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Module VII
Harmful Algal Blooms (4 hours)
Contents
1.1. Suggested reading
1.2. The harmful algae
1.3. The algal toxins
1.4. Biological effects of the toxins
1.5. Coupling between occurrence of toxic algae and toxicity of shellfish and finfish
1.6. References
References in bold are literature which will be made available during the practical part of the
course; selected articles are included in the literature folder of the distant learning
programme.
1.1. Suggested reading
Present document and the following papers:
Hallegraeff, G.M. 2010. Ocean climate change, phytoplankton community responses, and
harmful algal blooms: a formidable predictive challenge. – J. Phycol. 46: 220-235.
1.2. The harmful algae
Marine phytoplankton blooms - or 'red tides' - are naturally occurring phenomena. About 300
species are reported at times to form blooms with cell concentrations of several million per
liter. It appears that boththe frequency, intensity and geographical distribution of algal blooms
have increased over the last few decades (Smayda 1990, Hallegraeff 2004). The possible
influence of climate changes has been reviewed by Hallegraeff (2010), and the possible role
of ballast water dispersal in relation to harmful algal blooms was discussed by Smayda
(2007).
Close to one fourth of the bloom forming species is known to produce toxins that may be
detrimental or even fatal to other flora and fauna including human beings. Presently, six
human syndromes are recognized caused by algal toxins accumulated in fin- or shellfish.
Despite the very different chemical nature of the toxins, these do not generally change or
reduce significantly in amount upon cooking, and neither do they generally influence the
taste of the meat. Unfortunately, detection of contaminated seafood is not straightforward,
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Harmful algal blooms, page 2 of 12
and neither fishermen nor consumers can usually determine whether seafood products can
safely be consumed.
In recognition of the potential health risks associated with the consumption of contaminated
seafood, the government authorities in many countries have imposed restrictions on certain
seafood products for human consumption. These restrictions include analyses of the seafood
products for algal toxins, and by many countries it is also required that monitoring
programmes for the detection of harmful algae are established (Anderson et al. 2001).
In addition to posing serious health risks to consumers of seafood, some toxic algae may
have devastating effects on fish, both in the wild and in aquaculture. Several species of
phytoplankton belonging in different taxonomic groups can produce toxins, which may result
in extensive fish kills with major economic losses (Shumway 1990, Corrales & Maclean
1995, Zingone & Enevoldsen 2000). A comprehensive economic analysis of the global
impact of phytoplankton blooms on the aquaculture industry is not available, but the direct
economic losses from single events in North America and especially Japan and South East
Asia have on several occasions amounted to more than 10 million US dollars.
'Red tides' is a concept previously applied by the international scientific community to events
of harmful algal blooms (HAB), which is now the preferred terminology. It should be noted,
however, that harmful effects are not necessarily associated only with toxin production by the
microalgae. Some species may cause fish kills or other harmful events through secondary
effects of intensive blooms, e.g. oxygen depletion or physical damage to fish gills. Such
species include for example the dinoflagellate, P. micans, several species of the diatom
genus Chaetoceros and a number of others (Hallegraeff et al. 2004). On the other hand,
harmful effects may be caused by even very low cell concentrations of toxic species, e.g.
Alexandrium spp. or Dinophysis spp., which are by no means reminiscent of a bloom as
generally conceived. A bloom in this context may be defined as cell concentrations
sufficiently high to cause harmful effects.
In 1997, the IOC Intergovernmental Panel on Harmful Algal Blooms decided to establish a
Task Team on Algal Taxonomy with the aim of providing an agreed reference list of harmful
algal species, including correct citation of the author(s), date of valid publication, and a list of
synonyms http://www.marinespecies.org/hab/
Further reading on HAB may be found in the GEOHAB Science Plan (2001).
1.3. The algal toxins
Many species of microalgae are now known or suspected to produce toxins. In marine and
brackish water environments most toxic species belong in the Dinophyceae, but also the
Diatomophyceae, Haptophyceae, Raphidophyceae, and Cyanophyceae comprise toxic species.
The algal toxins may cause damage to other flora and fauna directly or they may accumulate
through the food web in e.g. shellfish or finfish thereby causing harm to their predators including
humans (Backer et al. 2004, Hallegraeff 2004, Landsberg 2002).
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Harmful algal blooms, page 3 of 12
Consumption of contaminated seafood may cause various gastrointestinal or neurological
diseases in humans. The human syndromes and their most important symptoms are
summarised in Table 1. There are currently no antidotes against these syndromes, but
prolonged artificial respiration may save persons from even severe PSP, and treatment with
mannitol may relieve the symptoms in case of ciguatera (Hallegraeff 2004).
Shellfish and coral reef fish are causing most problems, but also other marine animals, e.g.
birds, crabs, turtles, and sharks may accumulate algal toxins (Shumway 1990, Landsberg
2002, Shumway et al. 2003). IT IS IMPORTANT TO NOTICE THAT THE ALGAL TOXINS DO NOT GIVE
BAD SMELL OR TASTE TO THE SEAFOOD, AND THEREFORECANNOT IMMEDIATELY BE DETECTED BY
THE FISHERMEN OR THE CONSUMER, BUT ONLY THROUGH BIOASSAYS OR CHEMICAL ANALYSES. IT
IS ALSO VERY IMPORTANT TO EMPHASIZE THAT THE ALGAL TOXINS ARE NOT DESTROYED BY
COOKING AND THUS MAY BE PRESENT IN CANNED, FROZEN OR OTHERWISE PROCESSED SEAFOOD
PRODUCTS.
The highest toxin production in the algal cells may occur at different stages of growth in the
different species. Thus in the species of Alexandrium studied so far, the toxin production is
highest during the exponential growth phase (Cembella 1998 and references therein), while
in species of Pseudo-nitzschia, the toxin production takes place during the stationary growth
phase (Bates 1998 and references therein). A marked exception is Prorocentrum cordatum,
which seems to be toxic only in the late stationary and senescent growth phase (Grzebyk et
al. 1997).
Table 1. Symptoms of algal toxin poisoning (modified from Hallegraeff 2004).
Human syndrome
Amnesic shellfish
poisoning, ASP
Azaspirazid poisoning, AZP
Ciguateric fish
poisoning, CFP
Diarrheic shellfish
poisoning, DSP
Neurotoxic shellfish
poisoning, NSP
Paralytic shellfish
poisoning, PSP
Symptoms
Mild
Severe
After 3-5 hours: nausea, vomiting, diarDecreasing reaction to deep pain, dizzirhoea, abdominal cramps
ness, hallucinations, confusion, short-term
memory loss, seizures
Nausea, vomiting, severe diarrhoea,
stomach cramps
After 12- 24 hours: gastro-intestinal
Neurological symptoms such as numbsymptoms such as diarrhoea, abdominal
ness and tingling of hands and feet, cold
pain, nausea, vomiting.
objects feel hot to touch; difficulty in balance, low heart rate and blood pressure,
rashes.
In extreme cases death through respiratory failure.
After 30 min.- a few hours (seldom more
Chronic exposure may promote tumour
than 12 hours): diarrhoea, nausea,
formation in the digestive system.
vomiting, abdominal pain.
After 3-6 hours: chill, headache, diarrhoea, Paraesthesia, altered perception of hot and
muscle weakness, muscle and joint pain,
cold; difficulty in talking and swallowing
nausea and vomiting
Within 30 minutes: tingling sensation or
Muscular paralysis, pronounced respiratory
numbness around lips gradually spreading
difficulty, choking sensation, death through
to face and neck, prickly sensation in
respiratory paralysis may occur within 2-24
fingertips and toes, headache, dizziness,
hrs.
nausea, vomiting, diarrhoea.
Considerable clonal differences exist in many species ranging from highly toxic to low or
even non-toxic clones. These differences are in some cases seen within the same
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geographical area, while in other cases they relate to the geographical distribution. Such
clonal differences are known from e.g. species of Alexandrium (Cembella 1998),
Gymnodinium catanatum (Oshima et al. 1993), and species of Pseudo-nitzschia (Bates et
al. 1998).
1.4. Biological effects of the toxins
A detailed description of toxin chemistry and analytical methods is beyond the scope of this
course. The chemical nature and the biological effects of algal toxins in the marine environment
are summarised in Table 2. Extensive accounts of algal toxins, their effects, analytical methods
etc. may be found in Falconer (1993), Botana (2000), Landsberg (2002), and Hallegraeff et al.
(2004).
Table 2. Summary of the most important toxins produced by marine microalgae and their
biological effects with selected references. The human syndromes referred to in Table 1 are
indicated in bold in the first column.
Toxins and their effects
on the environment
Saxitoxins and saxitoxin
derivatives, heterocyclic
guanidines, about 20
naturally occurring
derivative are known,
causing PSP
Chemical
affinity
Alcaloids
Causative species
Biological effects
References
Alexandrium spp.,
Gymnodinuim
catenatum,
Pyrodinium
bahamense var.
compressum
Trichodesmium spp
Neurotoxic, block the
+
Na channels of
neuronal and muscular
cells, preventing
depolarisation and
propagation of the
action potential
Shimizu (2000)
Long &
Carmichael
(2004)
Domoic acids (DA), 10
congeners, causing ASP
Amino acids
Pseudo-nitzschia
spp, Nitzschia navisvaringica, Amphora
caffeaeformis
Both neurogical and
gastrointestinal effects,
strong glutamate
agonist
Azaspirazids, 3
congeners, causing AZP
Polyether
compounds
Azadinium spinosum
Neurotoxic symptoms
with slow pro-gressive
paralysis in mice, DSPlike symptoms in
humans
Brevetoxins, 2 groups of
toxins with 10 naturally
occurring analogues,
causing fish kills and NSP
Polyether
compounds
Karenia brevis,
Chattonella spp.
Ciguatoxins (CTX), more
than 20 analogues are
known, main cause of CFP
Polyether
compounds
Gambierdiscus
toxicus
Neurotoxic, bind to the
+
Na -channel resulting
in persistent activation
of nerve cells; some
toxin analogues with
haemolytic effects
Complex neurotoxic
effects primarily due to
+
activation of the Na channel of cell
membranes
Bates (1998),
Skov et al.
(1999), Nijjar &
Nijjar (2000),
Van Dolah
(2000), Quilliam
(2004a)
Tillmann et al.
2009, Satake et
al. (1998), Ito et
al. (2001), James
et al. (2001),
Quilliam (2004b)
Baden & Adams
(2000), Quilliam
(2004b)
Wright &
Cembella
(1998), Lewis et
al. (2000), Lewis
(2004)
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Cooliatoxin
Polyether
compounds
Coolia monotis
Galacto-lipids, fatty acids
Polyether
compounds
Gymnodimine
Polyether
compounds
Amphidinium
carterae, A. operculatum, Karenia
mikimotoi, Chrysochromulina polylepis
Karenia mikimotoi,
Gymnodinium spp. ?
Maitotoxins (MTX), 3
congeners, implicated in
CFP
Polyether
compounds
Gambierdiscus
toxicus
Okadaic acid (OA),
dinophysis toxins (DTX-1
and DTX-2), at least 8
conge-ners but some are
believed to be precursors
or shellfish metabolites,
casuing DSP
Palytoxins
Polyether
compounds
Dinophysis spp,
Prorocentrum spp
Polyether
compounds
Ostreopsis
lenticularis, O.
siamensis
Pectinotoxins, 10
analogues are known
Prorocentrolide, 2
analogues
Polyether
compounds
Polyether
compounds
Dinophysis spp.
Prymnesins
Polyether
compounds
Prymnesium parvum
Haemolytic,
ichthyotoxic
Spirolids, 4 naturally
occurring analogues
Polyether
compounds
Alexandrium
ostenfeldii
Yessotoxins, 6 congeners
are known
Polyether
compounds
Lingulodinium
polyedrum,
Protoceratium
reticulatum
Gonyaulax. spinifera
Chattonella marina,
C. antiqua,
Fibrocapsa japonica,
Olisthodiscus luteus,
Heterosigma
akashiwo,
Cochlodinium
polykrikoides
’Fast-acting toxins’,
neurological symptoms
including convulsions in
mice, effects on
humans unknown
Non-diarrhetic,
apparently interfering
with lipid membranes,
cardiotoxic
Reactive oxygen
compounds
Prorocentrum lima,
P. maculosum
Neurological effects,
blocking of
unmylenated nerves,
causing acute
respiratory distress in
mice
Haemolytic,
ichthyotoxic
Holmes et al.
(1995), James et
al. (2001)
‘Fast-acting toxin’
which is toxic to mice,
ichthyotoxic
Wright &
Cembella
(1998), James et
al. (2001)
Legrand (1998),
Estacion (2000),
Van Dolah
(2000),
Rossini (2000),
Van Dolah
(2000)
Neurotoxic affecting
Ca2+ influx, the precise
mechanism of action
unknown
Inhibitors of protein
phophatase enzymes,
OA presumably a
tumor promotor
Depolarising cell
membranes affecting
both cardiac, smooth,
and sceletal muscles,
and myelinated nerves,
cytotoxic
Non-diarrheic,
hepatotoxic
’Fast-acting toxins’,
Impairment of the
respiratory and
osmoregulatory
functions of the gills
Yasumoto et al.
(1990)
Wright &
Cembella
(1998), Tosteson
(2000)
Draisci et al.
(2000)
Wright &
Cembella
(1998), James et
al. (2001)
Igarishi et al.
(1996), Wright &
Cembella (1998)
Cembella et al.
(2000), Richard
et al. (2001)
Draisci et al.
(2000), Rhodes
et al. (2006)
Landsberg
(2002)
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Kalkitoxin
Nodularins
Cylindrospermopsins
Lipidic –
thiazoline
compound
Cyclic
pentapeptids
Lyngbya majuscula
neurotoxic
Nodularia spumigena
Alcaloids
Umezachia natans
hepatotoxic with
inhibition of proteins
(PP) Phosphatases 1
and 2A
Hepatotoxic, with
inhibition of glutathione
and protein synthesis.
Long &
Carmichael
(2004)
Long &
Carmichael
(2004)
Long &
Carmichael
(2004)
Most algal toxins are neurotoxic, but also toxins with gastro-intestinal effects and cytotoxins,
hepatotoxins, and dermatotoxins are known; the latter 3 types are produced by
cyanobacteria and found in fresh and brackish water habitats.
Neurotoxins. The PSP toxins comprise the largest and also the best characterised group of
neurotoxins. They may be divided into 3 group: 1) the highly toxic carbamate toxin (saxitoxin,
neosaxitoxin, gonyautoxins), 2) the decarbamoyl toxins of intermediate toxicity, and 3) the
weakly toxicN-sulfocarbamoyl toxin. The PSP toxins block the Na+ channels of neuronal and
muscular cells thereby preventing depolarisation and propagation of the action potential,
which is essential for the transmission of nerve impulses and muscle contraction. The
peripheral nervous system is particularly affected (Shimizu 2000).
The ASP toxins are strong competitors to kainate and bind with high affinity to the glutamate
receptors in the brain. Pertinent activation of the kainate glutamate receptors result in
increased intracellular concentration of Ca2+, which in turn may result in cell rupture.
Particularly the hippocampus, the site of learning and memory, part of the brain is affected by
domoic acid (Nijjar & Nijjar 2000).
The ciguatoxins (CTX) which are fat-soluble and the water-soluble maitotoxins (MTX) are the
most potent algal toxins known. The CTXs bind to the sodium-channels making these
permeable to Na+ thereby inducing depolarisation of cell membranes (the opposite effect of
PSP toxins) (Lewis et al. 2000). The biological activity of the MTXs is Ca2+ dependent
causing membrane depolarisation and influx of Ca2+into the cells, although the exact
mechanism of action is unknown (Estacion 2000). The CTX produced by the microalgae
Gambierdiscus toxicus may be transformed though the food web (herbivorous-carnivorous
fish) into more oxidised forms, which are up to 10-fold more toxic than the CTX toxin
produced by the alga (Lewis 2001); thus there may be a bio-magnification of the toxic effects
of CTX toxins. The biological effects of some NSP toxin analogues are similar to those of
CTX s.
Toxins with gastro-intestinal effects. The DSP toxins inhibit protein phophatase enzymes,
which regulate a large and diverse array of cellular processes. The diarrhoea associated with
DSP is presumably caused by hyper-phosphorylation of proteins in the epithelia of the
intestine resulting in disturbance of the water balance (Van Dolah 2000 and references
therein). There is mounting evidence that okadaic acid is a tumour promotor (Rossini 2000
and references therein).
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Pectenotoxins (PTXs) and Yessotoxins (YTXs) are usually grouped with the DSP toxins
because these toxins often co-occur and are extracted together from shellfish. The molecular
basis of the activity of these toxins is virtually unknown. None of them cause diarrhoea; PTXs
are strongly hepatotoxicwhile the most important effect of YTXs seems to be on the cardiac
muscle. The chemical structure of YTXs is closely related to MTXs (Draisci et al. 2000).
Fast-acting toxins. Gymnodimine, prorocentrolids, spirolids, and pinnatoxins are called fastacting toxins because they rapidly kill mice in bioassays. The origin of pinnatoxins is
unknown, while the others are producedby microalgae. The possible effects of these toxins
on humans are unknown.
Ichthyotoxins. Several species of harmful algae are known cause fish kills. The toxic
principles involved include various haemolytic and reactive oxygen compounds as well as
several compounds not yet characterized. (see Landsberg 2002 and Hallegraeff et al. 2004,
and reference therein). Haemolytic compounds are produced by different species of
unarmoured dinoflagellates, e.g. Amphidinium carterae, A. operculatum, and Karenia
mikimotoi, but also Alexandrium tamarense may produce haemolytic compounds, which may
cause fish kills. Shellfish mortality has been associated with blooms of Heterocapsa
circularisquama, and Oda et al. (2001) suggested that this was caused by a haemolytic toxin
but other unknown compounds may alsobe involved. Other species that may cause fish kills
through production of haemolytic toxins are the haptophytes Prymnesium spp. and
Chrysochromulina leadbeateri and C. polylepis.
Reactive oxygen compounds (e.g. superoxides and hydrogen peroxide) are produced by
several species of raphidophytes, which have caused severe fish kills on several occasions.
A number of unmamoured dinoflagellates, e.g. Karlodinium micrum, and some species
related to Karenia mikimotoi may cause fish kills but the toxic compounds are unknown
1.5. Coupling between occurrence of toxic algae and toxicity of
shellfish and finfish
In most cases where algal toxins cause human illness, the vector is shellfish or in case of
CFP finfish (Shumway 1990, Landsberg 2002). Planktonic microalgae are food for filter
feeding shellfish, and if toxic species are ingested, the algal toxins accumulate in the tissue
of the shellfish. The shellfish do not seem to be severely affected by the toxins, but in some
cases, the filtration rate decreases. Rates of toxin accumulation and depuration depend on
the species of shellfish. Mussels accumulate andeliminate the algal toxins fast (Peperzak et
al. 1995), while scallops (e.g. Saxidomus giganteus, Spisula solidissima, Siliqua patula) may
retain the algal toxins in their tissue for several years (Fernandez et al. 2004).
One of the main difficulties in the monitoring and management of HAB is the apparent lack of
a direct and simple relationship between the occurrence of potentially toxic algal species and
toxicity in shellfish. There may be many reasons for this apparent discrepancy including
insufficient knowledge of the autecology of both the algae and the shellfish species involved
and also insufficient sampling programmes and data analysis. One parameter, which is rarely
considered in monitoring programmes, is relative cell abundance. This may, however, be
important because the filtration rate of the shellfish depends on the food available, viz. the
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phytoplankton biomass. Thus, Dahl & Johannessen (2001) found good relationship
between the concentration of DSP toxins in blue mussels (Mytilus edulis) and increasing
ratios of Dinophysis acuta (cells l-1) to chlorophyll a.
Ciguatoxins accumulate in coral reef fish, and at least 400 species of fish may cause
ciguatera. Maitotoxins are even more potent than ciguatoxins, but being water-soluble they
are not believed to play a significant role in CFP (Estacion 2000, Lewis 2001).
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1.5. References
Anderson, D.M., Andersen, P., Bricelj, V.M.,Cullen, J.J., Rensel, J.E. 2001. Monitoring and
management strategies for harmful algal blooms in coastal waters. - APEC #201-MR01.1, Asia Pacific economic program, Singapore, and Intergovernmental
Oceanographic Commission technical series no. 59, Paris, 268 pp.
Backer, L.C., Fleming, L.E., Rowan, A.D. & Baden, D.G. 2004. Epidemiology, public health
and human deceases associated with harmful marinealgae. – In: Hallegraeff, G.M.,
Anderson, D.M., Cembella, A.D. (eds), Manual on Harmful Marine Microalgae. –
Monographs on oceanographic methodology 11, Unesco, Paris, pp. 723-750.
Baden, D.G. & Adams, D.J. 2000. Brevetoxin: chemistry, mechanism of action, and methods
of detection. – In: Botana, L.M. (ed.) 2000. Seafood and freshwater toxins, Marcel
Dekker, NewYork, pp. 505-532.
Bates, S.S. 1998. Ecophysiology and metabolism of ASP toxin production - In: Anderson,
D.M., Cembella, A.D. & Hallegraeff, G.M. (eds), Physiological ecology of harmful algal
blooms, NATO ASI series, Series G, Ecological Sciences, vol. 41, Springer-Verlag,
Berlin, pp. 267-292.
Bates, S.S., Garrison, D.L. & Horner, R.A. 1998. Bloom dynamics and physiology of
domoic-acid-producing Pseudo-nitzshcia species. - In: Anderson, D.M., Cembella, A.D.
& Hallegraeff, G.M. (eds), Physiological ecology of harmful algal blooms, NATO ASI
series, Series G, Ecological sciences, vol. 41, Springer-Verlag, Berlin, pp. 405-426.
Botana, L.M. (ed.) 2000. Seafood and freshwater toxins. - Marcel Dekker, New York, 798 pp.
Carstensen, J., Henriksen, P. & Heiskanen, A-S. 2007. Summer algal blomms in shallow
estuaries: definitions, mechanisms and link to eutrofication. – Limnol. Oceanogr. 52:
370-384.
Cembella, A.D. 1998. Ecophysiology and metabolism of paralytic shellfish toxins in marine
microalgae. - In: Anderson, D.M., Cembella, A.D. & Hallegraeff, G.M. (eds),
Physiological ecology of harmful algal blooms, NATO ASI series, Series G, Ecological
Sciences, vol. 41, Springer-Verlag,Berlin, pp. 381-426.
Cembella, A.D., Lewis, N.I. & Quilliam, M.A. 2000. The marine dinoflagellate Alexandrium
ostenfeldii (Dinophyceae) as the causative organism of spirolide shellfish toxins. –
Phycologia 39: 67-74.
Corrales, R. A. & Maclean, J. L. 1995. Impacts of harmful algae on sea farming in the AsiaPacific areas. - J. App. Phycol. 7: 151-162.
Dahl, E. & Johannesen, T. 2001. Relationship between occurrence of Dinophysis species
(Dinophyceae) and shellfish toxicity. - Phycologia 40: 223-227.
Draisci, R., Lucentini, L., Mascioni, A. 2000. Pectinotoxins and yessotoxins: chemistry,
toxicology, pharmacology, and analysis. - In: Botana, L.M. (ed.), Seafood and
freshwater toxins, Marcel Dekker, New York, pp. 289-324.
Estacion, M. 2000. Ciguatera toxins: mechanism of action and pharmacology of maitotoxin. In: Botana, L.M. (ed.), Seafood and freshwater toxins, Marcel Dekker, New York, pp.
473-503.
Falconer, I.R. (ed.) 1993. Algal toxins in seafood and drinking water. - Academic Press,
London, 224 pp.
Fernandes, L.F., Zehnder-Alves, L. & Bassfeld, J.C. 2001. The recently established
diatom Coscinodiscus wailesii (Coscinodiscales, Bacillariophyta): remarks on
morphology and distribution.- Phycological Research 49:89-96.
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Fernandez, M.L., Shumway, S. & Blanco, J. 2004. Management of shellfish resources. - In:
Hallegraeff, G.M., Anderson, D.M., Cembella, A.D. (eds), Manual on Harmful Marine
Microalgae, Monographs on oceanographic methodology 11, Unesco, Paris, pp. 657692.
GEOHAB, 2001. Global Ecology and Oceanography of Harmful Algal Blooms, Science Plan.
P. Glibert & G. Pitcher (eds). SCOR and IOC, Baltimore and Paris. 87 pp.
Grzebyk, D., Denardou, A.,Berland, B. & Pouchus, T.F. 1997. Evidence of a new toxin in
the red-tide dinoflagellate Prorocentrum minimum. - J. Plankton Res. 19: 1111-1124.
Hallegraeff, G.M. 2004. Harmful algal blooms: a global overview. - In: Hallegraeff, G.M.,
Anderson, D.M., Cembella, A.D. (eds), Manualon Harmful Marine Microalgae,
Monographs on oceanographic methodology 11,Unesco, Paris, pp. 25-50.
Hallegraeff, G.M. 2010. Ocean climate change, phytoplankton community responses, and
harmful algal blooms: a formidable predictive challenge. – J. Phycol. 46: 220-235.
Hallegraeff, G.M., Anderson, D.M., Cembella, A.D. (eds) 2004. Manual on Harmful Marine
Microalgae. - Monographs on oceanographic methodology 11, Unesco, Paris, 793 pp.
Hasle, G. R. 1972. The distribution of Nitzshia seriata and allied species. - Nova Hedwigia,
Beih. 39: 171-190.
Holmes, M.J., Lewis, R.J., Jones, A. & Wong Hoy, A.W. 1995. Cooliatoxin, the first toxin from
Coolia monotis (Dinophyceae). - Nat. Toxins 3: 355-362.
Igarishi, T., Satake, M. & Yasumoto, T. 1996. Prymnesin-2: a potent ichthyotoxin and
hemolytic glycoside isolated from the red tide alga Prymnesium parvum. - J. Am.
Chem. Soc. 118: 479-480.
Ito, E., Satake, M., Ofuji, K., McMahon, T., Silke, J., James, K. & Yasumoto, T. 2001. Small
intestinal injuries in mice caused by a new toxin, azaspirazid, isolated from Irish
mussles. - In: Hallegraeff, G.M., Blackburn, S.I., Boalch, C.J. & Lewis, R.J. (eds),
Harmful Algal Blooms 2000, Intergovernmental Oceanographic Commission of
Unesco, Paris, pp. 395-398.
James, K.J., Furey, A., Satake, M. & Yasumoto, T. 2001. Azaspirazid poisoning (AZP): a
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