Skip to main content
SpringerLink
Log in

Comparing the Trophic Impact of Microzooplankton during the Spring and Autumn Blooms in Temperate Waters

  • Published:
Estuaries and Coasts Aims and scope Submit manuscript

Abstract

To appreciate coastal trophodynamics, it is necessary to understand the dynamics and control of the spring and late summer/autumn phytoplankton blooms. Classically mesozooplankton are considered as main players in these blooms. Microzooplankton likely also are important in these dynamics, but their role is poorly understood. Critically, due to their rapid generation times, microzooplankton may exhibit rapid shifts during blooms. Through field sampling and rate measurements (dilution experiments) in a well-studied temperate coastal ecosystem (Helgoland, southern North Sea) we ask if there are differences in the trends exhibited between and within the spring and late summer/autumn blooms. To achieve this, we examined early, mid and late bloom periods in both seasons. We found 1) a shift in trophic composition during both blooms, with a trend from strongly autotrophic mixotrophs (e.g. Mesodinium) to mixotrophs and then towards heterotrophs; 2) an increase in intraguild predation at the end of the blooms; and 3) although microzooplankton were major consumers of the spring bloom (grazing coefficient g: 0.23–0.25 d−1; daily percent loss of production Pp: 36–47%), they were unlikely to control it, while in contrast, microzooplankton appeared to play a major role in controlling the late summer/autumn bloom (grazing coefficient g: 0.14–1.53 d−1; daily percent loss of production Pp: 24–103%). In doing so, we suggest that any simplifications that consider these seasonal blooms to be relatively homogeneous and similar will lead to substantial errors in the assessment of coastal trophodynamics.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Banse, K. 1982. Cell volumes, maximal growth rates of unicellular algae and ciliates, and the role of ciliates in the marine pelagial. Limnology and Oceanography 27 (6): 1059–1071.

    Google Scholar 

  • Calbet, A., I. Trepat, R. Almeda, V. Saló, E. Saiz, J.I. Movilla, M. Alcaraz, L. Yebra, and R. Simó. 2008. Impact of micro- and nanograzers on phytoplankton assessed by standard and size-fractionated dilution grazing experiments. Aquatic Microbial Ecology 50: 145–156.

    Google Scholar 

  • Calbet, A., R.A. Martínez, S. Isari, S. Zervoudaki, J.C. Nejstgaard, P. Pitta, A.F. Sazhin, D. Sousoni, A. Gomes, S.A. Berger, T.M. Tsagaraki, and R. Ptacnik. 2012. Effects of light availability on mixotrophy and microzooplankton grazing in an oligotrophic plankton food web: Evidences from a mesocosm study in eastern Mediterranean waters. Journal of Experimental Marine Biology and Ecology 424-425: 66–77.

    Google Scholar 

  • Carey, P. 1992. Marine interstitial ciliates: An illustrated key. London: Chapman & Hall.

    Google Scholar 

  • Dolan, J.R., C.L. Gallegos, and A. Moigis. 2000. Dilution effects on microzooplankton in dilution grazing experiments. Marine Ecology Progress Series 200: 127–139.

    CAS  Google Scholar 

  • Field, C.B., M.J. Behrenfeld, J.T. Randerson, and P. Falkowski. 1998. Primary production of the biosphere: Integrating terrestrial and oceanic components. Science 281 (5374): 237–240.

    CAS  Google Scholar 

  • Fileman, E.S., and R.J.G. Leakey. 2005. Microzooplankton dynamics during the development of the spring bloom in the north-East Atlantic. Journal of the Marine Biological Association of the United Kingdom 85 (4): 741–753.

    CAS  Google Scholar 

  • Franke, H.D., F. Buchholz, and K.H. Wiltshire. 2004. Ecological long-term research at Helgoland (German bight, North Sea): Retrospect and prospect-an introduction. Helgoland Marine Research 58 (4): 223–229.

    Google Scholar 

  • Franze, G., and M. Modigh. 2013. Experimental evidence for internal predation in microzooplankton communities. Marine Biology 160 (12): 3103–3112.

    Google Scholar 

  • Gallegos, C.L. 1989. Microzooplankton grazing on phytoplankton in the Rhode River, Maryland: Nonlinear feeding kinetics. Marine Ecology Progress Series 57: 23–33.

    Google Scholar 

  • Grattepanche, J.D., D. Vincent, E. Breton, and U. Christaki. 2011. Microzooplankton herbivory during the diatom-Phaeocystis spring succession in the eastern English Channel. Journal of Expimental Marine Biology and Ecology 404 (1-2): 87–97.

    Google Scholar 

  • Greve, W., F. Reiners, J. Nast, and S. Hoffmann. 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. Helgoland Marine Research 58 (4): 274–288.

    Google Scholar 

  • Hansen, P.J. 1991. Dinophysis-a planktonic dinoflagellate genus which can act both as a prey and a predator of a ciliate. Marine Ecology Progress Series 69: 201–204.

    Google Scholar 

  • Hansen, P.J., L.T. Nielsen, M. Johnson, T. Berge, and K.J. Flynn. 2013. Acquired phototrophy in Mesodinium and Dinophysis--a review of cellular organization, prey selectivity, nutrient uptake and bioenergetics. Harmful Algae 28: 126–139.

    CAS  Google Scholar 

  • Hartmann, M., C. Grob, G.A. Tarran, A.P. Martin, P.H. Burkill, D.J. Scanlan, and M.V. Zubkov. 2012. Mixotrophic basis of Atlantic oligotrophic ecosystems. PNAS 109 (15): 5756–5760.

    CAS  Google Scholar 

  • Irigoien, X., K.J. Flynn, and R.P. Harris. 2005. Phytoplankton blooms: A loophole in microzooplankton grazing impact? Journal of Plankton Research 27 (4): 313–321.

  • Jeong, H.J., J.Y. Yoon, J.S. Kim, Y.D. Yoo, and K.A. Seong. 2002. Growth and grazing rates of the prostomatid ciliate Tiarina fusus on red-tide and toxic algae. Aquatic Microbial Ecology 28: 289–297.

    Google Scholar 

  • Jeong, H.J., Y.D. Yoo, J.S. Kim, K.A. Seong, N.S. Kang, and T.H. Kim. 2010. Growth, feeding and ecological roles of the mixotrophic and heterotrophic dinoflagellates in marine planktonic food webs. Ocean Science Journal 45 (2): 65–91.

    CAS  Google Scholar 

  • Johnson, M.D. 2011. Acquired phototrophy in ciliates: A review of cellular interactions and structural adaptations. Journal of Eukaryotic Microbiology 58 (3): 185–195.

    Google Scholar 

  • Johnson, M.D., D.K. Stoecker, and H.G. Marshall. 2013. Seasonal dynamics of Mesodinium rubrum in Chesapeake Bay. Journal of Plankton Research 35 (4): 877–893.

    Google Scholar 

  • Kraberg, A.C., M. Baumann, and C.D. Dürselen. 2010. Coastal phytoplankton-photo guide for northern European seas. München: Verlag Dr. Freidrich Pfeil.

    Google Scholar 

  • Landry, M.R., and R.P. Hassett. 1982. Estimating the grazing impact of marine microzooplankton. Marine Biology 67 (3): 283–288.

    Google Scholar 

  • Landry, M.R., and A. Calbet. 2004. Microzooplankton production in the oceans. ICES Journal of Marine Science 61 (4): 501–507.

    Google Scholar 

  • Latasa, M. 2014. Comment: A potential bias in the databases of phytoplankton growth and microzooplankton grazing rates because of the improper formulation of the null hypothesis in dilution experiments. Limnology and Oceanography 59 (3): 1092–1094.

    Google Scholar 

  • Löder, M.G.J., N. Aberle, C. Klaas, A.C. Kraberg, and K.H. Wiltshire. 2010. Conserving original in situ diversity in microzooplankton grazing set-ups. Marine Biodiversity Records 3: 1–9.

    Google Scholar 

  • Löder, M.G.J., C. Meunier, K.H. Wiltshire, M. Boersma, and N. Aberle. 2011. The role of ciliates, heterotrophic dinoflagellates and copepods in structuring spring plankton communities at Helgoland roads, North Sea. Marine Biology 158 (7): 1551–1580.

    Google Scholar 

  • Longhurst, A. 1995. Seasonal cycles of pelagic production and consumption. Progress in Oceanography 36 (2): 77–167.

    Google Scholar 

  • Miller, C.B., and P.A. Wheeler. 2012. Biological oceanography. John Wiley & Sons.

  • Mitra, A., K.J. Flynn, J.M. Burkholder, T. Berge, A. Calbet, J.A. Raven, E. Granéli, P.M. Glibert, P.J. Hansen, D.K. Stoecker, F. Thingstad, U. Tillmann, S. Våge, S. Wilken, and M.V. Zubkov. 2014. The role of mixotrophic protists in the biological carbon pump. Biogeosciences 11 (4): 995–1005.

    Google Scholar 

  • Montagnes, D.J.S., D.H. Lynn, J.C. Roff, and W.D. Taylor. 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. Marine Biology 99 (1): 21–30.

    Google Scholar 

  • Montagnes, D.J.S., and D.H. Lynn. 1989. The annual cycle of Mesodinium rubrum in the waters surrounding the isles of shoals, gulf of Maine. Journal of Plankton Research 11 (2): 193–201.

    Google Scholar 

  • Montagnes, D.J.S., and D.H. Lynn. 1991. Taxonomy of the major groups of marine planktonic ciliates, with emphasis on the aloricate forms. Marine Microbial Food Webs 5: 59–74.

    Google Scholar 

  • Montagnes, D.J.S., and E.J. Lessard. 1999. Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: Its potential to control phytoplankton blooms. Aquatic Microbial Ecology 20 (2): 167–181.

    Google Scholar 

  • Park, M.G., S. Kim, H.S. Kim, G. Myung, Y.G. Kang, and W. Yih. 2006. First successful culture of the marine dinoflagellate Dinophysis acuminata. Aquatic Microbial Ecology 45: 101–106.

    Google Scholar 

  • Polis, G.A., and R.D. Holt. 1992. Intraguild predation: The dynamics of complex trophic interactions. Trends in Ecology and Evolution 7 (5): 151–154.

    CAS  Google Scholar 

  • Quinlan, E.L., C.H. Jett, and E.J. Phlips. 2009. Microzooplankton grazing and the control of phytoplankton biomass in the Suwannee River estuary, USA. Hydrobiologia 632 (1): 127–137.

    Google Scholar 

  • Raven, J.A. 1997. Phagotrophy in phototrophs. Limnology and Oceanography 42 (1): 198–205.

    CAS  Google Scholar 

  • Schmoker, C., S. Hernández-León, and A. Calbet. 2013. Microzooplankton grazing in the oceans: Impacts, data variability, knowledge gaps and future directions. Journal of Plankton Research 35 (4): 691–706.

    Google Scholar 

  • Smetacek, V. 1981. The annual cycle of protozooplankton in the Kiel bight. Marine Biology 63 (1): 1–11.

    Google Scholar 

  • Smalley, G.W., D.W. Coats, and D.K. Stoecker. 2003. Feeding in the mixotrophic dinoflagellate Ceratium furca is influenced by intracellular nutrient concentrations. Marine Ecology Progress Series 262: 137–151.

    Google Scholar 

  • Song, W.B., A. Warren, and X.Z. Hu. 2009. Free-living ciliates in the Bohai and yellow seas, China. Beijing: Science Press.

    Google Scholar 

  • Stoecker, D.K., P.J. Hansen, D.A. Caron, and A. Mitra. 2017. Mixotrophy in the marine plankton. Annual Review of Marine Science 9 (1): 311–335.

    Google Scholar 

  • Sverdrup, H.U. 1953. On conditions for the vernal blooming of phytoplankton. ICES Journal of Marine Science 18 (3): 287–295.

    Google Scholar 

  • Tamigneaux, E., M. Mingelbier, B. Klein, and L. Legendre. 1997. Grazing by protists and seasonal changes in the size structure of protozooplankton and phytoplankton in a temperate nearshore environment (western gulf of St. Lawrence, Canada). Marine Ecology Progress Series 146: 231–247.

    Google Scholar 

  • Thingstad, T.F., H. Havskum, K. Garde, and B. Riemann. 1996. On the strategy of "eating your competitor": A mathematical analysis of algal mixotrophy. Ecology 77 (7): 2108–2118.

    Google Scholar 

  • Wang, Q., Z. Lyu, S. Omar, S. Cornell, Z. Yang, and D.J.S. Montagnes. 2019. Predicting temperature impacts on aquatic productivity: Questioning the metabolic theory of ecology's "canonical" activation energies. Limnology and Oceanography 64 (3): 1172–1185.

    Google Scholar 

  • Wiltshire, K.H., and C.D. Dürselen. 2004. Revision and quality analyses of the Helgoland Reede long-term phytoplankton data archive. Helgoland Marine Research 58 (4): 252–268.

    Google Scholar 

  • Wiltshire, K.H., M. Boersma, K. Carstens, A.C. Kraberg, S. Peters, and M. Scharfe. 2015. Control of phytoplankton in a shelf sea: Determination of the main drivers based on the Helgoland roads time series. Journal of Sea Research 105: 42–52.

    Google Scholar 

  • Worden, A.Z., and B.J. Binder. 2003. Application of dilution experiments for measuring growth and mortality rates among Prochlorococcus and Synechococcus populations in oligotrophic environments. Aquatic Microbial Ecology 30: 159–174.

    Google Scholar 

Download references

Acknowledgements

We would like to thank Silvia Peters for her help in the laboratory and the crew of the research vessel Aade for helping to take samples. Special thanks to Dr. Nicole Aberle for her help in the setting-up of the experiments and the whole team of the AWI Food-Web Project for their helpful discussions.

Funding

This work was supported by grants from the National Natural Science Foundation of China (Nos. 41606168) and the Natural Science Foundation of Guangdong Province, China (No. 2016A030310200).

Author information

Authors and Affiliations

  1. School of Marine Sciences, Sun Yat-Sen University, Guangzhou, 510006, China

    Jinpeng Yang

  2. Guangdong Provincial Key Laboratory of Marine Resources and Coastal Engineering, Guangzhou, 510006, China

    Jinpeng Yang

  3. Southern Marine Science and Engineering Guangdong Laboratory (Zhuhai), Zhuhai, 519000, China

    Jinpeng Yang

  4. Alfred Wegener Institute, Helmholtz Center for Polar and Marine Research, Biologische Anstalt Helgoland, P. O. Box 180, 27483, Helgoland, Germany

    Jinpeng Yang, Martin Günter Joachim Löder & Karen Helen Wiltshire

  5. Department of Animal Ecology I and BayCEER, University of Bayreuth, Universitätsstr. 30, 95440, Bayreuth, Germany

    Martin Günter Joachim Löder

  6. Institute of Integrative Biology, University of Liverpool, BioScience Building, Crown Street, Liverpool, L697ZB, UK

    David J. S. Montagnes

Authors
  1. Jinpeng Yang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Martin Günter Joachim Löder
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Karen Helen Wiltshire
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. David J. S. Montagnes
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Jinpeng Yang or David J. S. Montagnes.

Additional information

Communicated by Wim J. Kimmerer

Electronic supplementary material

ESM 1

(DOCX 481 kb)

ESM 2

(XLSX 50 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yang, J., Löder, M.G.J., Wiltshire, K.H. et al. Comparing the Trophic Impact of Microzooplankton during the Spring and Autumn Blooms in Temperate Waters. Estuaries and Coasts 44, 189–198 (2021). https://doi.org/10.1007/s12237-020-00775-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12237-020-00775-4

Keywords

Search

Navigation