, Volume 83, Issue 1–3, pp 311–330 | Cite as

Current understanding of Phaeocystis ecology and biogeochemistry, and perspectives for future research

  • Peter G. VerityEmail author
  • Corina P. Brussaard
  • Jens C. Nejstgaard
  • Maria A. van Leeuwe
  • Christiane Lancelot
  • Linda K. Medlin
Review Paper


The phytoplankton genus Phaeocystis has well-documented, spatially and temporally extensive blooms of gelatinous colonies; these are associated with release of copious amounts of dimethyl sulphide (an important climate-cooling aerosol) and alterations of material flows among trophic levels and export from the upper ocean. A potentially salient property of the importance of Phaeocystis in the marine ecosystem is its physiological capability to transform between solitary cell and gelatinous colonial life cycle stages, a process that changes organism biovolume by 6–9 orders of magnitude, and which appears to be activated or stimulated under certain circumstances by chemical communication. Both life-cycle stages can exhibit rapid, phased ultradian growth. The colony skin apparently confers protection against, or at least reduces losses to, smaller zooplankton grazers and perhaps viruses. There are indications that Phaeocystis utilizes chemistry and/or changes in size as defenses against predation, and its ability to create refuges from biological attack is known to stabilize predator–prey dynamics in model systems. Thus the life cycle form in which it occurs, and particularly associated interactions with viruses, determines whether Phaeocystis production flows through the traditional “great fisheries” food chain, the more regenerative microbial food web, or is exported from the mixed layer of the ocean.

Despite this plethora of information regarding the physiological ecology of Phaeocystis, fundamental interactions between life history traits and system ecology are poorly understood. Research summarized here, and described in the various papers in this special issue, derives from a central question: how do physical (light, temperature, particle distributions, hydrodynamics), chemical (nutrient resources, infochemistry, allelopathy), biological (grazers, viruses, bacteria, other phytoplankton), and self-organizational mechanisms (stability, indirect effects) interact with life-cycle transformations of Phaeocystis to mediate ecosystem patterns of trophic structure, biodiversity, and biogeochemical fluxes? Ultimately the goal is to understand and thus predict why Phaeocystis occurs when and where it does, and the bio-feedbacks between this keystone species and the multitrophic level ecosystem.


Biocomplexity Plankton life cycles Phaeocystis Viruses Zooplankton 



This special issue of Biogeochemistry represents the culmination of extensive efforts by many scientists involved in various aspects of Phaeocystis research. Integration of their activities would not have been possible without the support of the scientific committee on ocean research (SCOR) (, accessed 6/30/06). SCOR working group #120 was devoted to Phaeocystis studies; chair and co-chair were W.W.C. Gieskes and S. Belviso, respectively. We thank E. Urban at SCOR and the organizers and participants of the Phaeocystis workshops held in 2002 (University of East Anglia, UK), 2004 (Savannah, GA, USA), and 2005 (University of Groningen, The Netherlands). Participation by the senior author in the research and SCOR activities reported here was provided by USA National Science Foundation grant OPP-00-83381 and Department of Energy grant FG02-98ER62531. We thank G. Malin, J. Stefels, and W.W.C. Gieskes for improvements to an earlier draft, and A. Boyette for drafting the figure.


  1. Admiraal W, Veldhuis MJW (1987) Determination of nucleosides and nucleotides in seawater by HPLC: application to phosphatase activity in cultures of the alga Phaeocystis pouchetii. Mar Ecol Prog Ser 36:277–285Google Scholar
  2. Alcaraz M, Paffenhöfer G-A, Strickler JR (1980) Catching the algae: a first account of visual observations of filter-feeding copepods. In: Kerfoot WC (ed) Evolution and ecology of zooplankton communities. Univ. Press of New England, Hanover, NH, pp 241–248Google Scholar
  3. Alderkamp A-C, Buma AGJ, van Rijssel M The carbohydrates of Phaeocystis and their degradation in the microbial food web. Biogeochemistry. doi:10.1007/s10533-007-9078-2Google Scholar
  4. Alderkamp A-C, Nejstgaard JC, Verity PG, Zirbel MJ, Sazhin AF, van Rijssel M (2006) Dynamics in carbohydrate composition of Phaeocystis pouchetii colonies during spring blooms in mesocosms. J Sea Res 55:169–181Google Scholar
  5. Anderson TR (2005) Plankton functional type modeling: running before we can walk? J Plankton Res 27:1073–1081Google Scholar
  6. Anderson DM, Cembella AD, Hallegraeff GM (1998) Physiological ecology of harmful algal blooms. Springer-Verlag, BerlinGoogle Scholar
  7. Armbrust EV et al (2004) The genome of the diatom Thalassiosira pseudonana: ecology, evolution, and metabolism. Science 306:79–86Google Scholar
  8. Arrieta JM, Weinbauer MG, Lute C, Herndl GJ (2004) Response of bacterioplankton to iron fertilization in the Southern Ocean. Limnol Oceanogr 49:799–808CrossRefGoogle Scholar
  9. Arrigo KR, Tagliabue A (2005) Iron in the Ross Sea, Part II: impact of discrete iron addition strategies. J Geophys Res 110, C03010. DOI:10.1029/2004JC002568Google Scholar
  10. Arrigo KR, Worthen DL, Robenson DH (2003) A coupled ocean-ecosystem model of the Ross Sea: 2. Iron regulation of phytoplankton taxonomic variability and primary production. J Geophys Res 108(C7):3231. DOI:10:1029/2001JC000856Google Scholar
  11. Becquevort S, Lancelot C, Schoemann V Experimental study on the role of Fe in the bacterial degradation of organic matter derived from Phaeocystis antarctica. Biogeochemistry. doi:10.1007/s10533-007-9079-1Google Scholar
  12. Bratbak G, Jacobsen A, Heldal M (1998a) Viral lysis of Phaeocystis pouchetii and bacterial secondary production. Aquat Microb Ecol 16:11–16Google Scholar
  13. Bratbak G, Jacobsen A, Heldal M, Nagasaki K, Thingstad F (1998b) Virus production in Phaeocystis pouchetii and its relation to host cell growth and nutrition. Aquat Microb Ecol 16:1–9Google Scholar
  14. Breton E, Rousseau V, Parent J-Y, Ozer J, Lancelot C (2006) Hydroclimatic modulation of diatom/Phaeocystis blooms in nutrient-enriched Belgian coastal waters (North Sea). Limnol Oceanogr 51:1401–1409CrossRefGoogle Scholar
  15. Brussaard CPD, Bratbak G, Baudoux A-C, Ruardij P Phaeocystis and its interaction with viruses. Biogeochemistry. doi:10.1007/s10533-007-9096-0Google Scholar
  16. Brussaard CPD, Kuipers B, Veldhuis MJW (2005a) A mesocosm study of Phaeocystis globosa population dynamics. I. Regulatory role of viruses in bloom control. Harmful Algae 4:859–874Google Scholar
  17. Brussaard CPD, Mari X, Van Bleijswijk JDL, Veldhuis MJW (2005b) A mesocosm study of Phaeocystis globosa population dynamics. II. Significance for the microbial community. Harmful Algae 4:875–893Google Scholar
  18. Buesseler KO, Benitez-Nelson CR, Moran SB, Burd A, Charette M, Cochran JK, Coppola L, Fisher NS, Fowler SW, Gardner WD, Guo LD, Gustafsson O, Lamborg C, Masque P, Miquel JC, Passow U, Santschi PH, Savoye N, Stewart G, Trull T (2006) An assessment of particulate organic carbon to thorium-234 ratios in the ocean and their impact on the application of 234Th as a POC flux proxy. Mar Chem 100:213–233Google Scholar
  19. Butterfield NJ (1997) Plankton ecology and the Proterozoic–Phanerozoic transition. Paleobiology 23:247–262Google Scholar
  20. Canziani GA, Hallam TG (1996) A mathematical model for a Phaeocystis sp. dominated plankton community dynamics. I. The basic model. Nonlin World 3:19–76Google Scholar
  21. Chan AT, Andersen RJ, LeBlanc MJ, Harrison PJ (1980) Algal plating as a tool for investigating allelopathy among marine microalgae. Mar Biol 59:7–13Google Scholar
  22. Chen Q, Mynett A (2004) Predicting algal blooms in the Dutch coast by integrated numerical and fuzzy cellular automata. In: Liong S-Y, Phoon K-K, Babovic V (eds) Proceedings of the 6th international conference on hydroinformatics. World Scientific Publishing Company, Singapore, pp 502–510Google Scholar
  23. Costas E, Aguilera A, Gonzalez-Gil S, Lopez-Rodas V (1993) Contact inhibition: also a control for cell proliferation in unicellular algae? Biol Bull 184:1–5Google Scholar
  24. Derelle E et al (2006) Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci 103:11647–11652Google Scholar
  25. DiTullio GR, Garcia N, Riseman SF, Sedwick PN Effects of iron concentration on the pigment composition of Phaeocystis antarctica in the Ross Sea. Biogeochemistry. doi:10.1007/s10533-007-9080-8Google Scholar
  26. DiTullio GR, Grebmeier JM, Arrigo KR, Lizotte MP, Robinson DH, Leventer A, Barry JB, VanWoert ML, Dunbar RB (2000) Rapid and early export of Phaeocystis antarctica blooms in the Ross Sea, Antarctica. Nature 404:595–598Google Scholar
  27. Dufresne A et al (2003) Genome sequence of the cyanobacterium Prochlorococcus marinus SS120, a nearly minimal oxyphototrophic genome. Proc Natl Acad Sci 100:10020–10025Google Scholar
  28. Dutz J, Klein Breteler WCM, Kramer G (2005) Inhibition of copepod feeding by exudates and transparent exoplymer particles (TEP) derived from a Phaeocystis globosa dominated phytoplankton community. Harmful Algae 4:929–940Google Scholar
  29. Dutz J, Koski M (2006) Low grazing vulnerability in flagellated, solitary cells of the prymnesiophyte Phaeocystis globosa. Limnol Oceanogr 51:1230–1238CrossRefGoogle Scholar
  30. Edvardsen B, Paasche E (1998) Bloom dynamics and physiology of Prymnesium and Chrysochromulina. In: Anderson DM, Cembella AD, Hallegraef GM (eds) The physiological ecology of harmful algal blooms. Springer Verlag, Heidelberg, pp 193–208Google Scholar
  31. Estep KW, Nejstgaard JC, Skjoldal HR, Rey F (1990) Predation by copepods upon natural populations of Phaeocystis pouchetii as a function of the physiological state of the prey. Mar Ecol Prog Ser 67:235–249Google Scholar
  32. Flynn KJ (2005) Castles built on sand: dysfunctionality in plankton models and the inadequacy of dialogue between biologists and modelers. J Plankton Res 27:1205–1210Google Scholar
  33. Friedman MM, Strickler JR (1975) Chemoreception and feeding in the calanoid copepods. Proc Nat Acad Sci USA 72:4185–4188Google Scholar
  34. Gaebler S, Hayes PK, Medlin LK Methods used to reveal genetic diversity in the colony forming prymnesiophyte Phaeocystis antarctica – preliminary results. Biogeochemistry. doi:10.1007/s10533-007-9084-4Google Scholar
  35. Gast RJ, Moran D, Dennett MR, Beaudoin DJ, Caron DA (2006) Studies in protistan diversity in Antarctica. Abstract 57th Annual meeting of the International Society of Protozoologists, June 20–24 (p 24). Lisbon, PortugalGoogle Scholar
  36. Gauthier MJ, Aubert M (1981) Chemical telemediators in the marine environment. In: Duursma EK, Dawson E (eds) Marine organic chemistry: evolution, composition, interactions, and chemistry of organic matter in seawater. Elsevier, Amsterdam, pp 225–257Google Scholar
  37. Gieskes WWC, Leterme SC, Peletier H, Edwards M, Reid PC Annual variation of Phaeocystis colonies Atlantic-wide since 1948, and interpretation of long-term changes in ‘Phaeocystis hotspot’ North Sea. Biogeochemistry. doi:10.1007/s10533-007-9082-6Google Scholar
  38. Gypens N, Lancelot C, Borges AV (2004) Carbon dynamics and CO2 air-sea exchanges in the eutrophied coastal waters of the Southern Bight of the North Sea: a modelling study. Biogeosciences 1:147–157CrossRefGoogle Scholar
  39. Hamm CE, Simson DA, Merkel R, Smetacek V (1999) Colonies of Phaeocystis globosa are protected by a thin but tough skin. Mar Ecol Prog Ser 187:101–111Google Scholar
  40. Hamm C, Reigstad M, Riser CW, Muhlebach A, Wassmann P (2001) On the trophic fate of Phaeocystis pouchetii. VII. Sterols and fatty acids reveal sedimentation of Phaeocystis—derived organic matter via krill fecal strings. Mar Ecol Prog Ser 209:55–69Google Scholar
  41. Jacobsen A (2002) Morphology, relative DNA content, and hypothetical life cycle of Phaeocystis pouchetii (Prymnesiophyceae); with special emphasis on the flagellated cell type. Sarsia 87:338–349Google Scholar
  42. Jacobsen A, Martinez-Martinez J, Verity P, Frischer ME, Sandaa R-A, Larsen A (2005) Are colonies or colonial cells of Phaeocystis pouchetii (Prymnesiophyceae) susceptible to virus infection? American Society of Limnology and Oceanography, Summer Meeting, June 19–24, Santiago de Compostela, Spain Google Scholar
  43. Jacobsen A, Larsen A, Martínez-Martínez J, Frischer ME, Verity PG Are colonies and colonial cells of Phaeocystis pouchetii (Haptophyta) susceptible to viral infection? Aquat Microb Ecol (Subm.)Google Scholar
  44. Janse I, van Rijssel M, van Hall PJ, Gerwig GJ, Gottschal JC, Prins RA (1996) The storage glucan of Phaeocystis globosa (Prymnesiophyceae) cells. J Phycol 32:382–387Google Scholar
  45. Johnston R (1963) Antimetabolites as an aid to the study of phytoplankton nutrition. J Mar Biol Assoc UK 43:409–425CrossRefGoogle Scholar
  46. Kamermans P (1994) Nutritional value of solitary cells and colonies of Phaeocystis sp. for the bivalve Macoma balthica (L.). Ophelia 39:35–44Google Scholar
  47. Keller MD, Bellows WK, Guillard RRL (1989) Dimethyl sulfide production in marine phytoplankton. In: Saltzman ES, Cooper WJ (eds) Biogenic sulfur in the environment. American Chemical Society, Wash DC, pp 167–182Google Scholar
  48. 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 4:915–927Google Scholar
  49. Kwint RLJ, Kramer KJM (1996) Annual cycle of the production and fate of DMS and DMSP in a marine coastal system. Mar Ecol Prog Ser 134:217–224Google Scholar
  50. Lacroix G, Ruddick R, Park Y, Gypens N, Lancelot C (2007) Validation of the 3D biogeochemical model MIRO&CO with field nutrient and phytoplankton data and MERIS-derived surface chlorophyll a images. J Mar Syst 64:66–88Google Scholar
  51. Lalande C (2006) Vertical export of biogenic in the Barents and Chukchi Seas. PhD. Thesis, University of Knoxville, Tennessee, USAGoogle Scholar
  52. Lancelot C, Rousseau V (1994) Ecology of Phaeocystis: the key role of colony forms. In: Green JC, Leadbeater BSC (eds) The haptophyte algae. Clarendon Press, Oxford, pp 229–245Google Scholar
  53. Lancelot C, Billen G, Sournia A, Weisse T, Colijn F, Veldhuis M, Davies A, Wassman P (1987) Phaeocystis blooms and nutrient enrichment in the continental coastal zones of the North Sea. Ambio 16:38–46Google Scholar
  54. Lancelot C, Gypens N, Billen G, Garnier J, Roubeix V (2007) Testing an integrated river-ocean mathematical tool for linking marine eutrophication to land use: the Phaeocystis dominated Belgian coastal zone (Southern North Sea) over the past 50 years. J Mar Syst 64:216–228Google Scholar
  55. Lancelot C, Keller MD, Rousseau V, Smith WO Jr, Mathot S (1998) Autecology of the marine haptophyte Phaeocystis sp. In: Anderson DM, Cembella AD, Hallegraeff GM (eds) Physiological ecology of harmful algal blooms, NATO ASI series, vol G41. Springer-Verlag, Berlin, pp 209–224Google Scholar
  56. Lancelot C, Spitz Y, Gypens N, Ruddick K, Becquevort S, Rousseau V, Lacroix G, Billen G (2005) Modelling diatom–Phaeocystis blooms and nutrient cycles in the Southern Bight of the North Sea: the MIRO model. Mar Ecol Prog Ser 289:63–78Google Scholar
  57. Lange M, Chen Y-Q, Medlin LK (2002) Molecular genetic delineation of Phaeocystis species (Prymnesiophyceae) using coding and non-coding regions of nuclear and plastid genomes. Eur J Phycol 37:77–92Google Scholar
  58. Lange M, Guillou L, Vaulot D, Simon N, Amann RI, Ludwig W, Medlin LK (1996) Identification of the class Prymnesiophyceae and the genus Phaeocystis with ribosomal RNA-targeted nucleic acid probes detected by flow cytometry. J Phycol 32:858–868Google Scholar
  59. Lawton JH, Jones CG (1995) Linking species and ecosystems: organisms as ecosystem engineers. In: Jones CG, Lawton JH (eds) Linking species and ecosystems. Chapman and Hall, NY, pp 141–150Google Scholar
  60. Lewis WM Jr (1986) Evolutionary interpretations of allelochemical interactions in phytoplankton algae. Am Nat 127:184–194Google Scholar
  61. Liss PS, Malin G, Turner SM, Holligan PM (1994) Dimethyl sulfide and Phaeocystis: a review. J Mar Syst 5:41–53Google Scholar
  62. Long JD, Hay ME (2006) When intraspecific exceeds interspecific variance: effects of phytoplankton morphology and growth phase on copepod feeding and fitness. Limnol Oceanogr 51:988–996CrossRefGoogle Scholar
  63. Long JD, Anderson JT, Nejstgaard JC, Verity PG, Hay ME Allelopathy of a bloom-froming marine phytoplankton, Phaeocystis, in mesocosm blooms and laboratory cultures. Aquat Microb Ecol (Subm.)Google Scholar
  64. Lubchenco J, Cubit J (1980) Heteromorphic life histories of certain marine algae as adaptations to variations in herbivory. Ecology 61:676–687Google Scholar
  65. Madhupratap M, Sawant S, Gauns M (2000) A first report on a bloom of the marine prymnesiophycean, Phaeocystis globosa, from the Arabian Sea. Ocean Acta 23:83–90Google Scholar
  66. Mari X, Rassoulzadegan F, Brussaard CPD, Wassmann P (2005) Dynamics of transparent exopolymeric particles (TEP) production by Phaeocystis globosa under N- or P-limitation: a controlling factor of the export/retention balance. Harmful Algae 4:895–914Google Scholar
  67. Medlin LK, Lange M, Baumann MEM (1994) Genetic differentiation among three colony-forming species of Phaeocystis: further evidence for the phylogeny of the Prymnesiophyta. Phycologia 33:199–212Google Scholar
  68. Medlin L, Zingone A A Review: the genus Phaeocystis and its species. Biogeochemistry. doi:10.1007/s10533-007-9087-1Google Scholar
  69. Mock T, Valentin K (2004) Photosynthesis and cold acclimation: molecular evidence from a polar diatom. J Phycol 40:732–741Google Scholar
  70. Nejstgaard JC, Tang KW, Steinke M, Dutz J, Koski M, Antajan E, Long JD Zooplankton grazing on Phaeocystis: a quantitative review and future challenges. Biogeochemistry (in press)Google Scholar
  71. Nichols PD, Skerrat JH, Davidson A, Burton H, McMeekin TA (1991) Lipids of cultured Phaeocystis pouchetii: signatures for food web, biogeochemical and environmental studies in Antarctica and the Southern Ocean. Phytochem 30:3209–3214Google Scholar
  72. Noel MH, Kawachi M, Inouye I (2004) Induced dimorphid life cycle of a coccolithophorid Calytrosphaera sphaeroidea (Prymnesiophyceae). J Phycol 40:112–129Google Scholar
  73. Noordkamp DJB, Gieskes WWC, Gottschal JC, Forney LJ, van Rijssel M (2000) Acrylate in Phaeocystis colonies does not affect the surrounding bacteria. J Sea Res 43:287–296Google Scholar
  74. Noordkamp DJB, Schotten M, Gieskes WWC, Forney LJ, Gottschal JC, van Rijssel M (1998) High acrylate concentrations in the mucus of Phaeocystis globosa colonies. Aquat Microb Ecol 16:45–52Google Scholar
  75. Nygaard K, Tobiesen A (1993) Bacterivory in algae: a survival strategy during nutrient limitation. Limnol Oceanogr 38:273–279CrossRefGoogle Scholar
  76. Pasquer B, Laruelle G, Becquevort S, Schoemann V, Goosse H, Lancelot C (2005) Linking ocean biogeochemical cycles and ecosystem structure and function: results of the complex Swamco-4 model. J Sea Res 53:93–108Google Scholar
  77. 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 versus the daily irradiance threshold hypothesis. J Plankton Res 20:517–537Google Scholar
  78. Peperzak L, Duin RMN, Colijn F, Gieskes WWC (2000) Growth and mortality of flagellates and non-flagellate cells of Phaeocystis globosa (Prymnesiophyceae). J Plankton Res 22:107–119Google Scholar
  79. Pohnert G (2004) Chemical defense strategies of marine organisms. In: Schulz SE (ed) Topics in current chemistry. Springer-Verlag GmBH, Berlin, pp 179–219Google Scholar
  80. Pratt DM (1966) Competition between Skeletonema costatum and Olisthodiscus luteus in Narragansett Bay and in culture. Limnol Oceanogr 11:447–455CrossRefGoogle Scholar
  81. Puerta MVS, Bachvaroff TR, Delwiche CF (2004) The complete mitochondrial genome sequence of the haptophyte Emiliania huxleyi and its relation to heterokonts. DNA Res 11:1–10Google Scholar
  82. Ratkova T, Wassmann P (2002) Seasonal variation and spatial distribution of phyto- and protozooplankton in the central Barents Sea. J Mar Syst 38:47–75Google Scholar
  83. Raven JA (1990) Predictions of Mn and Fe use efficiencies of phototrophic growth as a function of light availability for growth and of C assimilation pathway. New Phytol 116:1–18Google Scholar
  84. Reid PC, Colebrook JM, Matthews JBL, Aiken J (2003) Continuous plankton recorder: concepts and history, from plankton indicator to undulating recorders. Prog Oceanogr 58:117–173Google Scholar
  85. Reigstad M, Wassmann P Does Phaeocystis spp. contribute significantly to vertical export of biogenic matter? Biogeochemistry. doi:10.1007/s10533-007-9093-3Google Scholar
  86. Rousseau V, Chrétiennot-Dinet M-J, Jacobsen A, Verity P, Whipple S The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology. Biogeochemistry doi:10.1007/s10533-007-9085-3Google Scholar
  87. Rousseau V, Vaulot D, Casotti R, Cariou V, Lenz J, Gunkel JJ, Baumann M (1994) The life cycle of Phaeocystis (Prymnesiophyceae): evidence and hypotheses. J Mar Syst 5:23–39Google Scholar
  88. Ruardij P, Veldhuis MJW, Brussaard CPD (2005) Modeling the bloom dynamics of the polymorphic phytoplankter Phaeocystis globosa: impact of grazers and viruses. Harmful Algae 4:941–963Google Scholar
  89. Sanders RW, Wickham SA (1993) Planktonic protozoa and metazoa: predation, food quality, and population control. Mar Microb Food Webs 7:197–223Google Scholar
  90. Sazhin AF, Felipe Artigas L, Nejstgaard JC, Frischer ME Colonization of Phaeocystis species by pennate diatoms and other protists: an important contribution to colony biomass. Biogeochemistry. doi:10.1007/s10533-007-9086-2Google Scholar
  91. Schmidt S, Belviso S, Wassmann P, Thouzeau G, Stefels J, Reigstad M Vernal sedimentation trends in north Norwegian fjords: temporary anomaly in 234Th particulate fluxes related to Phaeocystis pouchetii proliferation. Biogeochemistry. doi:10.1007/s10533-007-9094-2Google Scholar
  92. 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 53:43–66Google Scholar
  93. Schrage M, Peters T (1999) Serious play: how the world’s best companies simulate to innovate. Harvard Business School Press, Cambridge, MDGoogle Scholar
  94. Sedwick PN, Garcia N, Riseman SF, Marsay CM, DiTullio GR Evidence for high iron requirements of colonial Phaeocystis antarctica in the Ross Sea. Biogeochemistry. doi:10.1007/s10533-007-9081-7Google Scholar
  95. Seuront L, Lacheze C, Doubell MJ, Seymour JR, Mitchell JG The influence of Phaeocystis globosa bloom dynamics on microscale spatial patterns of phytoplankton biomass and bulk-phase seawater viscosity. Biogeochemistry. doi:10.1007/s10533-007-9097-zGoogle Scholar
  96. Shenoy DM, Dileep Kumar M Variability in abundance and fluxes of dimethyl sulphide in the Indian Ocean. Biogeochemistry. doi:10.1007/s10533-007-9092-4Google Scholar
  97. Sieburth JMcN (1960) Acrylic acid, an “antibiotic” principle in Phaeocystis blooms in Antarctic waters. Science 132:676–677Google Scholar
  98. Slocum CJ (1980) Differential susceptibility to grazers in two phases of an intertidal alga: advantages of heteromorphic generations. J Exp Mar Biol Ecol 46:99–110Google Scholar
  99. Smaal AC, Twisk F (1997) Filtration and absorption of Phaeocystis cf. globosa by the mussel Mytilus edulis L. J Exp Mar Biol Ecol 209:33–46Google Scholar
  100. Spero HJ (1985) Chemosensory capabilities in the phagotrophic dinoflagellate Gymnodinium fungiforme. J Phycol 21:181–184CrossRefGoogle Scholar
  101. Stanley SM (1973) An ecological theory for the sudden origin of multicellular life in the late Precambrian. Proc Nat Acad Sci USA 70:1486–1489Google Scholar
  102. Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197Google Scholar
  103. Stefels J, Dijkhuizen L (1996) Characteristics of DMSP-lyase in Phaeocystis sp. (Prymnesiophyceae). Mar Ecol Prog Ser 131:307–313Google Scholar
  104. Stefels J, Van Boekel WHM (1993) Production of DMS from dissolved DMSP in axenic cultures of the marine phytoplankton species Phaeocystis sp. Mar Ecol Prog Ser 97:11–18Google Scholar
  105. Stefels J, van Leeuwe MA (1998) Effects of iron and light stress on the biogeochemical composition of Antarctic Phaeocystis sp. (Prymnesiophyceae). I. Intracellular DMSP concentrations. J Phycol 34:486–495Google Scholar
  106. Stefels J, Steinke M, Turner S, Malin G, Belviso S Environmental constraints on the production of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modeling. Biogeochemistry. doi:10.1007/s10533-007-9091-5Google Scholar
  107. Steinke M, Stefels J, Stamhuis E (2006) Dimethyl sulfide triggers search behavior in copepods. Limnol Oceanogr 51:1925–1930CrossRefGoogle Scholar
  108. Stelfox-Widdicombe CE, Archer SD, Burkill PH, Stefels J (2004) Microzooplankton grazing in Phaeocystis and diatom-dominated waters in the southern North Sea in spring. J Sea Res 51:37–51Google Scholar
  109. Strom SL, Loukos H (1998) Selective feeding by protozoa: model and experimental behaviors and their consequences for population stability. J Plankton Res 20:831–846Google Scholar
  110. Strom S, Wolfe G, Holmes J, Stecher H, Shimeneck C, Lambert S, Moreno E (2003) Chemical defense in microplankton. I. Feeding and growth rates of heterotrophic protests on the DMS-producing phytoplankter Emiliania huxleyi. Limnol Oceanogr 48:217–229Google Scholar
  111. Sunda W, Kieber DJ, Kiene RP, Huntsman S (2002) An antioxidant function for DMSP and DMS in marine algae. Nature 418:317–320Google Scholar
  112. Tagliabue A, Arrigo KR (2005) Iron in the Ross Sea: 1. Impact on CO2 fluxes via variation in phytoplankton functional group and non-Redfield stoichiometry. J Geophys Res 110, C03009. DOI: 10.1029/2004JC002531Google Scholar
  113. Tagliabue A, Arrigo KR (2006) Processes governing the supply of iron to phytoplankton in stratified seas. J Geophys Res 111, C06019. DOI: 10.1029/2005JC003363Google Scholar
  114. Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842Google Scholar
  115. Targett NM, Ward JE (1991) Bioactive microalgal metabolites: mediation of subtle ecological interactions in phytophagous suspension-feeding marine invertebrates. Bioorganic Mar Chem 4:91–118Google Scholar
  116. Thingstad F, Billen G (1994) Microbial degradation of Phaeocystis material in the water column. J Mar Syst 5:55–66Google Scholar
  117. Tillmann U (1998) Phagotrophy by a plastidic haptophyte, Prymnesium patelliferum. Aquat Microb Ecol 14:155–160Google Scholar
  118. Turner SM, Nightingale PD, Broadgate W, Liss PS (1995) The distribution of dimethyl sulfide and dimethylsulphoproprionate in Antarctic waters and sea ice. Deep-Sea Res II 42:1059–1080Google Scholar
  119. Uchida T (1977) Excretion of a diatom inhibitory substance by Prorocentrum micans Ehrenberg. Jap J Ecol 27:1–4Google Scholar
  120. Van Alstyne KL (1986) Effects of phytoplankton taste and smell on feeding behavior of the copepod Centropages hamatus. Mar Ecol Prog Ser 34:187–190Google Scholar
  121. van Boekel WHM (1992) Phaeocystis colony mucus components and the importance of calcium ions for stability. Mar Ecol Prog Ser 87:301–305Google Scholar
  122. van 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 226:1–12Google Scholar
  123. van Leeuwe MA, de Baar HJW (2000) Photoacclimation by the Antarctic flagellate Pyramimonas sp. (Prasinophyceae) in response to iron limitation. Eur J Phycol 35:295–303Google Scholar
  124. van Leeuwe MA, Stefels J (1998) Effects of iron and light stress on the biogeochemical composition of Antarctic Phaeocystis sp. (Prymnesiophyceae). II. Pigment composition. J Phycol 34:496–503Google Scholar
  125. van Leeuwe MA, Stefels J Photosynthetic responses in Phaeocystis antarctica towards varying light and iron conditions. Biogeochemistry. doi:10.1007/s10533-007-9083-5Google Scholar
  126. van Rijssel M, Alderkamp A-C, Nejstgaard JC, Sazhin AF, Verity PG Haemolytic activity of living Phaeocystis pouchetii during mesocosm blooms. Biogeochemistry. doi:10.1007/s10533-007-9095-1Google Scholar
  127. van Rijssel M, Hamm CE, Gieskes WWC (1997) Phaeocystis globosa (Prymnesiophyceae) colonies: hollow structures built with small amounts of polysaccharides. Eur J Phycol 32:185–192Google Scholar
  128. Vaulot D, Birrien J-L, Marie D, Casotti R, Veldhuis MJW, Kraaij GW, Chretiennot-Dinet M-J (1994) Morphology, ploidy, pigment composition, and genome size of cultured strains of Phaeocystis (Prymnesiophyceae). J Phycol 30:1022–1035Google Scholar
  129. Veldhuis MJW, Admiraal W (1987) Influence of phosphate depletion on the growth and colony formation of Phaeocystis pouchetii. Mar Biol 95:47–54Google Scholar
  130. Veldhuis MJW, Wassmann P (2005) Bloom dynamics and biological control of a high biomass HAB species in European coastal waters: a Phaeocystis case study. Harmful Algae 4:805–809Google Scholar
  131. Veldhuis MJW, Brussaard CPD, Noordeloos AAM (2005) Living in a Phaeocystis colony: a way to be a successful algal species. Harmful Algae 4:841–858Google Scholar
  132. Veldhuis MJW, Colijn F, Admiraal W (1991) Phosphate utilization in Phaeocystis pouchetii (Haptophyceae). Mar Biol 12:53–62Google Scholar
  133. Verity PG (1988) Chemosensory behavior in marine planktonic ciliates. Bull Mar Sci 43:772–782Google Scholar
  134. Verity PG (1991) Feeding in planktonic protozoans: evidence for non-random acquisition of prey. Mar Microb Food Webs 5:69–76Google Scholar
  135. Verity PG (2000) Grazing experiments and model simulations of the role of zooplankton in Phaeocystis food webs. J Sea Res 43:317–343Google Scholar
  136. Verity PG, Medlin LK (2003) Observations on colony formation by the cosmopolitan phytoplankton genus Phaeocystis. J Mar Syst 43:153–164Google Scholar
  137. Verity PG, Smetacek V (1996) Organism life cycles, predation, and the structure of marine pelagic ecosystems. Mar Ecol Prog Ser 130:277–293Google Scholar
  138. Verity PG, Villareal TA, Smayda TJ (1988a) Ecological investigations of blooms of colonial Phaeocystis pouchetii. I. Abundance, biochemical composition, and metabolic rates. J Plankton Res 10:219–248Google Scholar
  139. Verity PG, Villareal TA, Smayda TJ (1988b) Ecological investigations of blooms of colonial Phaeocystis pouchetii. II. The role of life cycle phenomena in bloom termination. J Plankton Res 10:749–766Google Scholar
  140. Wassmann P (1994) Significance of sedimentation for the termination of Phaeocystis blooms. J. Mar Syst 5:81–100Google Scholar
  141. Wassmann P, Ratkova T, Reigstad M (2005) The contribution of single and colonial cells of Phaeocystis pouchetii to spring and summer blooms in the north-eastern North Atlantic. Harmful Algae 4:823–840Google Scholar
  142. Wassmann P, Slagstad D (1993) Seasonal and annual dynamics of particulate carbon flux in the Barents Sea, a model approach. Polar Biol 13:363–372Google Scholar
  143. Weisse T, Tande K, Verity P, Hansen F, Gieskes W (1994) The trophic significance of Phaeocystis blooms. J Mar Syst 5:67–79Google Scholar
  144. Whipple SJ, Patten BC, Verity PG (2005a) Life cycle of the marine alga Phaeocystis: a conceptual model to summarize literature and guide research. J Mar Syst 57:83–110Google Scholar
  145. Whipple SJ, Patten BC, Verity PG (2005b) Colony growth and evidence for colony multiplication in Phaeocystis pouchetii (Prymnesiophyceae) isolated from mesocosm blooms. J Plankton Res 27:495–501Google Scholar
  146. Whipple SJ, Patten BC, Verity PG, Nejstgaard JC, Long JD, Anderson JT, Jacobsen A, Larsen A, Martinez-Martinez J, Borrett SR. Gaining integrated understanding of Phaeocystis spp. (Prymnesiophyceae) through model-driven laboratory and mesocosm studies. Biogeochemistry. doi:10.1007/s10533-007-9089-2Google Scholar
  147. Wolfe GV (2000) The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. Biol Bull 198:225–244Google Scholar
  148. Wolfe GV, Levasseur M, Cantin G, Michaud S (2000) DMSP and DMS dynamics and microzooplankton grazing in the Labrador Sea: application of the dilution technique. Deep-Sea Res I 47:2243–2264Google Scholar
  149. Wolfe GV, Steinke M, Kirst GO (1997) Grazing-activated chemical defense in a unicellular marine alga. Nature 387:894–897Google Scholar
  150. Wooten EC, Roberts EC (2006) Biochemical recognition of prey by planktonic protozoa. Abstract 57th Annual meeting of the International Society of Protozoologists, June 20–24, 2006 (p 57). Lisbon, Portugal Google Scholar
  151. Yoshida T, Hairston NG, Ellner SP (2004) Evolutionary trade-off between defense against grazing and competitive ability in a simple unicellular alga, Chlorella vulgaris. Proc Royal Soc Lond Ser B, Biol Sci 271:1947–1953Google Scholar
  152. Zingone A, Chretiennot-Dinet M-J, Lange M, Medlin L (1999) Morphological and genetic characterization of Phaeocystis cordata and P. jahnii (Prymnesiophyceae), two new species from the Mediterranean Sea. J Phycol 35:1322–1337Google Scholar

Copyright information

© Springer Science+Business Media, Inc. 2007

Authors and Affiliations

  • Peter G. Verity
    • 1
    Email author
  • Corina P. Brussaard
    • 2
  • Jens C. Nejstgaard
    • 3
  • Maria A. van Leeuwe
    • 4
  • Christiane Lancelot
    • 5
  • Linda K. Medlin
    • 6
  1. 1.Skidaway Institute of OceanographySavannahUSA
  2. 2.Royal Netherlands Institute for Sea ResearchDen BurgThe Netherlands
  3. 3.UNIFOB AS, Department of BiologyUniversity of Bergen, Bergen High Technology CentreBergenNorway
  4. 4.University of Groningen, Biological CentreHarenThe Netherlands
  5. 5.Ecologie des Systèmes AquatiquesUniversité Libre de BruxellesBruxellesBelgium
  6. 6.Alfred Wegener Institute for Polar and Marine ResearchBremerhavenGermany

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