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The colonization of two Phaeocystis species (Prymnesiophyceae) by pennate diatoms and other protists: a significant contribution to colony biomass

Biogeochemistry volume 83, pages 137–145 (2007)Cite this article

Abstract

The association of Phaeocystis spp. with small pennate diatoms during three Phaeocystis-dominated spring blooms were investigated in the Eastern English Channel (2003 and 2004) and in coastal waters of Western Norway during a mesocosm experiment (2005). In each of these studies, colonization of the surface of large Phaeocystis spp. colonies by small needle-shaped diatoms (Pseudo-nitzschia spp.) were observed. In the English Channel the diatom Pseudo-nitzschia delicatissima colonized the surface of large (>100 μm) Phaeocystis globosa colonies. The abundance of Pseudo-nitzschia delicatissima reached 130 cells per colony and formed up to 70% of the total carbon associated with Phaeocystis cells during late bloom stages. In Norwegian waters, the surface of large (>250 μm) Phaeocystis pouchetii colonies were colonized by Pseudo-nitzschia cf. granii var. curvata and to a lesser degree by other phytoplankton and protist species, although the abundance of these diatoms was never greater than 40 cells per colony. Based on these observations we suggest that diatoms utilize Phaeocystis colonies not only as habitat, but that they are able to utilize the colonial matrix as a growth substrate. Furthermore, these observations indicate that a considerable fraction of biomass (chlorophyll) associated with Phaeocystis colonies, especially large colonies concerned with intense and prolonged blooms, are due to co-occurring plankton species and not exclusively Phaeocystis cells.

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Notes

  1. In a recent article (a combination of the morphological and molecular findings) Pseudo-nitzschia delicatissima was shown to be a complex of three different species (Pseudo-nitzschia delicatissima, P. decipiens sp. nov. and P. dolorosa sp. nov. (Lundholm et al. 2006).

References

  • Arndt CE, Fernandez-Leborans G, Seuthe L, Berge J, Gulliksen B (2005) Ciliated epibionts on the Arctic sympagic amphipod Gammarus wilkitzkii as indicators for sympago-benthic coupling. Mar Biol 147:643–652

    Article  Google Scholar 

  • Fernandez-Leborans G, Tato-Porto ML (2000) A review of the species of protozoan epibionts on crustaceans II. Suctorian ciliates. Crustaceana 73:1205–1237

    Article  Google Scholar 

  • Graham LE, Wilcox LW (2000) Algae. Prentice-Hall, NY, 700 p

  • Hamm CE (2000) Architecture, ecology and biogeochemistry of Phaeocystis colonies. J Sea Res 43:307–315

    Article  Google Scholar 

  • Hamm CE, Rousseau V (2003) Composition, assimilation and degradation of Phaeocystis globosa-derived fatty acids in the North Sea. J Sea Res 50:271–283

    Article  Google Scholar 

  • Hamm CE, Simson D, Merkel L, Smetacek V (1999) Colonies of Phaeocystis globosa are protected by a thin but tough skin. Mar Ecol Prog Ser 187:101–111

    Google Scholar 

  • Hasle GR (1964) Nitzschia and Fragilariopsis species studied in the light and electron microscopes. 1. Some marine species of the groups Nitzschiella and Lanceolatae. Skrifter utgitt av Det Norske Videnskaps-Akademi i Oslo. I. Matematisk-Naturvidenskapelig Klasse. Ny Serie 16:1–48

  • Hasle GR, Syvertsen EE (1997) Marine Diatoms. In: Tomas CR (ed) Identifying marine phytoplankton. Academic Press, San Diego, pp 5–385

  • Hasle GR, Lange CB, Syvertsen EE (1996) A review of Pseudo-nitzschia, with special reference to the Skagerrak, North Atlantic, and adjacent waters. Helgol Meeres 50:131–175

    Article  Google Scholar 

  • Hilst CM, Smith WO Jr (2002) Photosynthesis/irradiance relationships in the Ross Sea, Antarctica, and their control by phytoplankton assemblage composition and environmental factors. Mar Ecol Prog Ser 226:1–12

    Google Scholar 

  • Irigoien X, Meyer B, Harris R, Harbour D (2004) Using HPLC pigment analysis to investigate phytoplankton taxonomy: the importance of knowing your species. Helgol Mar Res 58:77–82

    Article  Google Scholar 

  • Lewin J, Hellebust JA (1976) Heterotrophic nutrition of the marine pennate diatom Nitzschia angularis var. affinis. Mar Biol 36(4):313–320

    Article  Google Scholar 

  • Lundholm N, Moestrup Ø, Kotaki Y, Hoef-Emden K, Scholin C, Miller P (2006) Inter- and intraspecific variation of the Pseudo-nitzschia delicatissima complex (Bacillariophyceae) illustrated by RRNA probes, morphological data and phylogenetic analyses. J Phycol 42:464–481

    Article  Google Scholar 

  • Menden-Deuer S, Lessard EJ (2000) Carbon to volume relationship for dinoflagellates, diatoms and other protists plankton. Limnol Oceanogr 45(3):569–579

    Article  Google Scholar 

  • Miralto A, Barrone G, Romano G, Poulet SA, Ianora A, Russo GL, Buttino I, Mazzarella G, Laabir M, Cabrini M, Giacobbe MG (1999) The insidious effect of diatoms on copepod reproduction. Nature 42:174–176

    Google Scholar 

  • Molloy CJ, Syrett PJ (1988) Interrelationships between uptake of urea and uptake of ammonium by microalgae. J Exp Mar Biol Ecol 118:85–95

    Article  Google Scholar 

  • Naumann E (1922) Zwei neue typen von planktonkammern. Z Wiss Mikrosk 39:163–164

    Google Scholar 

  • Nejstgaard JC, Frischer ME, Verity PG, Anderson JT, Jacobsen A, Zirbel MJ, Larsen A, Martinez-Martinez J, Sazhin AF, Walters T, Bronk DA, Whipple SJ, Borrett SR, Patten BC, Long JD (2006) Plankton development and trophic transfer in sea water enclosures added nutrients and P. pouchetii. Mar Ecol Prog Ser (in press, forthcoming publications, No M 6307)

  • Peperzak L, Colijn F, Gieskes WWC, Peeters JCH (1998) Development of the diatom-Phaeocystis spring bloom in the Dutch coastal zone of the North Sea: the silicon depletion versus the daily irradiance threshold hypothesis. J Plankton Res 20:517–537

    Article  Google Scholar 

  • Petterson K, Sahlsten E (1990) Diet patterns of combined nitrogen uptake and intracellular storage of nitrate by phytoplankton in the open Skagerrak. J Exp Mar Biol Ecol 138:167–182

    Article  Google Scholar 

  • Pouchet MG (1892) Sur une algue pélagique nouvelle. CR Séances Soc Biol 44:34–36

    Google Scholar 

  • Priisholm K, Moestrup Ø, Lundholm N (2002) Taxonomic notes on the marine diatom genus Pseudo-nitzschia in the Andaman Sea near the island of Phuket, Thailand, with a description of Pseudo-nitzschia micropora sp. nov. Diatom Res 17(1):153–175

    Google Scholar 

  • Proshkina-Lavrenko AI (1963) Benthic Diatoms of the Black Sea. Academy of Sciences of the USSR, Moscow-Leningrad, 237 p (in Russian)

  • Rijssel M, Hamm CE, Gieskes WWC (1997) Phaeocystis globosa (Prymnesiophyceae) colonies: hollow structures built with small amounts of polysaccharides. Eur J Phycol 32:185–192

    Google Scholar 

  • Rousseau V, Mathot S, Lancelot C (1990) Calculating carbon biovolume of Phaeocystis sp. from microscopic observations. Mar Biol 107(2):305–314

    Article  Google Scholar 

  • Rousseau V, Vaulot D, Casotti D, Cariou V, Lenz J, Gunkel J, Baumann M (1994) The life cycle of Phaeocystis (Prymnesiophyceae): evidence and hypotheses. J Mar Syst 5:23–39

    Article  Google Scholar 

  • Sapozhnikov FV (2003) Colonial Diatoms – satellites of Mussels-filtrators. Ecol Sea 64:13–17 (in Russian)

    Google Scholar 

  • Schoemann V, Becquevort S, Stefels J, Rousseau V, Lancelot C (2005) Phaeocystis blooms in the global ocean and their controlling mechanisms: a review. J Sea Res 53(1–2):43–66

    Article  Google Scholar 

  • Sherr EB, Caron DA, Sherr BF (2000) Staining of heterotrophic Protists for visualization via Epifluorescence Microscopy. In: Kemp PF et al (eds) Handbook of methods in Aquatic microbial ecology. Levis publishers, pp 213–227

  • Shields AR, Smith WO Jr (2005) A novel technique to examine the role of colonial Phaeocystis antarctica in the microbial loop of the Ross Sea, Antarctica. In: Thesis SCOR working group ( 120. Phaeocystis, major link in the biogeochemical cycling of elements, 30 August–3 September 2005. University of Groningen, Haren, The Netherlands, pp 54–55

  • Sukhanova IN, Flint MV (2001) Phaeocystis pouchetii at the Eastern Bering Sea shelf. Oceanology 41(1):75–85

    Google Scholar 

  • Throndsen J, Hasle GR, Tangen K (2003) Norsk Kystplankton Flora. Almater Forlag AS, Oslo, 341 p

  • Wassmann P, Rat’kova T, Andreassen I, Vernet M, Pedersen G, Rey F (1999) Spring bloom development in the Marginal ice zone and the Central Barents Sea. Mar Ecol 20(3–4): 321–346

    Article  Google Scholar 

  • Whipple SJ, Patten BC, Verity PG (2005) Life cycle of the marine alga Phaeocystis: a conceptual model to summarize literature and guide research. J Mar Syst 57:83–110

    Article  Google Scholar 

Download references

Acknowledgments

We are indebted to Dr. Lucie Courcot from Universite du Littoral Cote d’Opale, Wimereux, France for SEM photographs that were useful for identification of the Pseudo-nitzschia delicatissima. We thank the crews of R.V. Sepia II and Côtes de la Manche for their help during cruises in the Eastern English Channel, as well as staff of Université of Littoral and University of Bergen for their technical support and help. Anna Boyette (Skidaway Institute of Oceanography) prepared the figures. This work was part of CPER “Bloom of Phaeocystis” and “PNEC Manche Orientale” French regional and national programs for Eastern Channel Monitoring. Jens C. Nejstgaard was supported by the Norwegian Research Council (152714/120). This study was also funded by the US National Science Foundation Office of Polar Programs grant (OPP−00-83381) and the US Department of Energy Biotechnology Investigations–Ocean Margins Program (FG02-98EF 62531).

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Authors and Affiliations

  1. P.P. Shirshov Institute of Oceanology RAS, Nakhimovsky Prospect, Moscow, 117851, Russia

    Andrey F. Sazhin

  2. UMR 8013 ELICO (FORTEC), MREN-Universite du Littoral Cote d’Opale, Wimereux, France

    L. Felipe Artigas

  3. Department of Biology, University of Bergen, Bergen, Norway

    Jens C. Nejstgaard

  4. Skidaway Institute of Oceanography, Savannah, GA, 31411, USA

    Marc E. Frischer

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  1. Andrey F. Sazhin
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  2. L. Felipe Artigas
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  3. Jens C. Nejstgaard
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Correspondence to Andrey F. Sazhin.

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Sazhin, A.F., Artigas, L.F., Nejstgaard, J.C. et al. The colonization of two Phaeocystis species (Prymnesiophyceae) by pennate diatoms and other protists: a significant contribution to colony biomass. Biogeochemistry 83, 137–145 (2007). https://doi.org/10.1007/s10533-007-9086-2

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Keywords

  • Biomass estimate, colonies
  • Colonization
  • Phaeocystis bloom
  • Pseudo-nitzschia species