia D (1979a) Caculation and use of selectivity coefficients of feeding: zooplankton grazing. Ecol Model 7:135–149Google Scholar
  125. Vanderploeg H, Scavia D (1979b) Two electivity indices for feeding with special reference to zooplankton grazing. J Fish Res Board Can 36:362–365Google Scholar
  126. Verity PG (1991) Feeding in planktonic protozoans—evidence for nonrandom acquisition of prey. J Protozool 38:69–76Google Scholar
  127. Wiltshire KH, Dürselen CD (2004) Revision and quality analyses of the Helgoland Reede long-term phytoplankton data archive. Helgol Mar Res 58(4):252–268Google Scholar
  128. Wiltshire KH, Malzahn AM, Wirtz K, Greve W, Janisch S, Mangelsdorf P, Manly BFJ, Boersma M (2008) Resilience of North Sea phytoplankton spring bloom dynamics: an analysis of long-term data at Helgoland Roads. Limnol Oceanogr 53:1294–1302Google Scholar
  129. Xu DP, Song WB, Hu XZ (2005) Morphology of Cyclotrichium taniguchii sp. nov and C. cyclokaryon with establishment of a new genus, Dicyclotrichium gen. nov (Ciliophora: Haptorida). J Mar Biol Assoc UK 85:787–794Google Scholar
  130. Zöllner E, Hoppe HG, Sommer U, Jürgens K (2009) Effect of zooplankton-mediated trophic cascades on marine microbial food web components (bacteria, nanoflagellates, ciliates). Limnol Oceanogr 54:262–275Google Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Martin G. J. Löder
    • 1
  • Cédric Meunier
    • 1
  • Karen H. Wiltshire
    • 1
  • Maarten Boersma
    • 1
  • Nicole Aberle
    • 1
  1. 1.Biologische Anstalt HelgolandAlfred Wegener Institute for Polar and Marine ResearchHelgolandGermany

Personalised recommendations