Harmful or exceptional phytoplankton blooms in the marine ecosystem

Publisher Summary This chapter discusses the harmful or exceptional phytoplankton blooms in the marine ecosystem. Phytoplankton blooms are natural phenomena that play an important role in relation to carbon and energy flow, as well as geochemical cycling in marine ecosystems. Phytoplankton growth will occur wherever and whenever adequate light and nutrient (both macro- and micronutrient) conditions occur. Blooms (accumulations of phytoplankton biomass) will result when the combined effect of population loss factors (grazing, advection and lysis, or sedimentation) is less than the biomass accumulation due to growth of the phytoplankton and via advective processes. It is estimated that the world's phytoplankton flora consists of approximately 4000 different species. Of these, about 200 species have been identified as “harmful” or “exceptional” phytoplankton blooms. About 2% of the world's phytoplankton flora has been implicated as toxin producers. The toxins produced vary in their chemical structures and their effects but their public health implications are important as some are neurotoxins that can cause death at low concentrations and others are, apparently, carcinogenic. It is clear that harmful phytoplankton blooms occurred in prehistoric times so anthropogenic influence is certainly not a prerequisite for the occurrence of such blooms. Nevertheless, a number of mechanisms by which anthropogenic activities can, theoretically, affect (directly or indirectly) the occurrence of harmful blooms are discussed. These include eutrophication, the use of pesticides which may influence herbivore abundance, and the distribution and transport of harmful species from one geographic region to another via ballast water or in connection with aquaculture activities.

[1]  B. Dale,et al.  Evidence for prehistoric and historic ‘blooms’ of the toxic dinoflagellate Gymnodinium catenatum in the Kattegat-Skagerrak region of Scandinavia , 1993 .

[2]  S. Warren,et al.  Oceanic phytoplankton, atmospheric sulphur, cloud albedo and climate , 1987, Nature.

[3]  P. Holligan,et al.  Vertical distribution of plankton in the skagerrak in relation to doming of the seasonal thermocline , 1982 .

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

[5]  M. D. Keller,et al.  Spring phytoplankton blooms in the absence of vertical water column stratification , 1992, Nature.

[6]  T. Legovic,et al.  Trends in oxygen content 1911–1984 and occurrence of benthic mortality in the northern Adriatic Sea , 1987 .

[7]  J. Ives,et al.  Possible mechanisms underlying copepod grazing responses to levels of toxicity in red tide dinoflagellates , 1987 .

[8]  C. Lundsgaard,et al.  Seasonal sedimentation of autochthonous material from the euphotic zone of a coastal system , 1995 .

[9]  G. Tracey.  Feeding reduction, reproductive failure, and mortality in Mytilus edulis during the 1985 "brown tide" in Narragansett Bay, Rhode Island. , 1988 .

[10]  Karl Tangen,et al.  Blooms of Gyrodinium aureolum (Dinophygeae) in North European waters, accompanied by mortality in marine organisms , 1977 .

[11]  E. Paasche,et al.  The Chrysochromulina polylepis Bloom in Scandinavian Waters During Spring 1988 , 1989 .

[12]  Ulrich Sommer,et al.  Plankton ecology, succession in plankton communities , 1989 .

[13]  A. Cembella,et al.  Occurrence and elimination kinetics of PSP toxins in the American lobster (Homarus americanus) , 1995 .

[14]  S. Shumway.  A Review of the Effects of Algal Blooms on Shellfish and Aquaculture , 1989 .

[15]  P. Boyd,et al.  Production Of Organic And Inorganic Carbon Within A Large-Scale Coccolithophore Bloom In The Northeast Atlantic-Ocean , 1993 .

[16]  M. S. Finch,et al.  The impact of a coccolithophore bloom on oceanic carbon uptake in the northeast Atlantic during summer 1991 , 1994 .

[17]  E. Steemann Nielsen,et al.  The Use of Radio-active Carbon (C14) for Measuring Organic Production in the Sea , 1952 .

[18]  K. Richardson,et al.  Dynamics of a subsurface phytoplankton maximum in the Skagerrak , 1993 .

[19]  R. Nuzzi,et al.  The Spatial and Temporal Distribution of ”Brown Tide“ in Eastern Long Island , 1989 .

[20]  E. Laws,et al.  of a marine diatom: implications to dynamics of chlorophyll maximum layers , 1983 .

[21]  D. H. Cushing,et al.  The seasonal variation in oceanic production as a problem in population dynamics , 1959 .

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

[23]  A. Longhurst.  Seasonal cooling and blooming in tropical oceans , 1993 .

[24]  D. Anderson,et al.  Alongshore transport of a toxic phytoplankton bloom in a buoyancy current: Alexandrium tamarense in the Gulf of Maine , 1992 .

[25]  A. lanora,et al.  Do diatoms arrest embryonic development in cope-pods? , 1994 .

[26]  S. Nixon.  An Extraordinary Red Tide and Fish Kill in Narragansett Bay , 1989 .

[27]  F. H. Chang,et al.  First record of a Heterosigma (Raphidophyceae) bloom with associated mortality of cage-reared salmon in Big Glory Bay, New Zealand , 1990 .

[28]  Robert R. Bidigare,et al.  Seasonal patterns of ocean biogeochemistry at the U.S. JGOFS Bermuda Atlantic time-series study site , 1994 .

[29]  B. Leadbeater,et al.  The Haptophyte algae , 1994 .

[30]  S. Nixon.  Coastal marine eutrophication: A definition, social causes, and future concerns , 1995 .

[31]  F. Rassoulzadegan,et al.  Plankton and nutrient dynamics in marine waters , 1995 .

[32]  B. Dale,et al.  Possible environmental factors regulating prehistoric and historic ‘blooms’ of the toxic dinoflagellate Gymnodinium catenatum in the Kattegat-Skagerrak region of Scandinavia. , 1993 .

[33]  George A. Jackson,et al.  A model of the formation of marine algal flocs by physical coagulation processes , 1990 .

[34]  I. Jenkinson,et al.  Bulk-phase viscoelastic properties of seawater relationship with plankton components , 1995 .

[35]  O. Lindahl.  On the development of a Gyrodinium aureolum occurrence on the Swedish west coast in 1982 , 1983 .

[36]  N. Loneragan,et al.  Blue-green algal blooms and the commercial fishery of a large Australian estuary , 1985 .

[37]  V. Garçon,et al.  Tidal flushing of an estuarine embayment subject to recurrent dinoflagellate blooms , 1986 .

[38]  K. Richardson.  Comparison of 14C primary production determinations made by different laboratories , 1991 .

[39]  V. Smetácek,et al.  Patterns of production and sedimentation in the boreal and polar Northeast Atlantic , 1991 .

[40]  K. Richardson,et al.  Structure of plankton communities in the Dogger Bank area (North Sea) during a stratified situation , 1993 .

[41]  L. Rhodes,et al.  Algal blooms and climate anomalies in north‐east New Zealand, August ‐December 1992 , 1993 .

[42]  N. Ginther,et al.  The effects of Heterosigma akashiwo on juvenile Oncorhynchus tshawytscha and its implications for fish culture. , 1991 .

[43]  E. Granéli,et al.  Environmental-conditions and ecophysiological mechanisms which led to the 1988 chrysochromulina-polylepis bloom - an hypothesis , 1991 .

[44]  M. D. Keller,et al.  Dimethylsulfide in a large-scale coccolithophore bloom in the Gulf of Maine , 1993 .

[45]  Edward J. Noga,et al.  New 'phantom' dinoflagellate is the causative agent of major estuarine fish kills , 1992, Nature.

[46]  J. Le Fèvre,et al.  Aspects of the Biology of Frontal Systems , 1987 .

[47]  E. Donk.  The role of fungal parasites in phytoplankton succession, a review , 1989 .

[48]  J. Burkholder,et al.  Response of two zooptankton grazers to an ichthyotoxic estuarine dinoflagellate , 1995 .

[49]  M. S. Finch,et al.  A biogeochemical study of the coccolithophore, Emiliania huxleyi, in the North Atlantic , 1993 .

[50]  P. Thompson,et al.  Does energy control the sinking rates of marine diatoms , 1992 .

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

[52]  G. Bell.  Penetration of Spines from a Marine Diatom into the Gill Tissue of Lingcod (Ophiodon elongatus) , 1961, Nature.

[53]  P. Abreu,et al.  Structuring of a postspring phytoplankton community by manipulation of trophic interactions , 1992 .

[54]  G. Friederich,et al.  Nutrient cycling and primary production in the marine systems of the Arctic and Antarctic , 1991 .

[55]  Y. Ishida,et al.  Viral mortality in the final stage of Heterosigma akashiwo (Raphidophyceae) red tide , 1994 .

[56]  Colin S. Reynolds,et al.  Phytoplankton periodicity: the interactions of form, function and environmental variability , 1984 .

[57]  B. Dale,et al.  Red Tide and Paralytic Shellfish Poisoning. , 1978 .

[58]  F. Taylor,et al.  Phytoplankton ecology of Sechelt Inlet, a fjord system on the British Columbia coast. II. Potentially harmful species , 1994 .

[59]  Y. Shimizu,et al.  Biosynthesis of brevetoxins and heterotrophic metabolism in Gymnodinium breve , 1995 .

[60]  S. Hsiao.  Spatial and seasonal variations in primary production of sea ice microalgae and phytoplankton in Frobisher Bay, Arctic Canada , 1988 .

[61]  Gustaaf M. Hallegraeff,et al.  Transport of diatom and dinoflagellate resting spores in ships' ballast water: implications for plankton biogeography and aquaculture , 1992 .

[62]  S. Piasecki,et al.  Bivalve mass mortality caused by toxic dinoflagellate blooms in a Berriasian-Valanginian lagoon, Bornholm, Denmark , 1987 .

[63]  J. L. Hansen,et al.  Aggregation and sedimentation processes during a spring phytoplankton bloom: A field experiment to test coagulation theory , 1994 .

[64]  E. Stoermer,et al.  Modification of the biogeochemical cycle of silica with eutrophication , 1993 .

[65]  I. Falconer.  Tumor promotion and liver injury caused by oral consumption of cyanobacteria , 1991 .

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

[67]  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 .

[68]  Mark E. Huntley,et al.  Chemically-mediated rejection of dinoflagellate prey by the copepods Calanus pacificus and Paracalanus parvus: mechanism, occurrence and significance , 1986 .

[69]  Donald M. Anderson,et al.  Toxic Marine Phytoplankton , 1987 .

[70]  L. Fortier,et al.  Vulnerability of marine fish larvae to the toxic dinoflagellate Protogonyaulax tamarensis , 1989 .

[71]  S. Lochmann,et al.  Effect of coagulation on nutrient and light limitation of an algal bloom , 1992 .

[72]  W. Esaias,et al.  Two approaches to determining the sea-to-air flux of dimethyl sulfide : satellite ocean color and a photochemical model with atmospheric measurements , 1990 .

[73]  H. Sverdrup,et al.  On Conditions for the Vernal Blooming of Phytoplankton , 1953 .

[74]  B. Mitchell,et al.  Mass sedimentation of Phaeocystis pouchetii in the Barents Sea , 1990 .

[75]  T. Braarud,et al.  A Quantitative Study of the Phytoplankton in the Bay of Fundy and the Gulf of Maine (including Observations on Hydrography, Chemistry and Turbidity) , 1935 .

[76]  A. White.  Dinoflagellate Toxins as Probable Cause of an Atlantic Herring (Clupea harengus harengus) Kill, and Pteropods as Apparent Vector , 1977 .

[77]  P. Harrison,et al.  Spring bloom sedimentation in a subarctic ecosystem , 1992, Marine Biology.

[78]  Ian Morris.  The Physiological Ecology of Phytoplankton , 1981 .

[79]  J. Egge,et al.  Blooms of phytoplankton including Emiliania huxleyi (Haptophyta). Effects of nutrient supply in different N : P ratios , 1994 .

[80]  L. Rhodes,et al.  Suffocation of pilchards (Sardinops sagax) by a green microalgal bloom in Wellington Harbour, New Zealand , 1994 .

[81]  C. D’Elia,et al.  Biological Oceanography: An Early History, 1870-1960 , 2012 .

[82]  P. Holligan,et al.  Satellite and ship studies of coccolithophore production along a continental shelf edge , 1983, Nature.

[83]  A. Herbland,et al.  Do Dinophysis spp. come from the "open sea" along the French Atlantic coast? , 1993 .

[84]  Silva Es.  Intracellular bacteria: the origin of dinoflagellate toxicity. , 1990 .

[85]  K. Wakamatsu,et al.  Okadaic acid: an additional non-phorbol-12-tetradecanoate-13-acetate-type tumor promoter. , 1988, Proceedings of the National Academy of Sciences of the United States of America.

[86]  F. Rey,et al.  Oceanographic conditions in the sandsfjord system, western Norway, after a bloom of the toxic prymnesiophyte Prymnesium parvum carter in August 1990 , 1992 .

[87]  K. P. Andersen,et al.  Coagulation efficiency and aggregate formation in marine phytoplankton , 1990 .

[88]  D. Cushing,et al.  The loss of diatoms in the spring bloom , 1992 .

[89]  Engel G. Vrieling,et al.  TOXIC PHYTOPLANKTON BLOOMS IN THE SEA , 1993 .

[90]  M. Kent,et al.  Gill lesions and mortality in seawater pen-reared Atlantic salmon Salmo salar associated with a dense bloom of Skeletonema costatum and Thalassiosira species , 1995 .

[91]  F. Jochem,et al.  Productivity regime and phytoplankton size structure in the tropical and subtropical North Atlantic in spring 1989 , 1993 .

[92]  G. Hallegraeff.  A review of harmful algal blooms and their apparent global increase , 1993 .

[93]  F. Colijn,et al.  Primary production of phytoplankton at a frontal zone located at the northern slope of the Dogger Bank (North Sea) , 1990 .

[94]  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 .

[95]  K. Richardson,et al.  Seasonal distribution of chlorophyll-a in relation to physical structure in the western irish sea , 1985 .

[96]  P. Holligan,et al.  The vertical distribution and succession of phytoplankton in the western English Channel in 1975 and 1976 , 1977, Journal of the Marine Biological Association of the United Kingdom.

[97]  S. Shumway,et al.  The Physiological Effect of Aureococcus anophagefferens ("brown tide") on the Lateral Cilia of Bivalve Mollusks. , 1991, The Biological bulletin.

[98]  Dennis A. Hansell,et al.  Chemical characterization of three large oceanic diatoms: potential impact on water column chemistry , 1992 .

[99]  W. Dennison,et al.  Recurrent and persistent brown tide blooms perturb coastal marine ecosystem , 1987 .

[100]  F. Taylor,et al.  A bloom of the planktonic diatom, Cerataulina pelagica, off the coast of northeastern New Zealand in 1983, and its contribution to an associated mortality of fish and benthic fauna , 1985 .

[101]  G. Cadée.  Increased phytoplankton primary production in the Marsdiep area (Western Dutch Wadden Sea) , 1986 .

[102]  E. Durbin,et al.  Effect of the ”Brown Tide“ on Feeding, Size and Egg Laying Rate of Adult Female Acartia Tonsa , 1989 .

[103]  Katherine Richardson,et al.  Plankton distribution and activity in the North Sea/Skagerrak-Kattegat frontal area in April 1984 , 1985 .

[104]  H. Bigelow,et al.  Phytoplankton and Planktonic Protozoa of the Offshore Waters of the Gulf of Maine , 1940 .

[105]  L. Edler,et al.  29 NOVEL AND NUISANCE PHYTOPLANKTON BLOOMS IN THE SEA : EVIDENCE FOR A GLOBAL EPIDEMIC , 2022 .

[106]  Timothy R. Parsons,et al.  Biological Oceanographic Processes , 1973 .

[107]  E. G. Vrieling,et al.  Harmful Marine Algal Blooms , 1995 .

[108]  G. Cadée,et al.  Seasonal and annual variation in phaeocystis pouchetii (haptophyceae) in the westernmost inlet of the Wadden Sea during the 1973 to 1985 period , 1986 .

[109]  C. Garside,et al.  The “f-ratio” on 20°W during the North Atlantic Bloom Experiment , 1993 .

[110]  D. Purdie,et al.  Evidence for avoidance of flushing from an estuary by a planktonic, phototrophic ciliate , 1991 .

[111]  S. Bates,et al.  Pennate Diatom Nitzschia pungens as the Primary Source of Domoic Acid, a Toxin in Shellfish from Eastern Prince Edward Island, Canada , 1989 .

[112]  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 .

[113]  Donald M. Anderson,et al.  Dynamics and physiology of saxitoxin production by the dinoflagellatesAlexandrium spp. , 1990 .

[114]  Ø. Moestrup,et al.  Domoic acid, the toxic amino acid responsible for amnesic shellfish poisoning, now in Pseudonitzschia seriata (Bacillariophyceae) in Europe , 1994 .

[115]  D. Cushing.  A difference in structure between ecosystems in strongly stratified waters and in those that are only weakly stratified , 1989 .

[116]  M. Huntley.  Temperature-Dependent Production of Marine Copepods: A Global Synthesis , 1992, The American Naturalist.

[117]  E. Carpenter,et al.  Novel Phytoplankton Blooms , 1989, Coastal and Estuarine Studies.

[118]  F. Taylor,et al.  Distribution of Potentially Harmful Phytoplankton Species in the Northern Strait of Georgia, British Columbia , 1990 .

[119]  T. O'Shea,et al.  AN EPIZOOTIC OF FLORIDA MANATEES ASSOCIATED WITH A DINOFLAGELLATE BLOOM , 1991 .

[120]  P. Liss,et al.  Dimethylsulphide and dimethylsulphoniopropionate in the Northeast atlantic during the summer coccolithophore bloom , 1993 .

[121]  S. Long,et al.  Photosynthesis in Contrasting Environments , 1986 .

[122]  Paul J. Harrison,et al.  Effects of nutrient limitation on toxin production and composition in the marine dinoflagellate Protogonyaulax tamarensis , 1987 .

[123]  P. Tester,et al.  Toxic effect of the bloom-forming Trichodesmium sp. (Cyanophyta) to the copepod Acartia tonsa. , 1994, Natural toxins.

[124]  Gustaaf M. Hallegraeff,et al.  Transport of toxic dinoflagellate cysts via ships' ballast water☆ , 1991 .

[125]  T. Honjo.  The biology and prediction of representative red tides associated with fish kills in Japan , 1994 .

[126]  W. Balch,et al.  Tidal Stirring vs. Stratification: Microalgal Dynamics with Special Reference to Cyst-Forming, Toxin Producing Dinoflagellates , 1986 .

[127]  P. Fiedler.  Zooplankton avoidance and reduced grazing responses to Gymnodinium splendens (Dinophyceae)1 , 1982 .

[128]  M. Huntley,et al.  Copepods in ice-covered seas—Distribution, adaptations to seasonally limited food, metabolism, growth patterns and life cycle strategies in polar seas , 1991 .

[129]  D. M. Nelson,et al.  Phytoplankton bloom dynamics of the western Ross Sea ice edge—II. Mesoscale cycling of nitrogen and silicon , 1986 .

[130]  M. Scranton.  The role of the cyanobacterium Oscillatoria (Trichodesmium) thiebautiim the marine hydrogen cycle , 1983 .

[131]  Patrick M. Holligan,et al.  Causes and consequences of variability in the timing of spring phytoplankton blooms , 1994 .

[132]  Meinrat O. Andreae,et al.  Ocean-atmosphere interactions in the global biogeochemical sulfur cycle* , 1990 .

[133]  B. Heimdal,et al.  Brown water on the Norwegian coast in autumn 1966 , 1970 .

[134]  H. J. Niebauer.  Bio-physical oceanographic interactions at the edge of the Arctic ice pack , 1991 .

[135]  Thomas Kiørboe,et al.  Turbulence, Phytoplankton Cell Size, and the Structure of Pelagic Food Webs , 1993 .

[136]  健児 安元,et al.  下痢性貝毒原因種,渦鞭毛藻Dinophysis fortiiの同定 , 1980 .

[137]  G. Llano,et al.  Biology of the Antarctic seas , 1964 .

[138]  W. Balch.  An apparent lunar tidal cycle of phytoplankton blooming and community succession in the Gulf of Maine , 1981 .

[139]  D. Baden,et al.  Brevetoxins, unique activators of voltage-sensitive sodium channels, bind to specific sites in rat brain synaptosomes. , 1986, Molecular pharmacology.

[140]  C. Reynolds.  Phytoplankton assemblages and their periodicity in stratifying lake systems , 1980 .

[141]  H. Kaas,et al.  The structure of the pelagic food web in relation to water column structure in the Skagerrak , 1990 .

[142]  R. Bak,et al.  Lysis-induced decline of a phaeocystis spring bloom and coupling with the microbial foodweb , 1992 .

[143]  J. Goering,et al.  UPTAKE OF NEW AND REGENERATED FORMS OF NITROGEN IN PRIMARY PRODUCTIVITY1 , 1967 .

[144]  E. Paasche,et al.  Three years after the Chrysochromulina polylepis bloom in Scandinavian waters in 1988 : some conclusions of recent research and monitoring , 1993 .

[145]  W. Gurney,et al.  Ecosystem models of Scottish sea lochs for assessing the impact of nutrient enrichment , 1993 .

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

[147]  P. Tett,et al.  A Red Tide of Gyrod Inium Aurelum in Sea Lochs of the Firth of Clyde and Associated Mortality of Pond-Reared Salmon , 1982, Journal of the Marine Biological Association of the United Kingdom.

[148]  C. Brown,et al.  Coccolithophorid blooms in the global ocean , 1994 .

[149]  E. Fahrbach,et al.  Early spring phytoplankton blooms in ice platelet layers of the southern Weddell Sea, Antarctica , 1992 .

[150]  J. Heilmann,et al.  Annual distribution and activity of phytoplankton in the Skagerrak/ Kattegat frontal region , 1994 .

[151]  S. Bates,et al.  Controls on Domoic Acid Production by the Diatom Nitzschia pungens f. multiseries in Culture: Nutrients and Irradïance , 1991 .

[152]  P. Holligan,et al.  Vertical distribution and partitioning of organic carbon in mixed frontal and stratified waters of the English Channel , 1984 .

[153]  D. L. Aksnes,et al.  Silicate as regulating nutrient in phytoplankton competition , 1992 .

[154]  K. Richardson,et al.  Seasonal distribution and production of phytoplankton in the southern Kattegat , 1991 .

[155]  P. Holligan,et al.  What controls the distribution of the coccolithophore, Emiliania huxleyi, in the North Sea? , 1993 .

[156]  K. Richardson,et al.  The Chrysochromulina polylepis bloom in the Kattegat (Scandinavia) May-June 1988. Distribution, primary production and nutrient dynamics in the late stage of the bloom , 1991 .

[157]  G. Codd,et al.  The Toxicity of Trichodesmium Blooms from Caribbean Waters , 1992 .

[158]  Ian R. Falconer,et al.  Algal toxins in seafood and drinking water , 1993 .

[159]  E. Carpenter,et al.  Marine pelagic cyanobacteria : Trichodesmium and other diazotrophs , 1992 .

[160]  F. Morel,et al.  Colimitation of phytoplankton growth by nickel and nitrogen , 1991 .

[161]  V. Smetácek.  Role of sinking in diatom life-history cycles: ecological, evolutionary and geological significance , 1985 .

[162]  A. Cembella,et al.  Potential impact of a toxic dinoflagellate (Alexandrium excavatum) bloom on survival of fish and crustacean larvae , 1991 .

[163]  T. Ogata,et al.  Effect of water temperature and light intensity on growth rate and toxicity change in Protogonyaulax tamarensis , 1987 .

[164]  W. Smith.  Nitrogen uptake and new production in the Greenland Sea : the spring Phaeocystis bloom , 1993 .

[165]  F. Olsgard.  Do toxic algal blooms affect subtidal soft-bottom communities? , 1993 .

[166]  O. Lindahl.  Offshore growth of Gyrodinium aureolum (Dinophyceae) ― the cause of coastal blooms in the Skagerrak area? , 1986 .

[167]  J. Burkholder,et al.  Fish kills linked to a toxic ambush-predator dinoflagellate: distribution and environmental conditions , 1995 .

[168]  Katherine Richardson,et al.  ADAPTATION OF UNICELLULAR ALGAE TO IRRADIANCE: AN ANALYSIS OF STRATEGIES , 1983 .

[169]  T. Aarup,et al.  The North Sea: Satellite colour atlas , 1989 .

[170]  Katherine Richardson,et al.  Primary production in the Kattegat: Past and present , 1995 .

[171]  P. Wal,et al.  Production and downward flux of organic matter and calcite in a North Sea bloom of the coccolithophore Emiliania huxleyi , 1995 .

[172]  R. Lingeman,et al.  Estimating the impact of fungal parasites on phytoplankton populations , 1992 .

[173]  J. Havenhand,et al.  Effects of the planktonic flagellate Chrysochromulina polylepis Manton et Park on fertilization and early development of the ascidian Ciona intestinalis (L.) and the blue mussel Mytilus edulis L , 1988 .

[174]  G. Doucette,et al.  Characterization of bacteria associated with different isolates of Alexandrium tamarense , 1995 .