Interactions between Planktonic Microalgae and Protozoan Grazers1

Abstract For an algal bloom to develop, the growth rate of the bloom-forming species must exceed the sum of all loss processes. Among these loss processes, grazing is generally believed to be one of the more important factors. Based on numerous field studies, it is now recognized that microzooplankton are dominant consumers of phytoplankton in both open ocean and coastal waters. Heterotrophic protists, a major component of microzooplankton communities, constitute a vast complex of diverse feeding strategies and behavior which allow them access to even the larger phytoplankton species. A number of laboratory studies have shown the capability of different protistan species to feed and grow on bloom-forming algal species. Because of short generation times, their ability for fast reaction to short-term variation in food conditions enables phagotrophic protists to fulfill the function of a heterotrophic buffer, which might balance the flow of matter in case of phytoplankton blooms. The importance of grazing as a control of microalgae becomes most apparent by its failure; if community grazing controls initial stages of bloom development, there simply is no bloom. However, if a certain algal species is difficult to graze, e.g. due to specific defense mechanisms, reduced grazing pressure will certainly favor bloom development. The present contribution will provide a general overview on the interactions between planktonic microalgae and protozoan grazers with special emphasis on species-specific interactions and algal defense strategies against protozoan grazers.

[1]  A. Cembella,et al.  THE MARINE DINOFLAGELLATE ALEXANDRIUM OSTENFELDII: PARALYTIC SHELLFISH TOXIN CONCENTRATION, COMPOSITION, AND TOXICITY TO A TINTINNID CILIATE 1 , 1992 .

[2]  E. Lessard The trophic role of heterotrophic dinoflagellates in diverse marine environments , 1991 .

[3]  H. Jeong The Ecological Roles of Heterotrophic Dinoflagellates in Marine Planktonic Community 1 , 1999 .

[4]  A. Prakash Source of Paralytic Shellfish Toxin in the Bay of Fundy , 1963 .

[5]  H. Jeong,et al.  NaOCl produced by electrolysis of natural seawater as a potential method to control marine red-tide dinoflagellates , 2002 .

[6]  P. J. Hansen Dinophysis - a planktonic dinoflagellate genus which can act both as a prey and a predator of a ciliate , 1991 .

[7]  D. Anderson,et al.  Growth and grazing rates of Protoperidinium hirobis Abè, a thecate heterotrophic dinoflagellate , 1993 .

[8]  J. R. Beers,et al.  Micro-zooplankters in the plankton communities of the upper waters of the eastern tropical Pacific , 1971 .

[9]  T. Nielsen,et al.  Decimeter scale heterogeneity in the plankton during a pycnocline bloom of Gyrodinium aureolum , 1991 .

[10]  H. Jakobsen,et al.  Prey size selection, grazing and growth response of the small heterotrophic dinoflagellate Gymnodinium sp. and the ciliate Balanion comatum--a comparative study , 1997 .

[11]  Victor Smetacek,et al.  Pelagic ecosystem structure: Heterotrophic compartments of the plankton and their relationship to plankton size fractions 1 , 1978 .

[12]  A. Bursa The Annual Oceanographic Cycle at Igloolik in the Canadian Arctic: II. The Phytoplankton , 1961 .

[13]  W. Carmichael The toxins of cyanobacteria. , 1994, Scientific American.

[14]  A. Kaplan,et al.  Dinoflagellate-Cyanobacterium Communication May Determine the Composition of Phytoplankton Assemblage in a Mesotrophic Lake , 2002, Current Biology.

[15]  H. Spero,et al.  PHAGOTROPHIC FEEDING AND ITS IMPORTANCE TO THE LIFE CYCLE OF THE HOLOZOIC DINOFLAGELLATE, GYMNODINIUM FUNGIFORME 1 , 1981 .

[16]  G. Pohnert,et al.  Are volatile unsaturated aldehydes from diatoms the main line of chemical defence against copepods , 2002 .

[17]  D. Stoecker,et al.  Grazing on Pfiesteria piscicida by microzooplankton , 2000 .

[18]  G. Wolfe,et al.  Chemical defense in the microplankton I: Feeding and growth rates of heterotrophic protists on the DMS‐producing phytoplankter Emiliania huxleyi , 2003 .

[19]  A. Taniguchi,et al.  Feeding activity of a tintinnid ciliate Favella taraikaensis and its variability observed in laboratory cultures , 1985 .

[20]  H. Jeong,et al.  Growth and Grazing Rates of the Heterotrophic Dinoflagellate Polykrikos kofoidii on Red-Tide and Toxic Dinoflagellates , 2001, The Journal of eukaryotic microbiology.

[21]  Y. Nakamura,et al.  Population dynamics of heterotrophic dinoflagellates during a Gymnodinium mikimotoi red tide in the Seto Inland Sea , 1995 .

[22]  D. Caron,et al.  Trophic Interactions Between Nano- and Microzooplankton and the “Brown Tide” , 1989 .

[23]  D. Montagnes,et al.  A Description of Occurrence and Morphology of a New Species of Red‐Water Forming Strombidium (Spirotrichea, Oligotrichia) , 1998 .

[24]  P. Verity Grazing, respiration, excretion, and growth rates of tintinnids1 , 1985 .

[25]  V. Smetácek The annual cycle of protozooplankton in the Kiel Bight , 1981 .

[26]  U. Tillmann,et al.  Toxic effects of Alexandrium spp. on heterotrophic dinoflagellates: an allelochemical defence mechanism independent of PSP-toxin content , 2002 .

[27]  P. Verity,et al.  Feeding by larval and post-larval ctenophores on microzooplankton , 1987 .

[28]  Coats Dw,et al.  Ingestion of fluorescently labeled and phycoerythrin-containing prey by mixotrophic dinoflagellates , 1996 .

[29]  P. J. Hansen Prey size selection, feeding rates and growth dynamics of heterotrophic dinoflagellates with special emphasis on Gyrodinium spirale , 1992 .

[30]  D. Anderson,et al.  WIDESPREAD PHAGOCYTOSIS OF CILIATES AND OTHER PROTISTS BY MARINE MIXOTROPHIC AND HETEROTROPHIC THECATE DINOFLAGELLATES 1 , 1996 .

[31]  G. Wolfe,et al.  Chemical defense in the microplankton II: Inhibition of protist feeding by β‐dimethylsulfoniopropionate (DMSP) , 2003 .

[32]  Hyun-Jin Cho,et al.  Observations of the feeding behavior and growth rates of the heterotrophic dinoflagellate Polykrikos kofoidii (Polykrikaceae, Dinophyceae) , 2000 .

[33]  A. Skovgaard Engulfment of ceratium spp. (dinophyceae) by the thecate photosynthetic dinoflagellate fragilidium subglobosum , 1996 .

[34]  L. Naustvoll Growth and grazing by the thecate heterotrophic dinoflagellate Diplopsalis lenticula (Diplopsalidaceae, Dinophyceae) , 1998 .

[35]  K. Fukami,et al.  Predation on naked protozoan microzooplankton by fish larvae , 1999 .

[36]  D. Anderson,et al.  Removal of red- and brown-tide cells using clay flocculation. I. Laboratory culture experiments with Gymnodinium breve and Aureococcus anophagefferens , 2001 .

[37]  P. Verity,et al.  The relative food value of diatoms, dinoflagellates, flagellates, and cyanobacteria for tintinnid ciliates , 1986 .

[38]  Y. Nakamura,et al.  Development and collapse of a Gymnodinium mikimotoi red tide in the Seto Inland Sea , 1996 .

[39]  D. A. Egloff Effects of Olisthodiscus luteus on the feeding and reproduction of the marine rotifer Synchaeta cecilia , 1986 .

[40]  G. Gorsky,et al.  Annual microplankton cycles in Villefranche Bay, Ligurian Sea, NW Mediterranean , 2003 .

[41]  P. Jonsson Particle size selection, feeding rates and growth dynamics of marine planktonic oligotrichous ciliates (Ciliophora: Oligotrichina) , 1986 .

[42]  D. W. Coats Parasitic Life Styles of Marine Dinoflagellates 1 , 1999 .

[43]  E. Grainger The Annual Oceanographic Cycle at Igloolik in the Canadian Arctic. 1. The Zooplankton and Physical and Chemical Observations , 1959 .

[44]  A. Cembella,et al.  Toxicity of cultured isolates and natural populations of Protogonyaulax tamarensis from the St. Lawrence Estuary , 1988 .

[45]  M. Levandowsky,et al.  Chemosensory responses of swimming algae and protozoa. , 1978, International review of cytology.

[46]  H. Jeong,et al.  Reduction in the toxicity of the dinoflagellate Gymnodinium catenatum when fed on by the heterotrophic dinoflagellate Polykrikos kofoidii , 2003 .

[47]  U. Tillmann,et al.  Dinoflagellate grazing on the raphidophyte Fibrocapsa japonica , 2002 .

[48]  Yuichi Kotani,et al.  Grazing impacts of the heterotrophic dinoflagellate Polykrikos kofoidii on a bloom of Gymnodinium catenatum , 1999 .

[49]  J. Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum , 2006 .

[50]  K. Šimek,et al.  Processing of ingested matter in Strombidium sulcatum, a marine ciliate (Oligotrichida) , 1997 .

[51]  R. P. Hassett,et al.  Estimating the grazing impact of marine micro-zooplankton , 1982 .

[52]  S. Strom Growth and grazing rates of the herbivorous dinoflagellate Gymnodinium sp. from the open subarctic Pacific Ocean , 1991 .

[53]  F. C. Hansen Trophic interactions between zooplankton andPhaeocystis cf.globosa , 1995, Helgoländer Meeresuntersuchungen.

[54]  J. Titelman,et al.  Feeding, prey selection and prey encounter mechanisms in the heterotrophic dinoflagellate Noctiluca scintillans , 1998 .

[55]  K. Tarutani,et al.  Viral Impacts on Total Abundance and Clonal Composition of the Harmful Bloom-Forming PhytoplanktonHeterosigma akashiwo , 2000, Applied and Environmental Microbiology.

[56]  R. Guillard,et al.  SELECTIVE PREDATION BY FAVELLA EHRENBERGII (TINTINNIA) ON AND AMONG DINOFLAGELLATES , 1981 .

[57]  S. Agatha,et al.  Morphology, infraciliature, and ecology of some strobilidiine ciliates (ciliophora, oligotrichea) from coastal brackish water basins of Germany , 1998 .

[58]  D. Anderson,et al.  Selective retention of two dinoflagellates in a well-mixed estuarine embayment: the importance of diel vertical migration and surface avoidance , 1985 .

[59]  H. Jeong,et al.  Feeding by the Heterotrophic Dinoflagellate Oxyrrhis marina on the Red-Tide Raphidophyte Heterosigma akashiwo: a Potential Biological Method to Control Red Tides Using Mass-Cultured Grazers , 2003, The Journal of eukaryotic microbiology.

[60]  Uchida,et al.  The red-tide dinoflagellate Heterocapsa sp. kills Gyrodinium instriatum by cell contact , 1995 .

[61]  B. Reguera,et al.  Zooplankton as a potential vector of diarrhetic shellfish poisoning toxins through the food web , 2000 .

[62]  F. Rassoulzadegan,et al.  Bacteria or microflagellates as a major food source for marine ciliates: possible implications for the microzooplankton , 1990 .

[63]  A. Skovgaard,et al.  Physiology of the mixotrophic dinoflagellate Fragilidium subglobosum. I. Effects of phagotrophy and irradiance on photosynthesis and carbon content , 2000 .

[64]  E. Sherr,et al.  Trophic Behaviour and Related Community Feeding Activities of Heterotrophic Marine Protists , 1991 .

[65]  T. Weisse,et al.  Growth and grazing loss rates in single-celledPhaeocystis sp. (Prymnesiophyceae) , 1990 .

[66]  J. Patočka,et al.  The toxins of Cyanobacteria. , 2001, Acta medica.

[67]  H. Jakobsen Escape response of planktonic protists to fluid mechanical signals , 2001 .

[68]  H. Jeong,et al.  Growth and Grazing Rates of the Marine Planktonic Ciliate Strombidinopsis sp. on Red‐Tide and Toxic Dinoflagellates , 1999 .

[69]  P. M. Williams,et al.  RED WATER IN LA JOLLA BAY, 1964–19661 , 1967 .

[70]  P. Verity Feeding In Planktonic Protozoans: Evidence For Non‐Random Acquisition of Prey , 1991 .

[71]  W. K. Breteler Continuous Breeding of Marine Pelagic Copepods in the Presence of Heterotrophic Dinoflagellates , 1980 .

[72]  C. Turley Protozoa and Their Role in Marine Processes , 1991, NATO ASI Series.

[73]  M. Paranjape Occurrence and significance of resting cysts in a hyaline tintinnid, Helicostomella subulata (Ehre.) Jorgensen , 1980 .

[74]  T. Smayda,et al.  Harmful algal blooms: Their ecophysiology and general relevance to phytoplankton blooms in the sea , 1997 .

[75]  M. Paranjape Occurrence and significance of resting cysts in a hyaline tintinnid, Helicostomella subulata (Ehre.) , 1980 .

[76]  K. Banse Grazing, Temporal Changes of Phytoplankton Concentrations, and the Microbial Loop in the Open Sea , 1992 .

[77]  P. Rublee,et al.  Use of fluorescently labelled algae (FLA) to estimate microzooplankton grazing , 1989 .

[78]  Y. Takeda,et al.  Feeding rate and behavior of the tintinnid ciliate Favella taraikaensis observed with a high speed VTR system , 1988 .

[79]  T. Dale,et al.  Mass occurrence of planktonic oligotrichous ciliates in a bay in southern Norway , 1987 .

[80]  E. Sherr,et al.  Bacterivory and herbivory: Key roles of phagotrophic protists in pelagic food webs , 1994, Microbial Ecology.

[81]  Stefan Schouten,et al.  Trophic upgrading of food quality by protozoans enhancing copepod growth: role of essential lipids , 1999 .

[82]  T. Nielsen,et al.  The trophic role of marine pelagic ciliates and heterotrophic dinoflagellates in arctic and temperate coastal ecosystems: A cross‐latitude comparison , 2002 .

[83]  Y. Nakamura,et al.  Growth and grazing of a naked heterotrophic dinoflagellate, Gyrodinium dominans , 1995 .

[84]  T. Honjo,et al.  Photosensitizing hemolytic toxin in Heterocapsa circularisquama, a newly identified harmful red tide dinoflagellate. , 2002, Aquatic toxicology.

[85]  A. B. Needler Paralytic Shellfish Poisoning and Goniaulax tamarensis. , 1949 .

[86]  Efstathios E Michaelides,et al.  Effects of turbulence , 2006 .

[87]  E. J. Adam,et al.  A new method using fluorescent microspheres to determine grazing on ciliates by the mixotrophic dinoflagellate Ceratium furca , 1999 .

[88]  D. W. Coats,et al.  Spatial and Temporal Aspects of Mixotrophy In Chesapeake Bay Dinoflagellates , 1993 .

[89]  D. Anderson,et al.  THECATE HETEROPHIC DINOFLAGELLATES: FEEDING BEHAVIOR AND MECHANISMS 1 , 1986 .

[90]  D. Stoecker,et al.  Respiration, photosynthesis and carbon metabolism in planktonic ciliates , 1991 .

[91]  M. Latz,et al.  Growth and grazing rates of the heterotrophic dinoflagellates Protoperidinium spp , 1994 .

[92]  D. Kulis,et al.  Toxin production of Alexandrium minutum (Dinophyceae) from the Bay of Plenty, New Zealand. , 1997, Toxicon : official journal of the International Society on Toxinology.

[93]  T. Harumoto,et al.  Defensive function of trichocysts in Paramecium against the predatory ciliate Monodinium balbiani , 1996 .

[94]  R. Negri,et al.  Toxic red-tide in the Argentine Sea. Phytoplankton distribution and survival of the toxic dinoflagellate Gonyaulax excavata in a frontal area , 1986 .

[95]  D. Montagnes,et al.  Growth rate of the marine planktonic ciliate Strombidinopsis cheshiri Snyder and Ohman as a function of food concentration and interclonal variability , 1996 .

[96]  W. Admiraal,et al.  Significance of tintinnid grazing during blooms of Phaeocystis pouchetii (haptophyceae) in Dutch coastal waters , 1986 .

[97]  A. Skovgaard,et al.  Food uptake in the harmful alga Prymnesium parvum mediated by excreted toxins , 2003 .

[98]  A. Uchida,et al.  Population structure of algicidal marine bacteria targeting the red tide forming alga Heterosigma akashiwo (Raphidophyceae), determined by restriction fragment length polymorphism analysis of the bacterial 16S ribosomal RNA genes , 1998 .

[99]  P. Verity Measurement and simulation of prey-uptake by marine planktonic ciliates fed plastidic and aplastidic nanoplankton , 1991 .

[100]  I. Jenkinson,et al.  Notes on Alexandrium population dynamics , 1997 .

[101]  V. Smetácek,et al.  Organism life cycles, predation, and the structure of marine pelagic ecosystems , 1996 .

[102]  Hyun-Jin Cho,et al.  Cell lysis of a phagotrophic dinoflagellate, Polykrikos kofoidii feeding on Alexandrium tamarense , 2000 .

[103]  S. Strom,et al.  Phytoplankton blooms are strongly impacted by microzooplankton grazing in coastal North Pacific waters , 2001 .

[104]  Paul G. Falkowski,et al.  Primary Productivity and Biogeochemical Cycles in the Sea , 1992 .

[105]  A. White High toxin content in the dinoflagellate Gonyaulax excavata in nature. , 1986, Toxicon : official journal of the International Society on Toxinology.

[106]  C. Gallegos,et al.  Parasitism of photosynthetic dinoflagellates in a shallow subestuary of Chesapeake Bay, USA , 1996 .

[107]  A. Cembella,et al.  Toxin accumulation and feeding behaviour of the planktonic copepod Calanus finmarchicus exposed to the red-tide dinoflagellate Alexandrium excavatum , 1995 .

[108]  David J. S. Montagnes,et al.  Population dynamics of the marine planktonic ciliate Strombidinopsis multiauris: its potential to control phytoplankton blooms , 1999 .

[109]  Katherine Richardson,et al.  Harmful or exceptional phytoplankton blooms in the marine ecosystem , 1997 .

[110]  P. Jonsson,et al.  Trophic interaction between copepods and ciliates: effects of prey swimming behavior on predation risk , 2001 .

[111]  D. Montagnes Growth responses of planktonic ciliates in the genera Strobilidium and Strombidium , 1996 .

[112]  P. Verity Chemosensory behavior in marine planktonic ciliates , 1988 .

[113]  M. Moran,et al.  Processing of ingested matter in Strombidium sulcatum, a marine ciliate (Oligotrichida) , 1999 .

[114]  S. Arima,et al.  Lethal effect of the dinoflagellate Heterocapsa circularisquama upon the tintinnid ciliate Favella taraikaensis , 1997 .

[115]  E. Buskey,et al.  Feeding, growth and bioluminescence of the heterotrophic dinoflagellate Protoperidinium huberi , 1994 .

[116]  P. J. Hansen,et al.  Effects of high pH on the growth and survival of six marine heterotrophic protists , 2003 .

[117]  André W. Visser,et al.  Phaeocystis globosa (Prymnesiophyceae) and the planktonic food web: Feeding, growth, and trophic interactions among grazers , 2001 .

[118]  J. Passarge,et al.  Grazing in the heterotrophic dinoflagellate Oxyrrhis marina: size selectivity and preference for calcified Emiliania huxleyi cells , 1996 .

[119]  E. Granéli,et al.  Cell density, chemical composition and toxicity of Chrysochromulina polylepis (Haptophyta) in relation to different N:P supply ratios , 1999 .

[120]  D. Stoecker,et al.  Behavioral responses of the marine tintinnid favella sp to phytoplankton influence of chemical mechanical and photic stimuli , 1989 .

[121]  P. J. Hansen Growth and grazing response of a ciliate feeding on the red tide dinoflagellate Gyrodinium aureolum in monoculture and in mixture with a non-toxic alga , 1995 .

[122]  P. Tester,et al.  Vectorial transport of toxins from the dinoflagellate Gymnodinium breve through copepods to fish , 2000 .

[123]  R. Benner,et al.  Planktonic grazers are a potentially important source of marine dissolved organic carbon , 1997 .

[124]  B. Sweeney,et al.  INFLUENCE OF DINOFLAGELLATE TRICHOCYSTS AND OTHER FACTORS ON THE FEEDING OF CRASSOSTREA VIRGINICA LARVAE ON MONOCHRYSIS LUTHERI1 , 1969 .

[125]  S. Strom,et al.  Nutritional role of protists in the diet of first stage larvae of the Dungeness crab Cancer magister , 1998 .

[126]  T. Kamiyama Growth and grazing responses of tintinnid ciliates feeding on the toxic dinoflagellate Heterocapsacircularisquama , 1997 .

[127]  Jeng Chang,et al.  SHORT COMMUNICATION Influence of light intensity on the ingestion rate of a marine ciliate, Lohmanniella sp. , 1999 .

[128]  D. W. Coats,et al.  Grazing of the mixotrophic dinoflagellate Gymnodinium sanguineum on ciliate populations of Chesapeake Bay , 1993 .

[129]  L. Naustvoll Prey size spectra and food preferences in thecate heterotrophic dinoflagellates , 2000 .

[130]  P. Andersen,et al.  Population dynamics and trophic coupling in pelagic microorganisms in eutrophic coastal waters , 1986 .

[131]  Torkel Gissel Nielsen,et al.  Effects of a Chrysochromulina polylepis subsurface bloom on the planktonic community , 1990 .

[132]  E. Paasche,et al.  Ammonium regeneration by microzooplankton in the Oslofjord , 1982 .

[133]  E. Buskey Behavioral components of feeding selectivity of the heterotrophic dinoflagellate Protoperidinium pellucidum , 1997 .

[134]  C. Legrand,et al.  Allelopathy in phytoplankton - biochemical, ecological and evolutionary aspects , 2003 .

[135]  D. Stoecker,et al.  Predation on Protozoa: its importance to zooplankton , 1990 .

[136]  U. Tillmann,et al.  A comparative approach to study inhibition of grazing and lipid composition of a toxic and non-toxic clone of Chrysochromulina polylepis (Prymnesiophyceae) , 2002 .

[137]  Victor Smetacek,et al.  A watery arms race , 2001, Nature.

[138]  F. Taylor,et al.  A ciliate red tide at Barrow, Alaska , 1970 .

[139]  Y. Nakamura,et al.  Growth and grazing of a heterotrophic dinoflagellate Gyrodinium dommans, feeding on a red tide flagellate, Chattonella antique , 1992 .

[140]  Yasuo Nakamura Growth and grazing of a large heterotrophic dinoflagellate, Noctiluca scintillans, in laboratory cultures , 1998 .

[141]  A. Skovgaard Mixotrophy in Fragilidium subglobosum (Dinophyceae): growth and grazing responses as functions of light intensity , 1996 .

[142]  W. V. Boekel,et al.  Grazing pressure of the calanoid copepod Temora longicornis on a Phaeocystis dominated spring bloom in a Dutch tidal inlet , 1991 .

[143]  J. Heinbokel Studies on the functional role of tintinnids in the Southern California Bight. I. Grazing and growth rates in laboratory cultures , 1978 .

[144]  S. Strom Novel interactions between phytoplankton and microzooplankton: their influence on the coupling between growth and grazing rates in the sea , 2002, Hydrobiologia.

[145]  J. R. Beers,et al.  Studies on the functional role of tintinnids in the Southern California Bight. III. Grazing impact of natural assemblages , 1979 .

[146]  D. Stoecker,et al.  Effects of protozoan herbivory and carnivory in a microplankton food web. , 1985 .

[147]  Jean-Paul Parkhill Effects of salinity, light and inorganic nitrogen on growth and toxigenicity of the marine dinoflagellate Alexandrium tamarense from northeastern Canada , 1999 .

[148]  Matthew D. Johnson,et al.  � 2003, by the American Society of Limnology and Oceanography, Inc. Microzooplankton grazing on Prorocentrum minimum and Karlodinium micrum in , 2022 .

[149]  U. Tillmann,et al.  On the quantitative importance of heterotrophic microplankton in the northern German Wadden Sea , 1998 .

[150]  V. Garçon,et al.  The effect of zooplankton grazing on estuarine blooms of the toxic dinoflagellate Gonyaulax tamarensis , 1985 .

[151]  A. Repak Suitability of Selected Marine Algae for Growing the Marine Heterotrich Ciliate Fabrea salina1 , 1983 .

[152]  E. Buskey,et al.  Feeding, growth, and behavior of the thecate heterotrophic dinoflagellate Oblea rotunda , 1993 .

[153]  D. Stoecker Are Marine Planktonic Ciliates Suspension‐Feeders?1,2 , 1988 .

[154]  S. F. Umani,et al.  The paradox of diatom-copepod interactions* , 1997 .

[155]  G. Wolfe The chemical defense ecology of marine unicellular plankton: constraints, mechanisms, and impacts. , 2000, The Biological bulletin.

[156]  A. Cembella,et al.  Grazing of toxic dinoflagellates, Alexandrium spp., by adult copepods of coastal Maine: Implications for the fate of paralytic shellfish toxins in marine food webs , 1996 .

[157]  H. Jeong,et al.  Interactions among the toxic dinoflagellate Amphidinium carterae, the heterotrophic dinoflagellate Oxyrrhis marina, and the calanoid copepods Acartia spp. , 2001 .

[158]  Per Juel Hansen,et al.  Allelopathy in the prymnesiophyte Chrysochromulina polylepis: effect of cell concentration, growth phase and pH , 2001 .

[159]  B. Leadbeater,et al.  Mixotrophy in marine species of Chrysochromulina (Prymnesiophyceae): ingestion and digestion of a small green flagellate , 1993, Journal of the Marine Biological Association of the United Kingdom.

[160]  U. Tillmann PHAGOTROPHY BY A PLASTIDIC HAPTOPHYTE, PRYMNESIUM PATELLIFERUM , 1998 .

[161]  U. Tillmann Kill and eat your predator: a winning strategy of the planktonic flagellate Prymnesium parvum , 2003 .

[162]  D. Wayne Coats,et al.  Ecology of the Red-Tide Dinoflagellate Ceratium furca: Distribution, Mixotrophy, and Grazing Impact on Ciliate Populations of Chesapeake Bay , 2002, The Journal of eukaryotic microbiology.

[163]  P. J. Hansen Quantitative importance and trophic role of heterotrophic dinoflagellates in a coastal pelagial food web , 1991 .

[164]  M. Steinke,et al.  Grazing‐activated production of dimethyl sulfide (DMS) by two clones of Emiliania huxleyi , 1996 .

[165]  Donald M. Anderson,et al.  Physiological ecology of harmful algal blooms , 1998 .

[166]  M. Elbrächter,et al.  Aspects of Noctiluca (Dinophyceae) population dynamics , 1998 .

[167]  P. Verity,et al.  Effects of Olisthodiscus luteus on the growth and abundance of Tintinnids , 1982 .

[168]  T. Uchida,et al.  Predation by a photosynthetic dinoflagellate Gyrodinium instriatum on loricated ciliates. , 1997 .

[169]  J. Cullen,et al.  Behavior, physiology and the niche of depth-regulating phytoplankton , 1998 .

[170]  M. Cabrini,et al.  The insidious effect of diatoms on copepod reproduction , 1999, Nature.

[171]  P. Burkill,et al.  Microbial dynamics in coastal waters of East Antarctica: Herbivory by heterotrophic dinoflagellates , 1996 .

[172]  K. Nygaard,et al.  Bacterivory in algae: A survival strategy during nutrient limitation , 1993 .

[173]  D. Stoecker,et al.  Differential grazing on protozoan microplankton by developmental stages of the calanoid copepod Eurytemora affinis Poppe , 1998 .

[174]  S. Arima,et al.  Feeding characteristics of two tintinnid ciliate species on phytoplankton including harmful species: effects of prey size on ingestion rates and selectivity. , 2001, Journal of experimental marine biology and ecology.

[175]  D. Stoecker,et al.  Locomotory patterns of the planktonic ciliate Favella sp.: adaptations for remaining within food patches , 1988 .

[176]  S. Strom,et al.  Comparative growth rates and yields of ciliates and heterotrophic dinoflagellates , 1998 .

[177]  D. Gifford Laboratory culture of marine planktonic oligotrichs (Ciliophora, Oligotrichida) , 1985 .

[178]  T. Harumoto The Role of Trichocyst Discharge and Backward Swimming in Escaping Behavior of Paramecium from Dileptus margaritifer 1 , 1994 .

[179]  E. Schnepf,et al.  Nutritional strategies in dinoflagellates: A review with emphasis on cell biological aspects. , 1992, European journal of protistology.

[180]  P. Olsson,et al.  Grazer elimination through poisoning: one of the mechanisms behind Chrysochromulina polylepis blooms? , 1990 .

[181]  M. Abrahams,et al.  Bioluminescence in Dinoflagellates: A Test of the Burgular Alarm Hypothesis , 1993 .

[182]  J. C. Goldman,et al.  Dynamics of herbivorous grazing by the heterotrophic dinoflagellate oxyrrhis marina , 1989 .

[183]  P. J. Hansen,et al.  Phagotrophic Mechanisms and Prey Selection in Free‐living Dinoflagellates 1 , 1999 .

[184]  A. Tobiesen Growth rates of Heterophrys marina (heliozoa) on Chrysochromulina polylepis(prymnesiophyceae) , 1991 .

[185]  J. M. Bralewska Heterotrophic dinoflagellates in the ecosystem of the Gulf of Gdansk , 1995 .

[186]  L. Naustvoll Prey size spectra in naked heterotrophic dinoflagellates , 2000 .

[187]  H. Jeong,et al.  Feeding by the mixotrophic thecate dinoflagellate Fragilidium cf. mexicanum on red-tide and toxic dinoflagellates , 1999 .

[188]  A. Cembella Ecophysiology and Metabolism of Paralytic Shellfish Toxins in Marine Microalgae , 1998 .

[189]  S. Chisholm,et al.  Effect of temperature on growth and ingestion rates of Favella sp. , 1985 .

[190]  M. Steinke,et al.  Grazing-activated chemical defence in a unicellular marine alga , 1997, Nature.

[191]  R. Riegman,et al.  Phaeocystis blooming enhanced by copepod predation on protozoa: evidence from incubation experiments , 1993 .

[192]  A. White Marine zooplankton can accumulate and retain dinoflagellate toxins and cause fish kills , 1981 .

[193]  H. Jakobsen Escape of protists in predator-generated feeding currents , 2002 .

[194]  P. Hansen The red tide dinoflagellate Alexandrmm tamarense: effects on behaviour and growth of a tintinnid ciliate , 1989 .

[195]  G. Pohnert Phospholipase A2 Activity Triggers the Wound-Activated Chemical Defense in the Diatom Thalassiosira rotula , 2002, Plant Physiology.

[196]  H. Jeong,et al.  Growth and grazing rates of the prostomatid ciliate Tiarina fusus on red-tide and toxic algae , 2002 .

[197]  G. Bell,et al.  Sex And Death In Protozoa , 1988 .