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Zooplankton grazing on Phaeocystis: a quantitative review and future challenges

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Abstract

The worldwide colony-forming haptophyte phytoplankton Phaeocystis spp. are key organisms in trophic and biogeochemical processes in the ocean. Many organisms from protists to fish ingest cells and/or colonies of Phaeocystis. Reports on specific mortality of Phaeocystis in natural plankton or mixed prey due to grazing by zooplankton, especially protozooplankton, are still limited. Reported feeding rates vary widely for both crustaceans and protists feeding on even the same Phaeocystis types and sizes. Quantitative analysis of available data showed that: (1) laboratory-derived crustacean grazing rates on monocultures of Phaeocystis may have been overestimated compared to feeding in natural plankton communities, and should be treated with caution; (2) formation of colonies by P. globosa appeared to reduce predation by small copepods (e.g., Acartia, Pseudocalanus, Temora and Centropages), whereas large copepods (e.g., Calanus spp.) were able to feed on colonies of Phaeocystis pouchetii; (3) physiological differences between different growth states, species, strains, cell types, and laboratory culture versus natural assemblages may explain most of the variations in reported feeding rates; (4) chemical signaling between predator and prey may be a major factor controlling grazing on Phaeocystis; (5) it is unclear to what extent different zooplankton, especially protozooplankton, feed on the different life forms of Phaeocystis in situ. To better understand the mechanisms controlling zooplankton grazing in situ, future studies should aim at quantifying specific feeding rates on different Phaeocystis species, strains, cell types, prey sizes and growth states, and account for chemical signaling between the predator and prey. Recently developed molecular tools are promising approaches to achieve this goal in the future.

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References

  • Aanesen RT, Eilertsen HC, Stabell OB (1998) Light-induced toxic properties of the marine alga Phaeocystis pouchetii towards cod larvae. Aquat Toxicol 40:109–121

    Google Scholar 

  • Admiraal W, Venekamp LAH (1986) Significance of tintinnid grazing during blooms of Phaeocystis pouchetii (haptophyceae) in Dutch coastal waters. Neth J Sea Res 20:61–66

    Google Scholar 

  • Al-Hasan RH, Ali AM, Radwan SS (1990) Lipids, and their constituent fatty-acids, of Phaeocystis sp. from the Arabian Gulf. Mar Biol 105:9–14

    Google Scholar 

  • Alderkamp A-C, Buma AGJ and van Rijssel M (this volume) The carbohydrates of Phaeocystis and their degradation in the microbial food web. Biogeochemistry. doi:10.1007/s10533-007-9078-2

  • 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 55:169–181

    Google Scholar 

  • Archer SD, Stelfox-Widdicombe CE, Malin G, Burkill PH (2003) Is dimethyl sulphide production related to microzooplankton herbivory in the southern North Sea? J. Plankton Res 25:235–242

    Google Scholar 

  • Archer SD, Verity PG, Stefels J (2000) Impact of microzooplankton on the progression and fate of the spring bloom in fjords of northern Norway. Aquat Microb Ecol 22:27–41

    Google Scholar 

  • 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 297–399

    Google Scholar 

  • Banse K (1994) Grazing and zooplankton production as key controls of phytoplankton production in the open ocean. Oceanography 7:13–20

    Google Scholar 

  • Barnard WR, Andreae MO, Iverson RL (1984) Dimethylsulfide and Phaeocystis poucheti in the Southeastern Bering Sea. Cont Shelf Res 3:103–113

    Google Scholar 

  • Baumann MEM, Lancelot C, Brandini FP, Sakshaug E, John DM (1994) The taxonomic identity of the cosmopolitan prymnesiophyte Phaeocystis: a morphological and ecophysiological approach. J Mar Syst 5:5

    Google Scholar 

  • Bautista B, Harris RP, Tranter PRG, Harbour D (1992) In situ copepod feeding and grazing rates during a spring bloom dominated by Phaeocystis sp. in the English Channel. J Plankton Res 14:691–703

    Google Scholar 

  • Blauw AN (this volume) Phaeocystis blooms forecasting in Dutch coastal waters, the impact of suspended matter. Biogeochemistry

  • Breton E, Sautour B, Brylinski J-M (1999) No feeding on Phaeocystis sp. as solitary cells (post bloom period) by the copepod Temora longicornis in the coastal waters of the English Channel. Hydrobiologia 414:13–23

    Google Scholar 

  • Brussaard CPD, Bratbak G, Baudoux A-C and Ruardij P (this volume) Phaeocystis and its interaction with viruses. Biogeochemistry. doi:10.1007/s10533-007-9096-0

  • Brussaard CPD, R. R, Noordeloos AAM, Cadée GC, Witte H, Kop AJ, Nieuwland G, van Duyl FC and 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

  • Bullen GE (1908) Plankton studies in relation to the western mackerel fishery. J Mar Biol Ass UK 8:269–302

    Google Scholar 

  • Caron DA (2005) Introductory remarks: advances in the molecular ecology of protists. J Eukaryot Microbiol 52:81–82

    Google Scholar 

  • Caron DA, Dennett MR, Lonsdale DJ, Moran DM, Shalapyonok L (2000) Microzooplankton herbivory in the Ross Sea, Antarctica. Deep Sea Res Part II Top Stud Oceanogr 47:3249–3272

    Google Scholar 

  • Chen Y-Q, Wang N, Zhang P, Zhou H, Qu L-H (2002) Molecular evidence identifies bloom-forming Phaeocystis (Prymnesiophyta) from coastal waters of southeast China as Phaeocystis globosa. Biochem Syst Ecol 30:15–22

    Google Scholar 

  • Chretiennot-Dinet MJ, Giraud-Guille MM, Vaulot D, Putaux JL, Saito Y, Chanzy H (1997) The chitinous nature of filaments ejected by Phaeocystis (Prymnesiophyceae). J Phycol 33:666–672

    Google Scholar 

  • Claustre H, Poulet SA, Williams R, Marty JC, Coombs S, Benmlih F, Hapette AM, Martinjezequel V (1990) A biochemical investigation of a Phaeocystis sp. bloom in the Irish Sea. J Mar Biol Ass U K 70:197–207

    Google Scholar 

  • Collier JL, Campbell L (1999) Flow cytometry in molecular aquatic ecology. Hydrobiologia 401:33–53

    Google Scholar 

  • Cook PA, Gabbott PA (1972) Seasonal changes in the biochemical composition of adult barnacle, Balanus balanoides, and the possible relationships between biochemical composition and cold-tolerance. J Mar Biol Ass U K 52:805–825

    Google Scholar 

  • Cotonnec G, Brunet C, Sautour B, Thoumelin G (2001) Nutritive value and selection of food particles by copepods during a spring bloom of Phaeocystis sp. in the English Channel, as determined by pigment and fatty acid analyses. J Plankton Res 23:693–703

    Google Scholar 

  • Daro M-H (1985) Field study of the diel, selective and efficiency feeding of the marine copepod Temora longicornis in the Southern Bight of the North Sea. In: Van Grieken R, Wollast R (eds) Proc progress in Belgian oceanographic research, Brussels, pp 250–263

  • Davies AG, Demadariaga I, Bautista B, Fernandez F, Harbour DS, Serret P, Tranter PRG (1992) The ecology of a coastal Phaeocystis bloom in the North-Western English-Channel in 1990. J Mar Biol Ass UK 72:691–708

    Google Scholar 

  • De Bernardi R, Giussani G (1990) Are blue-green algae suitable food for zooplankton? A review. Hydrobiologia 200/201:29–41

    Google Scholar 

  • Dicke M, Sabelis MW (1988) How plants obtain predatory mites as bodyguards. Neth J Zool 38:148–165

    Article  Google Scholar 

  • Dunne T, Doyle J, Parker M (1984) A review of the incidence and effects of unusual marine blooms in Irish coastal waters. ICES Spec Meet ICES CM 1984/D 9:4

  • Dutz J, Klein Breteler WCM, Kramer G (2005) Inhibition of copepod feeding by exudates and transparent exopolymer particles (TEP) derived from a Phaeocystis globosa dominated phytoplankton community. Harmful Algae 4:929

    Google Scholar 

  • Dutz J, Koski M (2006) Trophic significance of solitary cells of the prymnesiophyte Phaeocystis globosa depends on cell type. Limnol Oceanogr 51:1230–1238

    Article  Google Scholar 

  • 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 193–208

    Google Scholar 

  • Eilertsen HC, Raa J (1995) Phytoplankton toxins in sea-water. J Mar Biotechnol 3:115–119

    Google Scholar 

  • Escaravage V, Peperzak L, Prins TC, Peeters JCH, Joordens JCA (1995) The development of a Phaeocystis bloom in a mesocosm experiment in relation to nutrients, irradiance and coexisting algae. Ophelia 42:55–74

    Google Scholar 

  • 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 67:235–249

    Google Scholar 

  • Everitt BS, Dunn G (2001) Applied multivariate data analysis, 2nd edn. Oxford University Press, New York

    Google Scholar 

  • Frangoulis C, Belkhiria S, Goffart A, Hecq J-H (2001) Dynamics of copepod faecal pellets in relation to a Phaeocystis dominated phytoplankton bloom: characteristics, production and flux. J Plankton Res 23:75–88

    Google Scholar 

  • Fransz HG, Gieskes WWC (1984) The unbalance of phytoplankton and copepods in the North Sea. J Cons Int Explor Mer 183:218–225

    Google Scholar 

  • Fransz HG, Gonzalez SR, Cadée GC, Hansen FC (1992) Long-term change of Temora longicornis (copepoda, Calanoida) abundance in a Dutch tidal inlet (Marsdiep) in relation to eutrophication. Neth J Sea Res 30:23–32

    Google Scholar 

  • Fretter V, Montgomery MC (1968) The treatment of food by prosobranch veligers. J Mar Biol Ass UK 48:275–544

    Google Scholar 

  • Frost BW (1972) Effect of size and concentration of food particles on the feeding behaviour of the marine planktonic copepod Calanus pacificus. Limnol Oceanogr 17:805–815

    Article  Google Scholar 

  • Gasparini S, Daro MH, Antajan E, Tackx M, Rousseau V, Parent J-Y, Lancelot C (2000) Mesozooplankton grazing during the Phaeocystis globosa bloom in the southern bight of the North Sea. J Sea Res 43:345–356

    Google Scholar 

  • Goffart A, Catalano G, Hecq JH (2000) Factors controlling the distribution of diatoms and Phaeocystis in the Ross Sea. J Mar Syst 27:161

    Google Scholar 

  • González JM, Sherr EB, Sherr BF (1990) Size-selective grazing on bacteria by natural assemblages of estuarine flagellates and ciliates. Appl Environ Microbiol 56:583–589

    Google Scholar 

  • Gorsky G, Chretiennot-Dinet M-J, Blanchot J, Palazzoli I (1999) Picoplankton and nanoplankton aggregation by appendicularians: fecal pellet contents of Megalocercus huxleyi in the equatorial Pacific. J Geophys Res C 104:3381–3390

    Google Scholar 

  • Greenacre MJ (1984) Theory and applications of correspondence analysis. Academic Press, London

    Google Scholar 

  • Haberman KL, Quetin LB, Ross RM (2003) Diet of the Antarctic krill (Euphausia superba Dana): I. Comparisons of grazing on Phaeocystis antarctica (Karsten) and Thalassiosira antarctica (Comber). J Exp Mar Biol Ecol 283:79– 95

    Google Scholar 

  • Hamm CE, Reigstad M, Wexels Riser C, Mühlebac A, Wassmann P (2001) On the trophic fate of Phaeocystis pouchetii. VII. Sterols and fatty acids reveal sedimentation of P. puchetii-derived organic matter via krill fecal strings. Mar Ecol Prog Ser 209:55–69

    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

    Google Scholar 

  • 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 187:101–111

    Google Scholar 

  • Hansen B, Bjørnsen PK, Hansen PJ (1994a) The size ratio between planktonic predators and their prey. Limnol Oceanogr 39:395–403

    Article  Google Scholar 

  • Hansen B, Tande KS, Berggreen UC (1990) On the trophic fate of Phaeocystis pouchetii (Hariot). III. Functional responses in grazing demonstrated on juvenile stages of Calanus finmarchicus (Copepoda) fed diatoms and Phaeocystis. J Plankton Res 12:1173–1187

    Google Scholar 

  • Hansen B, Verity P, Falkenhaug T, Tande KS, Norrbin F (1994b) On the trophic fate of Phaeocystis pouchetti (Harriot). V. Trophic relationships between Phaeocystis and zooplankton: an assessment of methods and size dependence. J Plankton Res. 16:487–511

    Google Scholar 

  • Hansen E, Eilertsen HC, Ernstsen A, Geneviere A-M (2003) Anti-mitotic activity towards sea urchin embryos in extracts from the marine haptophycean Phaeocystis pouchetii (Hariot) Lagerheim collected along the coast of northern Norway. Toxicon 41:803–812

    Google Scholar 

  • Hansen E, Ernstsen A, Eilertsen HC (2004) Isolation and characterisation of a cytotoxic polyunsaturated aldehyde from the marine phytoplankter Phaeocystis pouchetii (Hariot) Lagerheim. Toxicology 199:207–217

    Google Scholar 

  • Hansen FC (1992) Zooplankton-Grazing an Phaeocystis mit besonderer Berücksichtigung der Calanoiden Copepoden. Institut für Meereskunde Kiel, Christian-Albrechts-Universität, Kiel, Kiel, p 137

    Google Scholar 

  • Hansen FC (1995) Trophic interactions between zooplankton and Phaeocystis cf globosa. Helgol Meeresunters 49:283–293

    Google Scholar 

  • 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 102:51–57

    Google Scholar 

  • Hansen FC, van Boekel WHM (1991) Grazing pressure of the calanoid copepod Temora longicornis on a Phaeocystis dominated spring bloom in a Dutch tidal inlet. Mar Ecol Prog Ser 78:123–129

    Google Scholar 

  • Hansen PJ, Bjørnsen PK, Hansen BW (1997) Zooplankton grazing and growth: scaling within the 2–2,000-μm body size range. Limnol Oceanogr 42:687–704

    Article  Google Scholar 

  • Hay ME, Fenical W (1988) Marine plant-herbivore interactions: the ecology of chemical defense. Annu Rev Ecol Syst 19:111–145

    Google Scholar 

  • Hay ME, Parker JD, Burkepile DE, Caudill CC, Wilson AE, Hallinan ZP, Chequer AD (2004) Mutualisms and aquatic community structure: the enemy of my enemy is my friend. Annu Rev Ecol Evol Syst 35:175–197

    Google Scholar 

  • Hegarty SG, Villareal TA (1988) Effects of light level and N:P supply ratio on the competition between Phaeocystis cf. pouchetii (Hariot) Lagerheim (Prymnesiophyceae) and five diatom species. J Exp Mar Biol Ecol 226:241–258

    Google Scholar 

  • Hollowday ED (1949) A preliminary report on the Plymouth marine and brackish-water rotifera. J Mar Biol Ass UK 28:239–253

    Google Scholar 

  • Houde SEL, Roman MR (1987) Effects of food quality on the functional ingestion response of the copepod Acartia tonsa. Mar Ecol Prog Ser 40:69–77

    Google Scholar 

  • Huntley M, Tande K, Eilertsen HC (1987) On the trophic fate of Phaeocystis pouchetii (Hariot). II. Grazing rates of Calanus hyperboreus (Krøyer) on diatoms and different size categories of Phaeocystis pouchetii. J Exp Mar Biol Ecol 110:197–212

    Google Scholar 

  • Irigoien X, Titelman J, Harris RP, Harbour D, Castellani C (2003) Feeding of Calanus finmarchicus nauplii in the Irminger Sea. Mar Ecol Prog Ser 262:193–200

    Google Scholar 

  • Jakobsen HH, Tang KW (2002) Effects of protozoan grazing on colony formation in Phaeocystis globosa (Prymnesiophyceae) and the potential costs and benefits. Aquat Microb Ecol 27:261–227

    Google Scholar 

  • Jebram D (1980) Prospection for a sufficient nutrition for the cosmopolitic marine bryozoan Electra pilosa (Linnaeus). Zool Jahrb Syst 107:368–390

    Google Scholar 

  • Jones PGV, Haq SM (1963) The distribution of Phaeocystis in the Eastern Irish Sea. J Cons Int Explor Mer 28:8–20

    Google Scholar 

  • Jonker R, Groben R, Tarran G, Medlin L, Wilkins M, Garcia L, Zabala L, Boddy L (2000) Automated identification and characterisation of microbial populations using flow cytometry: the AIMS project. Sci Mar 64:225–234

    Google Scholar 

  • Kamermans P (1994) Nutritional value of solitary cells and colonies of Phaeocystis sp. for the bivalve Macoma balthica (L). Ophelia 39:35–44

    Google Scholar 

  • Keller MD, Bellows WK, Guillard RRL (1989) Dimethyl sulfide production in marine phytoplankton. Acs Symp Ser 393:167–182

    Article  Google Scholar 

  • Klein Breteler WCM, Koski M (2003) Development and grazing of Temora longicornis (Copepoda, Calanoida) nauplii during nutrient limited Phaeocystis globosa blooms in mesocosms. Hydrobiologia 491:185–192

    Google Scholar 

  • Kopp J (1978) Les phénomènes d’eaux colorées ayant affecté le littoral Bas-Normand au cours du mois de juin 1978. Inst Sci Tech Pêches Mar, Centre de Quistreham: 30

  • Kornmann VP (1955) Beobachtungen an Phaeocystis-Kulturen. Helgoländer wiss Meeresunters 5:218–233

    Google Scholar 

  • 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

    Google Scholar 

  • Krogstad PK (1989) Produksjon av planteplankton til bruk som fór i intensivt oppdrett av torskelarver (Gadhus morhua L.) med referanse i ekstensivt oppdrettsystem (poll). Institute of Fisheries, University of Tromsø, Tromsø, p 147

    Google Scholar 

  • Lancelot C, Keller MD, Rousseau V, Smith WOJ, Mathot S (1998) Autecology of the marine haptophyte Phaeocystis sp. In: Anderson DM, Cembella AD, Hallegraef GM (eds) The physiological ecology of harmful algal blooms. Springer Verlag, Berlin, pp 209–224

    Google Scholar 

  • 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 229–245

  • Landry MR, Hassett RP (1982) Estimating the grazing impact of marine micro-zooplankton. Mar Biol 67:283–288

    Google Scholar 

  • Landry MR, Selph KE, Brown SL, et al (2002) Seasonal dynamics of phytoplankton in the Antarctic Polar Front region at 170? W Deep Sea Res Part II Top Stud Oceanogr 49:1843–1865

    Google Scholar 

  • Larsen A, Fonnes Flaten GA, Sandaa R-A, Castberg T, Thyrhaug R, Erga SR, Jacquet S, Bratbak G (2004) Spring phytoplankton bloom dynamics in Norwegian coastal waters: Microbial community succession and diversity. Limnol Oceanogr 49:180–190

    Article  Google Scholar 

  • Lebart L, Morineau A, Lambert T (1988) SPAD.N Système portable pour l’analyse des données. Manuel de référence. (SPAD.N a software for Correspondence Analysis User’s. guide). CISIA, Saint-Mandé, France

  • Lebart L, Morineau A, Piron M (2000) Statistique exploratoire multidimentionnelle. Dunod, Paris

    Google Scholar 

  • Lebour MV (1920) The food of young fish. No. III (1919). J Mar Biol Ass UK 12:261–324

    Google Scholar 

  • Lebour MV (1922) The food of planktonic organisms. J Mar Biol Ass UK 12:644–677

    Google Scholar 

  • Legendre P, Legendre L (1998) Numerical Ecology. Elsevier, Amsterdam

    Google Scholar 

  • Levinsen H, Turner JT, Nielsen TG, Hansen BW (2000) On the trophic coupling between protists and copepods in arctic marine ecosystems. Mar Ecol Prog Ser 204:65–77

    Google Scholar 

  • Lewis WMJ (1986) Evolutionary interpretations of allelochemical interactions in phytoplankton algae. Am Nat 127:184–194

    Google Scholar 

  • Liss PS, Malin G, Turner SM, Holligan PM (1994) Dimethyl sulphide and Phaeocystis: a review. J Mar Syst 5:41

    Google Scholar 

  • Long JD (2004) Plasticity of consumer-prey interactions in the sea: chemical signaling, learned aversions, and ecological consequences. Biology. Georgia Institute of Technology, Atlanta, p 111

  • Long JD, Hay ME (2006) When intraspecific exceeds interspecific variance: effects of phytoplankton morphology and growth phase on copepod feeding and fitness. Limnol Oceanogr 51:988–996

    Article  Google Scholar 

  • Løken S (1990) Næringsøkologi og vekst hos torskelarver (Gadus morhua L.) i poll og intensive system. Institute of Fisheries. University of Tromsø, Tromsø, p 86

    Google Scholar 

  • Lucas CE, Henderson GTD (1936) On the association of jelly-fish and other organisms with catches of herring. J Mar Biol Ass U K 21:293–304

    Google Scholar 

  • Lürling M (2003) Phenotypic plasticity in the green algae Desmodesmus and Scenedesmus with special reference to the induction of defensive morphology. Ann Limnol 39:85–101

    Google Scholar 

  • Lürling M, Van Donk E (1997) Morphological changes in Scenedesmus induced by infochemicals released in situ from zooplankton grazers. Limnol Oceanogr 42:783–788

    Article  Google Scholar 

  • Mathot S, Smith WO, Carlson CA, Garrison DL, Gowing MM, Vickers CL (2000) Carbon partitioning within Phaeocystis antarctica (Prymnesiophyceae) colonies in the Ross Sea, Antarctica. J Phycol 36:1049–1056

    Google Scholar 

  • Medlin L and Zingone A (this volume) A review: the genus Phaeocystis and its species. Biogeochemistry

  • Meixner R (1981) Herzmuschel-Suche mit FA-Niobe im ostfriesischen Wattenmeer. Inf Fischwirtsch 28:133–134

    Google Scholar 

  • Metz C (1998) Feeding of Oncaea curvata (Poecilostomatoida, Copepoda). Mar Ecol Prog Ser 169:229–235

    Google Scholar 

  • Nejstgaard JC, Frischer ME, Raule CL, Gruebel R, Kohlberg KE, Verity PG (2003) Molecular detection of algal prey in copepod guts and faecal pellets. Limnol Oceanogr Methods 1:29–38

    Google Scholar 

  • Nejstgaard JC, Frischer ME, Simonelli P, Brakel M, Sazhin A, Artigas LF (2005) Comparison of molecular and traditional methods to quantify selective copepod feeding in situ ASLO, Summer Meeting. Santiago de Compostela, Spain

  • Nejstgaard JC, Frischer ME, Verity PG, Anderson JT, Jacobsen A, Zirbel MJ, Larsen A, Martínez-Martínez J, Sazhin AF, Walters T, Bronk DA, Whipple SJ, Borett SR, Patten BC, Long JD (2006) Temporal patterns in planktonic food web development in mesocosms with added nutrients and Phaeocystis. Mar Ecol Prog Ser 321:99–121

    Google Scholar 

  • Nejstgaard JC, Naustvoll L-J, Sazhin A (2001) Correcting for underestimation of microzooplankton grazing in bottle incubation experiments with mesozooplankton. Mar Ecol Prog Ser 221:59–75

    Google Scholar 

  • Nevitt GA, Bonadonna F (2005) Sensitivity to dimethyl sulphide suggests a mechanism for olfactory navigation by seabirds. Biol Let 1:303–305

    Google Scholar 

  • Nevitt GA, Veit RR, Kareiva P (1995) Dimethyl sulfide as a foraging cue for Antarctic Procellariiform seabirds. Nature 376:680–682

    Google Scholar 

  • Nicholls AG (1935) The larval stages of Longipedia coronata Claus, L. scotti G. O. Sars, and L. minor T. and A. Scott, with a description of the male of L. scotti. J Mar Biol Ass UK 20:29–45

    Google Scholar 

  • Nichols PD, Skerratt 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. Phytochemistry 30:3209–3214

    Google Scholar 

  • Nielsen TG, Kiørboe T, Bjørnsen PK (1990) Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community. Mar Ecol Prog Ser 62:1–2

    Google Scholar 

  • 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 43:287–296

    Google Scholar 

  • Peperzak L (2002) The wax and wane of Phaeocystis globosa blooms. Wiskunde en Natuurwetenschappen. Rijksuniversitet Groningen, Groningen, p 254

    Google Scholar 

  • Peperzak L, Colijn F, Vrieling EG, Gieskes WWC, Peeters JCH (2000) Observations of flagellates in colonies of Phaeocystis globosa (Prymnesiophyceae); a hypothesis for their position in the life cycle. J Plankton Res 22:2181–2203

    Google Scholar 

  • Peperzak LM, 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

    Google Scholar 

  • Petri G, Donat FH, Vareschi E (1999) Investigations on uptake and utilization of Phaeocystis globosa colonies by the blue mussel Mytilus edulis. Senckenb Marit 29:117–118

    Article  Google Scholar 

  • Petri G, Vareschi E (1997) Utilization of Phaeocystis globosa colonies by young Mytilus edulis. Arch Fish Mar Res 45:77–91

    Google Scholar 

  • Pieters H, Kluytmans JH, Zandee DI, Cadée GC (1980) Tissue composition and reproduction of Mytilus edulis in relation to food availability. Neth J Sea Res 14:349–361

    Google Scholar 

  • Ploug H, Stolte W, Jørgensen BB (1999) Diffusive boundary layers of the colony-forming plankton alga Phaeocystis sp—implications for nutrient uptake and cellular growth. Limnol Oceanogr 44:1959–1967

    Article  Google Scholar 

  • Pohnert G (2004) Chemical defense strategies of marine organisms. In: Schulz SE (ed) Topics in current chemistry. Springer-Verlag GmBH, Berlin, pp 179–219

    Google Scholar 

  • Pohnert G (2005) Diatom/copepod interactions in plankton: the indirect chemical defense of unicellular algae. ChemBioChem 6:946–959

    Google Scholar 

  • Porter KG (1976) Enhancement of algal growth and productivity by grazing zooplankton. Science 192:1332–1334

    Google Scholar 

  • Reigstad M and Wassmann P (this volume) Does Phaeocystis spp. contribute significantly to vertical export of biogenic matter? Biogeochemistry

  • Richardson MG, Whitaker TM (1979) An Antarctic fast-ice food chain: observations on the interaction of the amphipod Pontogeneia antarctica Chevreux with ice-associated micro-algae. Br Antarct Surv Bull 47:107–115

    Google Scholar 

  • Riebesell U, Reigstad M, Wassmann P, Noji T, Passow U (1995) On the trophic fate of Phaeocystis pouchetii (Hariot): 6. Significance of Phaeocystis-derived mucus for vertical flux. Neth. J Sea Res 33:193–203

    Google Scholar 

  • Rogers SI, Lockwood SJ (1990) Observations on coastal fish fauna during a spring bloom of Phaeocystis pouchetii in the eastern Irish Sea. J Mar Biol Ass UK 70:249–253

    Article  Google Scholar 

  • Rousseau V, Becquevort S, Parent J-Y, Gasparini S, Daro M-H, Tackx M, Lancelot C (2000) Trophic efficiency of the planktonic food web in a coastal ecosystem dominated by Phaeocystis colonies. J Sea Res 43:357–372

    Google Scholar 

  • Rousseau V, Chrétiennot-Dinet M-J, Jacobsen A, Verity PG, Whipple SJ (this volume) The life cycle of Phaeocystis: state of knowledge and presumptive role in ecology. Biogeochemistry. doi:10.1007/s10533-007-9085-3

  • Rousseau V, Leynaert A, Daoud N, Lancelot C (2002) Diatom succession, silicification and silicic acid availability in Belgian coastal waters (Southern North Sea). Mar Ecol Prog Ser 236:61–73

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • Rynearson TA, Armbrust EV (2005) Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii. Mol Ecol 14:1631–1640

    Google Scholar 

  • Sargent JR, Eilertsen HC, Falk-Petersen S, Taasen JP (1985) Carbon assimilation and lipid production in phytoplankton in northern Norwegian fjords. Mar Biol 85:109–116

    Google Scholar 

  • Savage RE (1930) The influence of Phaeocystis on the migrations of the herring. Fish Invest II 12:1–14

    Google Scholar 

  • Savage RE (1932) Phaeocystis and herring shoals. J Ecol 20:326–340

    Google Scholar 

  • Sazhin AF, Artigas LF, Nejstgaard JC, Frischer ME (this volume) The colonization of two Phaeocystis species (Prymnesiophyceae) by pennate diatoms and other protists: a significant contribution to colony biomass. Biogeochemistry

  • Schnack SB (1983) On the feeding of copepods on Thalassiosira partheneia from the Northwest African upwelling area. Mar Ecol Prog Ser 11:49–53

    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 53:43

    Google Scholar 

  • See JH, Campbell L, Richardson TL, Pinckney JL, Shen R, Guinasso NL (2005) Combining new technologies for determination of phytoplankton community structure in the northern Gulf of Mexico. J Phycol 41:305–310

    Google Scholar 

  • Selph KE, Landry MR, Allen CB, et al (2001) Microbial community composition and growth dynamics in the Antarctic Polar Front and seasonal ice zone during late spring 1997. Deep Sea Res Part II Top Stud Oceanogr 48:4059–4080

    Google Scholar 

  • Seuront L, Lacheze C, Doubell MJ, Seymour JR, Mitchell JG (this volume) The influence of Phaeocystis globosa bloom dynamics on microscale spatial patterns of phytoplankton biomass and bulk-phase seawater viscosity. Biogeochemistry

  • Sheppard SK, Harwood JD (2005) Advances in molecular predator–prey ecology. Funct Ecol 19:751–762

    Google Scholar 

  • Shields AR, Smith WOJ (2005) A novel technique to examine the role of colonial Phaeocystis antarctica in the microbial loop of the Ross Sea, Antarctica. SCOR working group #120. Final meeting: Phaeocystis, major link in the biogeochemical cycling of climate-relevant elements. University of Groningen, Haren, the Netherlands, p 14

  • Sieburth JM (1960) Acrylic acid, an “antibiotic” principle in Phaeocystis blooms in antarctic waters. Science 132:676–677

    Google Scholar 

  • Sieburth JM (1961) Antibiotic properties of acrylic acid, a factor in the gastrointestinal antibiosis of polar marine animals. J Bacteriol 82:72–79

    Google Scholar 

  • Smaal AC, Twisk F (1997) Filtration and absorption of Phaeocystis cf. globosa by the mussel Mytilus edulis L. J Exp Mar Biol Ecol 209:33–46

    Google Scholar 

  • Smayda TJ (1973) The growth of Skeletonema costatum during a winter-spring bloom in Narragansett Bay, Rhode Island. Norw J Bot 20:219–247

    Google Scholar 

  • Smayda TJ (1997) What is a bloom? A commentary. Limnol Oceanogr 42:1132–1136

    Article  Google Scholar 

  • Sournia A (1988) Phaeocystis (Prymnesiophyceae): how many species? Nova Hedwigia 47:211–217

    Google Scholar 

  • Stabell OB, Aanesen RT, Eilertsen HC (1999) Toxic peculiarities of the marine alga Phaeocystis pouchetii detected by in vivo and in vitro bioassay methods. Aquat Toxicol 44:279–288

    Google Scholar 

  • Stefels J (2000) Physiological aspects of the production and conversion of DMSP in marine algae and higher plants. J Sea Res 43:183–197

    Google Scholar 

  • Stefels J, Steinke M, Turner S, Gill M and Belviso S (this volume) Environmental constraints on the production of the climatically active gas dimethylsulphide (DMS) and implications for ecosystem modelling. Biogeochemistry. doi:10.1007/s10533-007-9091-5

  • Steinke M, Malin G, Liss PS (2002) Trophic interactions in the sea: an ecological role for climate relevant volatiles? J Phycol 38:630–638

    Google Scholar 

  • Steinke M, Stefels J, Stamhuis E (2006) Dimethyl sulfide triggers search behavior in copepods. Limnol Oceanogr 51:1925–1930

    Article  Google Scholar 

  • 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

    Google Scholar 

  • Strom S, Wolfe G, Slajer A, Lambert S, Clough J (2003) Chemical defense in the microplankton II: Inhibition of protist feeding by ß-dimethylsulfoniopropionate (DMSP). Limnol Oceanogr 48:230–237

    Article  Google Scholar 

  • Strom SL, Loukos H (1998) Selective feeding by protozoa: model and experimental behaviors and their consequences for population stability. J Plankton Res 20:831–846

    Google Scholar 

  • Symondson WOC (2002) Molecular identification of prey in predator diets. Mol Ecol 11:627–641

    Google Scholar 

  • Tande KS, Båmstedt U (1987) On the trophic fate of Phaeocystis pouchetii 1. Copepod feeding rates on solitary cells and colonies of P. pouchetii. Sarsia 72:3–4

    Google Scholar 

  • Tang KW (2003) Grazing and colony size development in Phaeocystis globosa (Prymnesiophyceae): the role of a chemical signal. J Plankton Res 25:831–842

    Google Scholar 

  • Tang KW, Jakobsen HH, Visser AW (2001) Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: feeding, growth, and trophic interactions among grazers. Limnol Oceanogr 46:1860–1870

    Article  Google Scholar 

  • Tang KW, Simó R (2003) Trophic uptake and transfer of DMSP in simple planktonic food chains. Aquat Microb Ecol 31:193–202

    Google Scholar 

  • Thingstad F, Billen G (1994) Microbial degradation of Phaeocystis material in the water column. J Mar Syst 5:55

    Google Scholar 

  • Troedsson CG, Frischer ME, Nejstgaard JC, Thompson EM (2007) Molecular quantification of differential ingestion and particle trapping rates by the appendicularian Oikopleura dioica as a function of prey size and shape. Limnnol Oceanogr 52:416–427

    Article  Google Scholar 

  • Tungaraza C, Rousseau V, Brion N, Lancelot C, Gichuki J, Baeyens W, Goeyens L (2003) Contrasting nitrogen uptake by diatom and Phaeocystis-dominated phytoplankton assemblages in the North Sea. J Exp Mar Biol Ecol 292:19–41

    Google Scholar 

  • Turner JT (1994) Planktonic Copepods of Boston Harbor, Massachusetts Bay and Cape Cod Bay, 1992. Hydrobiologia 293:405–413

    Google Scholar 

  • Turner JT, Ianora A, Esposito F, Carotenuto Y, Miralto A (2002) Zooplankton feeding ecology: does a diet of Phaeocystis support good copepod grazing, survival, egg production and egg hatching success? J Plankton Res 24:1185–1195

    Google Scholar 

  • van Boekel WHM, Hansen FC, Riegman R, Bak RPM (1992) Lysis-induced decline of a Phaeocystis spring bloom and coupling with the microbial foodweb. Mar Ecol Prog Ser 81:269–276

    Google Scholar 

  • van Donk E, Luerling M, Hessen DO, Lokhorst GM (1997) Altered cell wall morphology in nutrient-deficient phytoplankton and its impact on grazers. Limnol Oceanogr 42:357–364

    Article  Google Scholar 

  • van Rijssel M, Alderkamp A-C, Nejstgaard JC, Sazhin AF, Verity PG (this volume) Haemolytic activity of living Phaeocystis pouchetii during mesocosm blooms. Biogeochemistry. doi:10.1007/s10533-007-9095-1

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

    Google Scholar 

  • Veldhuis MJW, Colijn F, Venekamp LAH (1986) The spring bloom of Phaeocystis pouchetii (Haptophyceae) in Dutch coastal waters. Neth J Sea Res 20:37–48

    Google Scholar 

  • Veldhuis MJW, Wassmann P (2005) Bloom dynamics and biological control of a high biomass HAB species in European coastal waters: a Phaeocystis case study. Harm Algae 4:805

    Google Scholar 

  • Verity PG (1988) Chemosensory behavior in marine planktonic ciliates. Bull Marine Sci 43:772–782

    Google Scholar 

  • Verity PG (2000) Grazing experiments and model simulations of the role of zooplankton in Phaeocystis food webs. J Sea Res 43:317–343

    Google Scholar 

  • Verity PG, Paffenhöfer G-A (1996) On assessment of prey ingestion by copepods. J Plankton Res 18:1767–1779

    Google Scholar 

  • Verity PG, Smayda TJ (1989) Nutritional value of Phaeocystis pouchetii (Prymnesiophyceae) and other phytoplankton for Acartia spp. (Copepoda): Ingestion, egg production, and growth of nauplii. Mar Biol 100:161–171

    Google Scholar 

  • Vestheim H, Edvardsen B, Kaartvedt S (2005) Assessing feeding of a carnivorous copepod using species specific PCR. Mar Biol 147:381–385

    Google Scholar 

  • Weisse T, Grimm N, Hickel W, Martens P (1986) Dynamics of Phaeocystis pouchetii blooms in the Wadden Sea of Sylt (German Bight, North Sea). Est Coast Shelf Sci 23:171

    Google Scholar 

  • Weisse T, Scheffel-Möser U (1990) Growth and grazing loss rates in single-celled Phaeocystis sp. (Prymnesiophyceae). Mar Biol 106:153–158

    Google Scholar 

  • Weisse T, Tande K, Verity P, Hansen F, Gieskes W (1994) The trophic significance of Phaeocystis blooms. J Mar Syst 5:67–79

    Google Scholar 

  • 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 Part I Oceanogr Res Pap 47:2243–2264

    Google Scholar 

  • Wolfe GV, Steinke M (1996) Grazing-activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi. Limnol Oceanogr 41:1151–1160

    Article  Google Scholar 

  • Wolfe GV, Steinke M, Kirst GO (1997) Grazing-activated chemical defence in a unicellular marine alga. Nature 387:894–897

    Google Scholar 

  • Wulff A (1934) Über Hydrographie und Oberflächenplankton nebst Verbreitung von Phaeocystis in der Deutschen Bucht im Mai 1933. Ber Deutsch Wiss Komm Meeresforsch NF 7:343–350

    Google Scholar 

  • Yoshida T, Hairston NG, Ellner SP (2004) Evolutionary trade-off between defence against grazing and competitive ability in a simple unicellular alga, Chlorelia vulgaris. Proc Roy Soc Lond Ser B Biol Sci 271:1947–1953

    Google Scholar 

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Acknowledgements

We thank S. Gasparini for his valuable suggestions concerning MCA and HCA analyses. This work was supported by the Norwegian Research Council project 152714/120 30 to JCN, the US-NSF OPP award ANT-0440478 to KWT, the UK Natural Environment Research Council grants NER/I/S/2000/00897 and NE/B500282/1 to MS, the German Federal Ministry for Education and Research grants within the GLOBEC Germany project 03F0418C to JD, the Carlsberg Foundation to MK, the Belgian Research Program for sustainable management of the North Sea within the AMORE project MN/DD/20/21/22 to EA, and the EPA Star Fellowship U-91599501-0 and a National Parks Ecological Research Fellowship to JDL.

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Authors and Affiliations

  1. UNIFOB AS, Department of Biology, University of Bergen, Bergen High Technology Centre, 5020, Bergen, Norway

    Jens C. Nejstgaard

  2. Virginia Institute of Marine Science, 1208 Greate Road, Gloucester Point, VA, 23062, USA

    Kam W. Tang

  3. Department of Biological Sciences, University of Essex, Wivenhoe Park, Colchester, CO4 3SQ, UK

    Michael Steinke

  4. Institute for Baltic Sea Research, Seestraße 15, 18119, Rostock Warnemunde, Germany

    Jörg Dutz

  5. Danish Institute for Fisheries Research, Kavalergården 6, 2920, Charlottenlund, Denmark

    Marja Koski

  6. Laboratoire d’Océanographie de Villefranche, Université Pierre et Marie Curie-Paris6, 06230, Villefranche-sur-Mer, France

    Elvire Antajan

  7. Laboratoire d’Océanographie de Villefranche, CNRS, 06230, Villefranche-sur-Mer, France

    Elvire Antajan

  8. Northeastern University Marine Science Center, 430 Nahant Road, Nahant, MA, 01908, USA

    Jeremy D. Long

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Nejstgaard, J.C., Tang, K.W., Steinke, M. et al. Zooplankton grazing on Phaeocystis: a quantitative review and future challenges. Biogeochemistry 83, 147–172 (2007). https://doi.org/10.1007/s10533-007-9098-y

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