Marine Biology

, Volume 159, Issue 11, pp 2441–2453 | Cite as

Warming induces shifts in microzooplankton phenology and reduces time-lags between phytoplankton and protozoan production

  • N. Aberle
  • B. Bauer
  • A. Lewandowska
  • U. Gaedke
  • U. Sommer
Original Paper

Abstract

Indoor mesocosm experiments were conducted to test for potential climate change effects on the spring succession of Baltic Sea plankton. Two different temperature (Δ0 °C and Δ6 °C) and three light scenarios (62, 57 and 49 % of the natural surface light intensity on sunny days), mimicking increasing cloudiness as predicted for warmer winters in the Baltic Sea region, were simulated. By combining experimental and modeling approaches, we were able to test for a potential dietary mismatch between phytoplankton and zooplankton. Two general predator–prey models, one representing the community as a tri-trophic food chain and one as a 5-guild food web were applied to test for the consequences of different temperature sensitivities of heterotrophic components of the plankton. During the experiments, we observed reduced time-lags between the peaks of phytoplankton and protozoan biomass in response to warming. Microzooplankton peak biomass was reached by 2.5 day °C−1 earlier and occurred almost synchronously with biomass peaks of phytoplankton in the warm mesocosms (Δ6 °C). The peak magnitudes of microzooplankton biomass remained unaffected by temperature, and growth rates of microzooplankton were higher at Δ6 °C (μ∆0 °C = 0.12 day−1 and μ∆6 °C = 0.25 day−1). Furthermore, warming induced a shift in microzooplankton phenology leading to a faster species turnover and a shorter window of microzooplankton occurrence. Moderate differences in the light levels had no significant effect on the time-lags between autotrophic and heterotrophic biomass and on the timing, biomass maxima and growth rate of microzooplankton biomass. Both models predicted reduced time-lags between the biomass peaks of phytoplankton and its predators (both microzooplankton and copepods) with warming. The reduction of time-lags increased with increasing Q10 values of copepods and protozoans in the tritrophic food chain. Indirect trophic effects modified this pattern in the 5-guild food web. Our study shows that instead of a mismatch, warming might lead to a stronger match between protist grazers and their prey altering in turn the transfer of matter and energy toward higher trophic levels.

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 150:668–681CrossRefGoogle Scholar
  2. Berger SA, Diehl S, Stibor H, Trommer G, Ruhenstroth M (2010) Water temperature and stratification depth independently shift cardinal events during plankton spring succession. Global Change Biol 16:1954–1965CrossRefGoogle Scholar
  3. Brock TD (1981) Calculating solar radiation for ecological studies. Ecol Modell 14:1–19CrossRefGoogle Scholar
  4. Brown JH, Gillooly JF, Allen AP, Savage VM, West GB (2004) Toward a metabolic theory of ecology. Ecology 85:1771–1789CrossRefGoogle Scholar
  5. Calbet A (2008) The trophic roles of microzooplankton in marine systems. ICES J Mar Sci 65:325–331CrossRefGoogle Scholar
  6. Castellani C, Irigoien X, Harris RP, Lampitt RS (2005) Feeding and egg production of Oithona similis in the North Atlantic. Mar Ecol Prog Ser 288:173–182CrossRefGoogle Scholar
  7. 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 43:458–464CrossRefGoogle Scholar
  8. Davis CS (1984) Predatory control of copepod seasonal cycles on Georges Bank. Mar Biol 82:31–40CrossRefGoogle Scholar
  9. Diehl S, Berger S, Ptacnik R, Wild A (2002) Phytoplankton, light, and nutrients in a gradient of mixing depths: field experiments. Ecology 83:399–411CrossRefGoogle Scholar
  10. Durant JM, Hjermann DO, Ottersen G, Stenseth NC (2007) Climate and the match or mismatch between predator requirements and resource availability. Clim Res 33:271–283CrossRefGoogle Scholar
  11. Edwards M, Richardson AJ (2004) Impact of climate change on marine pelagic phenology and trophic mismatch. Nature 430:881–884CrossRefGoogle Scholar
  12. Foissner W, Berger H, Kohmann F (1991, 1992, 1994, 1995) Taxonomische und ökologische revision der Ciliaten des Saprobiensystems Band I–IV, vol, Informationsberichte Bayerisches Landesamt für Wasserwirtschaft, MünchenGoogle Scholar
  13. Gaedke U, Rubenstroth-Bauer M, Wiegand I, Tirok K, Aberle N, Breithaupt P, Lengfellner K, Wohlers J, Sommer U (2010) Biotic interactions may overrule direct climate effects on spring phytoplankton dynamics. Global Change Biology 16:1122–1136Google Scholar
  14. 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
  15. Hillebrand H, Burgmer T, Biermann E (2011) Running to stand still: temperature effects on species richness, species turnover, and functional community dynamics. Mar Biol. doi:10.1007/s00227-011-1827-z
  16. IPCC (2007) Climate change 2007: the physical science basis. Contribution of working group I to the fourth assessment report of the intergovernmental panel on climate change. CambridgeGoogle Scholar
  17. Irigoien X, Flynn KJ, Harris RP (2005) Phytoplankton blooms: a ‘loophole’ in microzooplankton grazing impact? J Plankton Res 27:313–321CrossRefGoogle Scholar
  18. Isla JA, Lengfellner K, Sommer U (2008) Physiological response of the copepod Pseudocalanus sp in the Baltic Sea at different thermal scenarios. Global Change Biol 14:895–906CrossRefGoogle Scholar
  19. 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
  20. Jonsson PR (1986) Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina). Mar Ecol Prog Ser 33:265–277CrossRefGoogle Scholar
  21. Kahl A (1932) Urtiere oder Protozoa I. Wimpertiere oder Ciliata (Infusoria). In: Dahl F (ed) Tierwelt Deutschlands und der angrenzenden Meeresteile, vol 18, pp 1–886Google Scholar
  22. Keller AA, Oviatt CA, Walker HA, Hawk JD (1999) Predicted impacts of elevated temperature on the magnitude of the winter-spring phytoplankton bloom in temperate coastal waters: a mesocosm study. Limnol Oceanogr 44:344–356CrossRefGoogle Scholar
  23. Landry MR (1983) The development of marine calanoid copepods with comment on the isochronal rule. Limnol Oceanogr 28:614–624CrossRefGoogle Scholar
  24. Landry MR, Calbet A (2004) Microzooplankton production in the oceans. ICES J Mar Sci 61:501–507CrossRefGoogle Scholar
  25. Lasker R (1981) The role of a stable ocean in larval fish survival and subsequent recruitment. In: Lasker R (ed) Marine fish larvae. University of Washington press, Seattle, pp 80–88Google Scholar
  26. Leandro SM, Tiselius P, Queiroga H (2006) Growth and development of nauplii and copepodites of the estuarine copepod Acartia tonsa from southern Europe (Ria de Aveiro, Portugal) under saturating food conditions. Mar Biol 150:121–129CrossRefGoogle Scholar
  27. Lewandowska A, Sommer U (2010) Climate change and the spring bloom: a mesocosm study on the influence of light and temperature on phytoplankton and mesozooplankton. Mar Ecol Prog Ser 405:101–111CrossRefGoogle Scholar
  28. Loeder M, Meunier C, Wiltshire KH, Boersma M, Aberle N (2011) The role of ciliates, heterotrophic dinoflagellates and copepods in structuring spring phytoplankton communities at Helgoland Roads, North Sea. Mar Biol 158(7):1551–1580CrossRefGoogle Scholar
  29. Lopez-Urrutia A (2008) The metabolic theory of ecology and algal bloom formation. Limnol Oceanogr 53:2046–2047Google Scholar
  30. Malzahn AM, Boersma M (2009) Trophic flexibility in larvae of two fish species (lesser sandeel, Ammodytes marinus and dab, Limanda limanda). Sci Mar 73:131–139Google Scholar
  31. 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 162:35–48CrossRefGoogle Scholar
  32. McGowan JA, Bograd SJ, Lynn RJ, Miller AJ (2003) The biological response to the 1977 regime shift in the California Current. Deep Sea Res II 50:2567–2582CrossRefGoogle Scholar
  33. Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationships for dinoflagellates, diatoms, and other protist plankton. Limnol Oceanogr 45:569–579CrossRefGoogle Scholar
  34. Montagnes DJS, Kimmance SA, Atkinson D (2003) Using Q10: can growth rates increase linearly with temperature? Aquat Microb Ecol 32:307–313CrossRefGoogle Scholar
  35. Nielsen TG, Kiorboe T (1994) Regulation of zooplankton biomass and production in a temperate, coastal ecosystem.2. Ciliates. Limnol Oceanogr 39:508–519CrossRefGoogle Scholar
  36. Paffenhöfer GA, Harris RP (1976) Feeding, growth and reproduction of marine planktonic copepod Pseudocalanus elongatus (Boeck). J Mar Biol Ass UK 56:327–344CrossRefGoogle Scholar
  37. Piontek J, Handel N, Langer G, Wohlers J, Riebesell U, Engel A (2009) Effects of rising temperature on the formation and microbial degradation of marine diatom aggregates. Aquat Microb Ecol 54:305–318CrossRefGoogle Scholar
  38. Putt M, Stoecker DK (1989) An experimentally determined carbon:volume ratio for marine “oligotrichous” ciliates from estuarine and coastal waters. Limnol Oceanogr 34:1097–1103CrossRefGoogle Scholar
  39. Rose JM, Caron DA (2007) Does low temperature constrain the growth rates of heterotrophic protists? Evidence and implications for algal blooms in cold waters. Limnol Oceanogr 52:886–895CrossRefGoogle Scholar
  40. Rose JM, Feng YY, Gobler CJ, Gutierrez R, Hare CE, Leblanc K, Hutchins DA (2009) Effects of increased pCO(2) and temperature on the North Atlantic spring bloom. II. Microzooplankton abundance and grazing. Mar Ecol Prog Ser 388:27–40CrossRefGoogle Scholar
  41. Rosenzweig ML, MacArthur RH (1963) Graphical representation and stability conditions of predator-prey ineractions. Am Nat 97:209–223CrossRefGoogle Scholar
  42. Scott FJE (2005) Antarctic marine protists, vol ABRS. Canberra, Australia, p 563Google Scholar
  43. Smol JP, Wolfe AP, Birks HJB, Douglas MSV, Jones VJ, Korhola A, Pienitz R, Ruhland K, Sorvari S, Antoniades D, Brooks SJ, Fallu MA, Hughes M, Keatley BE, Laing TE, Michelutti N, Nazarova L, Nyman M, Paterson AM, Perren B, Quinlan R, Rautio M, Saulnier-Talbot E, Siitoneni S, Solovieva N, Weckstrom J (2005) Climate-driven regime shifts in the biological communities of arctic lakes. Proc Nat Acad Sci 102:4397–4402CrossRefGoogle Scholar
  44. Sommer U, Lengfellner K (2008) Climate change and the timing, magnitude, and composition of the phytoplankton spring bloom. Global Change Biol 14:1199–1208CrossRefGoogle Scholar
  45. 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 142:274–283CrossRefGoogle Scholar
  46. Stoecker DK, Capuzzo JM (1990) Predation on protozoa: its importance to zooplankton. J Plankton Res 12:891–908CrossRefGoogle Scholar
  47. 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
  48. 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
  49. Thackeray SJ, Jones ID, Maberly SC (2008) Long-term change in the phenology of spring phytoplankton: species-specific responses to nutrient enrichment and climatic change. J Ecol 96:523–535CrossRefGoogle Scholar
  50. Thackeray SJ, Sparks TH, Frederiksen M, Burthe S, Bacon PJ, Bell JR, Botham MS, Brereton TM, Bright PW, Carvalho L, Clutton-Brock T, Dawson A, Edwards M, Elliott JM, Harrington R, Johns D, Jones ID, Jones JT, Leech DI, Roy DB, Scott WA, Smith M, Smithers RJ, Winfield IJ, Wanless S (2010) Trophic level asynchrony in rates of phenological change for marine, freshwater and terrestrial environments. Global Change Biol 16:3304–3313CrossRefGoogle Scholar
  51. Tirok K, Gaedke U (2007) Regulation of planktonic ciliate dynamics and functional composition during spring in Lake Constance. Aquat Microb Ecol 49:87–100CrossRefGoogle Scholar
  52. Tomas CRE (1996) Identifying marine diatoms and dinoflagellates. Academic Press, Inc., San Diego, p 598Google Scholar
  53. Turner JT, Graneli E (1992) Zooplankton feeding ecology—grazing during enclosure studies of phytoplankton blooms from the West-Coast of Sweden. J Exp Mar Biol Ecol 157:19–31CrossRefGoogle Scholar
  54. Utermöhl H (1958) Zur Vervollkommnung der quantitativen Phytoplankton-Methodik. Mitt Int Ver Limnol 9:1–38Google Scholar
  55. Vincent D, Hartmann HJ (2001) Contribution of ciliated microprotozoans and dinoflagellates to the diet of three copepod species in the Bay of Biscay. Hydrobiologia 443:193–204CrossRefGoogle Scholar
  56. Walther G-R (2010) Community and ecosystem responses to recent climate change. Philos Trans R Soc B 365:2019–2024CrossRefGoogle Scholar
  57. Weisse T, Montagnes DJS (1998) Effect of temperature on inter- and intraspecific isolates of Urotricha (Prostomatida, Ciliophora). Aquat Microb Ecol 15:285–291CrossRefGoogle Scholar
  58. Wiltshire KH, Manly BFJ (2004) The warming trend at Helgoland Roads, North Sea: phytoplankton response. Helgol Mar Res 58:269–273CrossRefGoogle Scholar
  59. 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 53:1294–1302CrossRefGoogle Scholar
  60. Winder M, Schindler DE (2004) Climatic effects on the phenology of lake processes. Global Change Biol 10:1844–1856CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2012

Authors and Affiliations

  • N. Aberle
    • 1
  • B. Bauer
    • 2
    • 3
  • A. Lewandowska
    • 3
  • U. Gaedke
    • 2
  • U. Sommer
    • 3
  1. 1.Biologische Anstalt Helgoland, Alfred-Wegener Institute for Polar and Marine ResearchHelgolandGermany
  2. 2.Institute for Biochemistry and BiologyUniversity PotsdamPotsdamGermany
  3. 3.GEOMAR Helmholtz Centre for Ocean ResearchKielGermany

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