&EPA
United States
Environmental Protection
Agency
Office of Research and
Development
Washington DC 20460
EPA/600/R-92/079
June 1992
A Status Report on
Planktonic Cyanobacteria
(Blue-Green Algae) and
Their Toxins
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EPA/600/R-92/079
June 1992
A STATUS REPORT ON PLANKTONIC CYANOBACTERIA
(BLUE-GREEN ALGAE) AND THEIR TOXINS
Wayne W. Carmichael
Aquatic Biology/Toxicology
Department of Biological Sciences
Wright State University
Dayton, Ohio 45435
Project Officer
Robert S. Safferman
Microbiology Research Division
Environmental Monitoring Systems Laboratory
Cincinnati, Ohio 45268
ENVIRONMENTAL MONITORING SYSTEMS LABORATORY
OFFICE OF RESEARCH AND DEVELOPMENT
U.S. ENVIRONMENTAL PROTECTION AGENCY
CINCINNATI, OHIO 45268
$%) Printed on Recycled Paper
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DISCLAIMER
The development of this document has been funded wholly or in part by the United
States Environmental Protection Agency under Order No. OC6238NASXT to Wright State
University. The document has been subjected to the Agency’s administrative and peer
review and has been approved for publication as an EPA document.
II
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FOREWORD
Environmental measurements are required to determine the quality of ambient waters
and the character of waste effluents. The Environmental Monitoring Systems Laboratory -
Cincinnati (EMSL-Cincinnati) conducts research to:
• Develop and evaluate analytical methods to identify and measure the
concentration of chemical pollutants in drinldng waters, surface waters,
groundwaters, wastewaters, sediments, sludges, and solids wastes.
• Investigate methods for the identification and measurement of viruses, bacteria and
other microbiological organisms in aqueous samples and to determine the responses
of aquatic organisms to water quality.
• Develop and operate a quality assurance program to support the achievement of
data quality objectives in measurements of pollutants in drinking waters, surface
waters, groundwaters, wastewaters, sediments, and solid wastes.
• Develop methods and models to detect and quantify responses in aquatic and
terrestrial organisms exposed to environmental stressors and to correlate the
exposure with effects on chemical and biological indicators.
The overall objective of this document is to advise the U.S. Environmental Protection
Agency on the current impact of toxic cyanobäcteria (blue-green algae) on the water
environment. The document focuses specifically on the toxins of these organisms as they
relate to the deterioration of surface water quality. Toxic waterblooms are responsible for
sporadic, but recurrent episodes of illness and death among wild and domestic animals.
Cyanobactenal toxins have also been implicated in human poisoning from certain municipal
and recreational water supplies.
Thomas A. Clark, Director
Environmental Monitoring Systems
Laboratory - Cincinnati
111
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ABSTRACT
Toxic blue-green algae (cyanobacteria) continue to be agents of certain water-based
toxicoses. Their presence is now being acknowledged in many of the world ‘s fresh and
brackish waters with eutrophication status of meso to hypereutrophic. Dense surface scums
called waterblooms will occur for a few days, weeks or months when temperature, nutrient
and stratification status of these water bodies is appropriate. It is during these waterblooms
that the concentration of toxins exceeds a level such that any animal can ingest an acutely
lethal dose of toxic cells or toxins. Laboratory studies, using subacute levels of the main
blue-green toxin group, have shown them to be a potent promoter of liver tumors. It is the
continued presence of these toxins in water supplies, plus a new understanding of the
toxins’ structure and function, that has prompted this status report. This report summarizes
the present understanding on toxic blue-green algae and their toxins. This information can
be used to define directions for research and bring about those areas of concern for public
health studies.
iv
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TABLE OF CONTENTS
Title Page
111
iv
1
3
3
7
10
15
15
26
36
39
39
43
48
49
50
71
Foreword
Abstract
Introduction
Cyanobacteria and Their Toxins
Neurotoxins
Hepatotoxins
Microcystins
Nodularin
Occurrence of Toxic Cyanobacteria
Formation of Cyanobacteria Waterblooms and Surface Scums
Control of Cyanobacteria Populations
Health Effects of Cyanobacteria
Hazards to Wild and Domestic Animals
Hazards to Human Health..
Summary
Recommendations for Research and Development
References
Appendir
V
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INTRODUCTION
While algae responsible for producing toxins are found in the divisions Chrysophyta
(class Prymnesiophyceae), Pyrrhophyta (class Dinophyceae or dinoflagellates) and
Cyanophyta (cyanobacteria or blue-green algae), the latter causes most of the problems in
freshwater environments (Carmichael 1986, 1988, 1992; Carmichael et al. 1990; Gorham and
Carmichael 1988; Beasley et al. 1989). The blue-green algae are prokaryotes (without
nuclei) having cell walls composed of peptidoglycan and lipopolysaccharide layers. Many
people now refer to them as cyanobacteria (Staley et al. 1989). The main toxic
cyanobacterial genera include filamentousAnabaena, Aphanizonienon, Nodularia, Oscillatoria
and unicellular colonial Microcystis (Skulberg et a!.; in press). More than one species within
these genera can be toxic, and all toxic species can form water blooms. Surface water
blooms tend to occur on warm summer and autumn days with light wind when water
stagnation and sufficient nutrient concentrations, especially nitrogen and phosphorus, are
present (Skulberg et al. 1984; Pearl 1987). Nutrient concentrations, which contribute to
bloom formation, result from runoff of either fertilizer, livestock or human wastes. Toxic
water blooms can be found in many eutrophic to hypereutrophic lakes, ponds and rivers
throughout the world (Table 1). They are responsible for sporadic, but recurrent episodes
of wild and domestic animal illness and death. They are also implicated in human
poisonings from certain municipal and recreational water supplies.
The primary types of toxicosis include acute hepatotoxicosis, peracute neurotoxicosis,
gastrointestinal disturbances, respiratory and allergic reactions. It is not known whether the
latter toxicoses are caused by the hepato- or neurotoxic agents or by other chemical groups.
It has been suggested, but so far unproven, that lipopolysaccharide (LPS) endotoxins are
involved with the gastrointestinal disturbances (Sykora and Keleti, 1981; Martin et al. 1989).
Many cyanobacterial blooms are apparently not hazardous to animals. This can be due
to: low or no measurable concentrations of toxin within strains and species comprising the
waterbloom; low biomass concentration of the waterbloom; variation in animal species’
sensitivity; amount consumed by the animal as well as age, sex and amount of other food
in the animal ‘s gut. Since toxic and nontoxic blooms of the same species can be found, it
is not always possible to attribute clinical responses to the presence of a bloom of a
toxigenic species. Appropriate diagnostic procedures are therefore needed. These include:
1) establish that animals have been drinking from a concentrated surface bloom, 2)
microscopic identification of a toxigenic species, or at least genus, as the predominant
phytoplankton present, 3) laboratory analysis for the presence of the toxins in the cells, and
4) verification of toxic responses (clinical signs, survival times) in laboratory test animals
(intraperitoneal and oral dosed) to verif ’ that the clinical responses are compatible with the
properties of the algal toxins detected (Carmichael and Schwartz 1984; Beasley et al. 1989).
1
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Table 1. Known occurrences 1 of toxic cyanobacteria in fresh or marine water.
(updated from Gorham and Carmichael, 1988)
ARGENTINA INDIA
AUSTRALIA ISRAEL
CHiLE JAPAN
BANGLADESH NEW ZEALAND
BERMUDA OKINAWA (marine only)
BRAZIL PEOPLES REPUBLIC OF CHINA
SOUTH AFRICA
CANADA THAILAND
Alberta
British Columbia U.S.A.
Manitoba California
Ontario Colorado
Saskatchewan Florida
Hawaii (marine only)
EUROPE Idaho
Czechoslovakia Illinois
Denmark Indiana
Finland Iowa
France Michigan
Germany Minnesota
Greece Mississippi
Hungary Montana
Italy Nebraska
Netherlands Nevada
Norway New Hampshire
Poland New Mexico
Portugal New York
Russia North Dakota
Sweden Ohio
Ukraine Oklahoma
United Kingdom Oregon
Pennsylvania
South Dakota
Texas
Washington
Wisconsin
Wyoming
‘Based upon reports cited in Tables 4 and 5. Occurrences not listed in Tables 4 and 5 are
from previous review articles cited in this report and as primary references cited in the
Appendix [ The Directory to Toxic Blue-Green Algae (Cyanobacteria) Literature].
2
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CYANOBACTERIA AND THEIR TOXINS
Cyanobacteria (blue-green algae) toxins constitute the major source of natural product
toxins “biotoxins” found in surface supplies of freshwater. Species and strains in all of the
common planktonic cyanobactenal genera including Anabaena, Aphanizomenon, Microcystis,
Nodularia Nostoc and Oscillatoria produce biotoxins. Other genera including
Coelosphaerium, Cylindrospermopsis, Fischerella, Gloeotrichia, Gomphosphaeria,
Hapalosiphon, Microcoleus, Schizothth; Scytonem Spirulinq, Symploca Tolypothiix and
Trichodesmium have been reported toxic, but no toxin has been isolated and characterized
as yet from these genera (Scott 1991; Skulberg et al. in press).
These cyanotoxins produce intermittent but repeated cases of animal poisonings in many
areas of the world. Poisoning cases, known since the late 19th century, involve sickness and
death of livestock, pets and wildlife following ingestion of water containing toxic algae cells
or the toxin(s) released by the aging cells (Carmichael and Schwartz 1984; Beasley et al.
1989). No acute lethal poisoning of humans by freshwater cyanobacteria, such as occurs
with paralytic shellfish poisoning, has been confirmed. Humans are probably just as
susceptible as other mammals but people are repelled by the idea of consuming water
containing an algae bloom (Gorham and Carmichael 1988; Falconer 1989, 1991; Carmichael
and Falconer in press). Furthermore, there are no known food vectors, such as shellfish,
to concentrate toxins of freshwater cyanobacteria in the human food chain. However, the
decreasing water quality and increasing eutrophication of our freshwater supplies mean that
large growths or waterblooms of cyanobacteria are becoming more common. When tested,
these waterblooms are positive for the two main groups of cyanotoxins---the biotoxic alkaloid
neurotoxins and the cyclic peptide hepatotoxins.
Survey reports over the last few years indicate that a significant number of blooms are
toxic in any given area. In the U.S. many states have reported blooms of toxic
cyanobacteria. The only systematic survey study done to date in the U.S. is from Wisconsin.
That study reported about 40% of all cyanobacteria blooms tested were toxic during the
summer of 1987 (Repavich et a!. 1990). Reports from Scandinavia (Sivonen et al. 1990a)
and other areas of Europe (Skulberg et al. 1984; Pearson 1990) report a similar percentage
pattern. In some cases with small sample numbers, the percentage pattern of toxic blooms
has been much higher (Carmichael et al. 1988; Lanaras et al. 1989). Since waterblooms of
cyanobacteria commonly result from eutrophication processes, the toxic waterblooms will
likely increase in size and duration. It is possible that humans could become exposed to
levels of the toxins that can cause acute toxicity.
Neurotoxins
Neurotoxins are produced by species and strains of Anabaena (Carmichael et al. 1990),
Aphani.zomenon (Mahmood and Carmichael 1986a), Oscillatoria (Sivonen et al. 1989a;
Skulberg et al. 1992) and Trichodesmium (Hawser et al. 1991). Five chemically defined
3
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neurotoxins are now known from species within these genera. Anatoxin-a (antx-a) was the
first toxin from a freshwater cyanobacterium to be chemically and functionally defined. It
is the secondary amine, 2-acetyl-9-azabicyclo [ 4.2.1]non-2-ene (Huber 1972; Devlin et al.
1977), molecular weight 165 (M/Z) daltons (Figure 1). It has been synthesized by a number
of different methods (summarized in Carmichael et al. 1990). This alkaloid neurotoxin is
a potent postsynaptic cholinergic nicotinic agonist, which causes a depolarizing
neuromuscular blockade (Carmichael et al. 1975, 1979; Spivak et al. 1980, 1983; Aronstam
and Witkop 1981). Signs of toxicosis in field cases for wild and domestic animals include
staggering, muscle fasciculation, gasping, convulsions, and opistothonos (birds). Death is
probably due to respiratory arrest and occurs within minutes to a few hours depending on
species, dosage, and prior food consumption. The LD 50 intraperitoneal (i.p.) mouse for
purified toxin is about 200 g/kg body weight, with a survival time of minutes. While the oral
dose to produce acute lethality is much higher (hundreds of mg/kg body weight for the dry
weight cell material), the toxicity is still high enough that animals need to ingest only a few
milliliters to a few liters of the toxic surface waterbloom to receive a lethal bolus
(Carmichael and Gorham 1977; Carmichael et al. 1977; Carmichael and Biggs 1978).
No chemical antidote exists for antx-a intoxication. Artificial respiration has been used
in one instance with only partial success (Carmichael et a!. 1977). However, Beasley et al.
(1989) report a dose dependent reversal of antx-a toxicosis in laboratory rats using artificial
respiration. They suggest that animals given prolonged artificial respiration in addition to
lavage and instillation of activated charcoal should recover. Detection of antx-a is still
primarily by the mouse bioassay. There are some analytical methods, which developed as
methods of purification, were being used. These are based upon high performance liquid
chromatography (HPLC) (Astrachan and Archer 1981; Wong and Hindin 1982; Harada et
al. 1989), thin layer chromatography (Ojanpera 1991), gas chromatography-mass
spectrometry (GC-MS) (Smith and Lewis 1987; Himberg 1989), and gas chromatography-
electron capture detection (GC-ECD) (Stevens and Krieger 1988).
Most reports of antx-a occurrence are associated with Anabaena flos-aquae, A. spiroides
or A. circinalis. Recently Oscillatoria has been shown to produce antx-a (Sivonen et al.
1989a) and a strain of Oscillatoria rubescens has been shown to produce a methylene
homologue of antx-a termed homoanatoxin-a (Skulberg et al. 1992; Figure 2). This
homologue has a similar toxicity as antx-a.
Anatoxin-a is not the only neurotoxin to be produced by species and strains of
Anabaena. During screening of different Anabaena field samples Carmichael and Gorham
(1978) noted that some samples produced different signs of neurotoxicosis. in particular
some samples produced a marked salivation in laboratory mice. In order to differentiate
this from signs observed with antx-a the toxin was designated as anatoxin-a(s) [ s = salivation].
Antx-a(s) was subsequently shown to be a potent inhibitor of cholinesterase (Mahmood and
Carmichael 1986b, 1987). Structurally antx-a(s) is a unique N-hydroxyguanidine methyl
phosphate ester (m/z 252; C 7 H 17 N 4 0 4 P) (Matsunaga et al. 1989) (Figure 1). To date there
is no evidence which would indicate that strains of Anabaena produce both anatoxin-a and
4
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CH 3
10
anatoxin - a hydrochloride
(m/z 165)
C 10 H 15 N0
H 2 N
CH 3
N
CH 3
0
___ ,‘CH
O.d_ø• \ _0
anatoxin - a(s)
(m/z 252)
C 7 H 1 7 N 4 0 4 P
+ —
NH 2 CI
16
R = H; saxitoxin dihydrochioride
R = OH; neosaxitoxin dihydrochioride
Figure 1. Structure of anatoxin-a produced by species and/or strains of Anabaena fibs-
aquae, Aphanizomenon flos-aquae and Oscillatoria sp.; anatoxin-a(s) produced by
Anabaena flas-aquae, and saxitoxin, neosaxitoxin produced by Aphanizomenon flos-aquae
and certain marine microorganisms.
0
7
4
HN3
NH 2
+
0
21
20o
15
— +
CIH 2 N
H NH
NH
OH 18
OH
5
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B.
1I
aca
7! ø 91
I — I
BS tS
CH 2 CH 3
10 ii
122 .1%
I — — I - J
1*
1 (M+H)+
II
i71 182 19S 2
• • • 1
18S 2S
Figure 2. FAB.MS of niethylene (homo) anatoxin-a (A) produced by Osciflatoria
(Skulberg et al. 1992) and anatoxin-a (B).
A.
(M+H)+
4
0-
10
4
6
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a(s). Toxicosis associated with cholinesterase-inhibiting algae have been reported in dogs
and calves in South Dakota (Mahmood et al. 1988) and in pigs and ducks in Illinois (Cook
et al. 1989).
Clinical signs of toxicosis from laboratory experiments involving dosing of antx-a(s) have
been observed in ducks and pigs (Beasley et al. 1989). The LD 50 i.p. mouse for Antx-a(s)
is about 20 g/kg body weight or about ten times more lethally toxic than antx-a. At the
LD the survival time for mice is 10-30 minutes. Since antx-a(s) has the properties of an
organophosphorus insecticide, it should be possible to use therapy such as atropine to
antagonize its toxicosis. This has been partially successful (Mahmood and Carmichael
1986b; Beasley et al. 1989), but further studies are needed.
Kinetic studies comparing antx-a(s) with the organophosphate (OP) diisopropylfluoro-
phosphate (DFP) and studies looking at the nature of the interaction of antx-a(s) and
acetyicholinesterase have shown that antx-a(s) is an irreversible inhibitor of cholinesterase.
Comparing the bimolecular inhibition constants between antx-a(s) and the very potent
synthetic OP DFP, showed that antx-a(s) is about 22 times more potent than DFP
(Carmichael et al. 1990). This work plus that of Hyde and Carmichael (1991) suggests that
antx-a(s) uses the two-site attachment mechanism analogous to substrate and does not
inhibit acetyicholinesterase in the manner of the reversible anticholinesterases (Figures 3-4).
Aphanizomenon flos-aquae producing neurotoxins was first demonstrated by Sawyer et
al. (1968). These neurotoxins were later shown to be saxitoxin (STX) and neosaxitoxin
(NEOSTX) (LD i.p. mouse equals about 10 g/kg), the two primary toxins of red tide
paralytic shellfish poisoning (PSP) (Sasner et al. 1984; Mahmood and Carmichael 1986a).
Most work on STX and NEOSTX has been done using strains NH-i and NH-5 isolated by
Carmichael in 1980 from a small pond near Durham, New Hampshire (Carmichael 1982;
Ikawa et al. 1982). These toxins are fast acting neurotoxins that inhibit nerve conduction
by blocking sodium channels without affecting permeability to potassium, the
transmembrane resting potential, or membrane resistance (Adelman et a!. 1982). Mahmood
and Carmichael (i986a), using the NH-5 strain, showed that batch cultured cells have a
mouse i.p. LD of about 5 mg/kg. Each gram of lyophilized cells yielded about 1.3 mg of
neosaxitoxin and 0.1 mg of saxitoxin (Figure ic). Shimizu et a!. (1984) studied the
biosynthesis of the STX analog NEOSTX using Aph. flos-aquae NH-i. More recently
Sivonen et al. (1989a) has demonstrated antx-a production in a strain of Aph. flos-aquae.
Hepatotoxins
Acute hepatotoxicosis involving the hepatotoxins (liver toxins) is the most commonly
encountered toxicosis involving cyanobacteria. These toxins are produced by strains of
species within the genera Microcystis, Anabaena , Nodularia , Oscillatoria and Nostoc. In
addition, chemically undefined hepatotoxins are being studied in Cylindrosperinopsis,
Aphanizomenon, Gloeotrichia; and Coelosphaerium. Clinical signs of hepatotoxicosis have
been observed in field poisonings involving cattle, sheep, horses, pigs, ducks, and other wild
7
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Hydrolysis of Substrate by AChE
‘, ___
Anionic Hietidine Sertne
Subeft. EMer
Ac&yicho neeteraee Active Center
Acetyicholine
Enzyme.Substrat .
Tetrahedral Intermediate
Choline
CH OH
_____r13 . \ / 2
N CH 2
H 3 C CH 3
-e ‘
Acetyisted
Enzyme
c,,O
•H 2 0
Figure 3. Hydrolysis of. the substrate ac.tylcholin. by ac.tylcholin.steraae (AChE) in the
normal condition at nerve-muscle synapses.
Acetic Acid
0
HO —Ci’
Enzyme
-------
Hydrolysis of Anatoxin-a(s) by AChE
Anatoxln-a(s)
‘0 HC 2 HCT ’N(M.) 2 HO 0
N 0 P o - - - -,
20 _o,
-o
O&4.
NH 2 OMi NH 2 -
+
N_H _____ ____ ____ ____ ____
N: 0
V ’ V ) Y \ I ’
Enzyme InhIbitor Phosphorylated
Intermediate Enzyme
Figure 4 • A possible sah e for hydrolysis of anatoxin-a(e). Note dotted arrow indicates
slow dephosphorylation of tb. .nsym. l.ading to prolong.d (Jrr.v.rsibl.) inhibition of AChE
by anatoxin—a(e).
-------
and domestic animals. Most laboratory studies have involved the use of mice, rats, guinea
pigs, rabbits and pigs. Collectively, the signs of poisoning in these animals include weakness,
anorexia, pallor of mucous membranes, vomiting, cold extremities, and diarrhea. Death
occurs within a few hours to a few days after initial exposure and may be preceded by coma,
muscle tremors and forced expiration of air (Carmichael and Schwartz 1984; Beasley et al.
1989). Death most likely results from intrahepatic hemorrhage and hypovolemic shock
(Berg and Soli 1985 a,b; Theiss et a!. 1988). This conclusion is based on increases in liver
weight as a fraction of body weight (up to 100% in small animals tested in the laboratory)
as well as in hepatic hemoglobin and iron concentrations that account for blood loss
sufficient to induce irreversible shock. In animals that live longer, i.e., a few days, hepatic
insufficiency may develop to a degree that becomes incompatible with life (Jackson et al.
1984).
The mechanism of action for these hepatotoxins is the subject of current research in
several laboratories. Putting together certain aspects of this research it is possible to sketch
a sequence of events that could explain the hemorrhagic shock (based on a summary
described by Beasley et al. 1989). First, the toxin(s) are absorbed into the blood from the
ileum. Uptake in this area of the intestine may reflect the activity of abundant bile acid
carriers as conveyers of the peptide toxins across the mucosa (Dahiem et al. 1988). Second,
there is evidence that the toxin is transported preferentially into the hepatocytes (Runnegar
et al. 1981; Dabholkar and Carmichael 1987; Meriluoto et a!. 1990). The mechanism of
uptake into hepatocytes is believed to be via bile acid carrier salt transport (Runnegar et
al. 1981; Eriksson et a!. 1990). This transport mechanism has not been proven but evidence
is clear that the uptake is at least carrier mediated (Runnegar et al. 1991). Third,
hepatotoxin induced changes in the actin microfilaments, composing part of the cells
cytoskeleton, leads to a dense aggregation of the microfilaments near the center of the cell
(Runnegar and Falconer 1986; Eriksson et a!. 1989; Hooser et al. 1991). As a result of
these cytoskeletal changes there is a loss of cell-cell adhesion and the hepatocytes separate
leading to destruction of the sinusoid endothelial cells. Without intact liver sinusoids, lethal
intrahepatic hemorrhage (within hours) and/or hepatic insufficiency occurs within days.
Recent research is being directed toward the biochemical events leading to the
microfilament effects---these will be summarized once the structure of these hepatotoxins
has been presented.
Microcystins
The first report of these hepatotoxins being peptides was from Microcystis aeruginosa
strain NRC-i (ss-17) by Bishop et al. (1959). This toxin was later named microcystin
(MCYST) by Konst et al. (1965) and Carmichael et a!. (1988b). Subsequent isolations of
MCYST were made from the same strain (Murthy and Capindale 1970; Rabin and Darbre
1975) and from M. aeruginosa blooms in South Africa (Torrien. Scott and Pitout 1976) and
Australia (Elleman et al. 1978; Runnegar and Falconer 1981). Although the various extracts
had similar toxic properties, the hydrolysates of partially pure MCYST had substantially
different amino acid compositions which was later concluded to be due to the presence of
10
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different microcystins and to the varying degree of purity for the various extracts. Eloff,
Siegelman and Kycia (1982) were able to show that a single strain was capable of producing
more than one toxin, but it remained for Botes and his colleagues (Botes, Kruger and
Viljoen 1982; Botes et al. 1982a,b) and Santikarn et al. (1983) to provide us with the
structure of one of these toxins (designated as Microcystis toxin BE-4) produced by the
South African Microcystis aeruginosa strain WR7O (= UV-010). They concluded the toxin
to be a monocyclic peptide containing both D and L amino acids. Two of the D amino
acids were the novel N-methyldehydroalanine (Mdha) (which gives methylamine upon
hydrolysis) and a nonpolar side chain blocking group of 20 carbon atoms with a mass of 313
daltons termed ADDA (3-amino-9-methoxy-2,6,8-trimethyl- 10-phenyldeca-4,6-dienoic acid).
The two L amino acids were found to differ between the various toxins, and for the BE-4
toxin the L amino acids were leucine and alanine. Later Botes et al. (1985) reported the
structure of four other related toxins having L amino acid combinations of -LR (leucine-
arginine); -YR (tyrosine-arginine); -YA (tyrosine-alanine); and -YM (tyrosine-methionine).
The South African work was followed by Krishnamurthy et al. (1986, 1989) who found
the -LR toxin in a Norwegian waterbloom of M. aeruginosa and a Canadian Anabaena fibs-
aquae. They also found the -RR (arginine-arginine) toxin in a Norwegian laboratory culture
of Oscillatoria (Figures 5-6). The first definitive structure for MCYST-LR was by Rinehart
et al. (1988). This was followed by the work of Namikoshi et al. (1989) who published
results on the chemical synthesis of the ADDA component of microcystin. ADDA has been
shown to be the key structural component for biological activity. Ozonalysis of the double
bonds on ADDA yields free ADDA plus the corresponding cyclic peptide minus ADDA.
Mouse bioassay of these two structures shows that neither has toxicity in the mouse bioassay
(Dahlem 1989). Further structure/function work supports the importance of ADDA as the
key functional part of these cyclic peptides. During purification of microcystins using HPLC,
a small peak is often observed eluting close to the main toxin peak. When analyzed by
Harada et al. (1990a,b) this small peak was found to be a geometrical isomer of the parent
toxin. The isomerization was located at the C-8 position of ADDA. The toxins associated
with these minor peaks were MCYST-LR and RR. This isomer was found to be nontoxic
up to 1 mg/kg i.p. in the mouse bioassay.
Based on these beginnings our structural understanding for these microcystins has
progressed to the point where there are now about 23 known cyclic heptapeptide
microcystins plus nontoxic epimers of MCYST-LR and RR (Figures 5-7). These
microcystins differ in their L amino acid combinations, with MCYST-LR being most
common, and in being with or without methyl groups on amino acids 3, 5 and 7. These
microcystins’ toxicities do not vary greatly. All of the microcystins, except MCYST-RR and
the demethylated toxins D-Asp and Dha which have an LD 50 i.p. mouse of 200-250 pg/kg,
have an LD 50 i.p. mouse of about 60-70 g/kg with similar signs of poisoning. Some
biosynthesis work on MCYST-LR is now underway using M. aeruginosa strain PCC-7820.
These studies using C-13 precursors indicate that the carbon skeleton of ADDA arises from
condensation of phenylacetate with four acetates and C-i methylation of the polyketide
chain on C-2, C-6, and C-8. The work also shows that the Masp unit (Figure 6; amino acid
ii
-------
MCYST -
MCVST-
MCYST- IR:
MCYST- FR:
MCVST- AR:
MCYST- YM:
MCYST- RR:
MCYST- RR:
MCVST- RR:
MCVST - YR:
MCYST- HtyrR:
MCYST- HtyrR:
MCYST - WR:
H
MCYST - VA: X - Tyr; R 1 - CH 3 ;
X.Leu;R 1 —CH 3 ;
XsPhe;R 1 CH 3 ;
X.Ala;R 1 -CH 3 :
X.TyrR 1 .CH 3 ;
X-Arq;R 1 ‘iCIj ;
X • Arg; R’ - H;
XaArg:R’ -H;
X.TyrR 1 -CH 3 ;
X.HtyrR 1 aCH 3 .
X-HtyrR 1 .H;
X .Trp; R 1 . CH 3 ;
©
A 2
Y AIa; R 2 -CH 3
Y -Arg:R 2 -CH 3
Y Arg;R 2 -CH 3
Yi.Arg;R 2 . CH 3
V a. Met; R 2 i t CH 3
Y*Arg; R 2 . CH 3
Y.Arg; R 2 - CH 3
Ya.Arg;R 2 . H
YaArg; R 2 - CH 3
Y.Arg: R 2 . CH 3
YzArg; R 2 -CH 3
Y -Arg;R 2 .CH 3
Figure 5. Structures of known microcystins excluding analogues of MCYST-LR.
MCYST-FR (phenylalanine-arginine); AR (alanine-arginine); M(O)R (methionine
sulfoxide-arginine) and WR (tryptophan-arginine) are new toxins from Microcystis
isolated by Namikoshi et al. (1992).
17
13
12
10
Microcystin
(MCYST)
COOH
( ) M W .
LA: X-Leu;R’ CH 3 ; Y*AIa;R 2 -CH 3 909
M(O)R: X — Met(O); R 1 — CH 3 ;Y a Arg; R 2 . CH 3 1028
(D-Asp 3 J
(O-Asp ,Dha 7 )
(D Asp 3 )
959
994
1028
952
1018
1037
1023
1009
1044
1055
1044
1067
12
-------
®14
Microcystin. LR
and analogues
M.W .
MCVST - LR:R 1 = CH 3 R - CH 3 ; A 3 - CH 3 ; n -3 994
[ ADMAdda 5 j.MCYST-LRR _ 2 & 3 H 3 ;R2_cH 3 ;R3_CH 3 ;n_3 1022
[ ADMAdda 5 JMCYST-LHarg:R 1 .COCH 3 ;R 2 -CH 3 ;R 3 -CH 3 ;n -4 1036
[ D-Asp 3 ADMMda 5 J - MCYST -LR:R 1 - COCH , - H; A 3 - CH n 3 1008
(D-Asp ADMMda 5 J - MCYST- LHarg: A 1 =COcH 3 ; - R 2 -H; R 3 -CH n 4 1022
(D-Asp 3 ) - MCYST - LR:R 1 CH3; A 2 - H; A 3 - CH n -4 980
(DMMda 5 J- MCYST - Lft R 1 - H; R 2 - CH 3 ; A 3 - CH 3 ;n -3
[ Dha 7 ]- MCYST- LR: R 1 CH 3 ; R 2 - CH 3 ; R 3 . H; n 4 980
[ Mser 7 J - MCYST- LR:R — CH 3 ; R 2 .CH 3 ;7 -N.methyl$erlne;n.3 1012
Figure 6. Structure of microcystin-LR and its analogues. The last three toxins on this
list represent new toxins isolated from Mic.rocyslis by Namikoshi et al. (1992).
©
1
17
11
H 3 C
H
H
12
0
H
I
13
-------
0
NH
4
Structure of (1) Microcystin
component of Microcystin -
- LR; (2) Microcystin - AR; (3) nontoxic minor
LA; (4) nontoxic minor component of Microcystin - AR.
Figure 7. Structur. of microcystin-LR and RR plus nontoxic geometrical isomer minor peaks
isolated from Microcystis (Harada at al. 1990a,b).
N 3 C
N 1 N
1
I-
3
NH
N
N
14
-------
number 3) is formed from acetate and pyruvate via a pathway similar to the biosynthesis of
leucine (Moore et a!. 1991).
Nodularin
The biggest structure variation for these peptide hepatotoxins has been found in the
filamentous brackish water cyanobacterium Nodularia spumigena. Earlier reports indicated
that Nodularia could produce a hepatotoxin (Francis 1878; Main et al. 1977; Lindstrom 1976;
Edler et al. 1985; Perrson et al. 1984; Eriksson et a!. 1988; Runnegar et al. 1988).
Carmichael et aL (1988c), Rinehart et al. (1988), and Sivonen et al. (1989b) established the
structure for the Nodularia peptide as a cyclic pentapeptide M/Z 824 daltons and termed
it nodularin (NODLN) (Figure 8). The sources and types of cyclic peptide toxins produced
by the various cyanobacteria are listed in Figure 9.
Occurrence of Toxic Cyanobacteria
Since the first report of toxic cyanobacteria in the late 19th century (Francis 1878)
studies in several countries have revealed the wide occurrence of toxic cyanobacteria
waterblooms. All continents except Antarctica have reported toxic blooms. In the United
States 27 States have reported the presence of toxic cyanobacteria waterblooms, and many
of these have documented animal losses (Table 1). In Europe 16 countries have reported
toxic cyanobacteria blooms. Although not all of these countries have documented cases of
animal, fish or bird poisonings from the waterblooms, the positive laboratory toxicity tests
done on waterbloom samples clearly show that the incidence of toxic cyanobacteria is much
wider than would be inferred from suspected poisoning incidents. In addition, many of the
early toxicosis caused by cyanobacteria waterblooms are difficult to place into any category,
since specific toxic signs were not described at that time. It is also possible that other types
of toxins were produced in these cases from the cyanobacteria present or the coexisting
phytoplankton and bacteria. At present, in all toxicosis cases associated with freshwater
phytoplankton, cyanobacteria have been the toxic agent involved. It should be emphasized
that toxin forming cyanobacteria are all naturally occurring members of freshwater
phytoplankton. The secondary metabolites they produce that are biotoxic can be compared
with other natural product toxins. All these natural toxins show a range of toxicities
depending on the toxin ‘ s potency, the test animal used and the experimental conditions.
All the known cyanobacteria toxins are rated as supertoxic when compared against the
standard rating table of toxic substances (Table 2). When compared against other biotoxins
the cyanotoxins rank more toxic than plant, fungal or some marine phycotoxins toxins and
somewhat less toxic than most bacterial and some other marine phycotoxins (Table 3).
The numerous cases of animal poisonings that have been reported in the literature have
been summarized at various times over the years (Schwimmer and Schwimmer 1964, 1967;
Carmichael et al. 1985; Sivonen 1990). An updated version of these summaries is given in
Table 4. A summary of cases the author has investigated over the past 14 years is given in
15
-------
CH 3
H
Figur. 8. Structur. of nodularin produced by the brackish water fi1a antous cyanobact.riu*
Nodularia spumigena.
0
H
COOH
H
CH
I
0’
Nodularln-M.W. 824
Nodularla pumIg
NH
MN NH 2
-------
SOURCES OF MICROCYST1N AND NODULARIN
Organism Type of Microcystin
Microcystis aeruginosa MCY$T-LR . LA, YR. FR, YM, PR, LAba,
AR. E,DMAddOIMCY$T-LR,
[ Dha ]MCYST-LR, MCYST-M(O)R
Microcystis viridis MCYST-RR, IR, YR, LA
Microcystis wesenbergil MCYST- PR, IR
(based upon mixed waterbloom
samples)
Osciliatorla agardhtl MCYST-RR
var. lsothrlx [ D-Aspl-MCYST-RR
[ D-Asp 1-MCYST-RR
Oscillatorla agardhii MCYST-RR
var. (red pigmented) [ D-Asp’]-MCYST-RR
Anabaena flos-aguae MCY$T-LR
ED-Aspi- MCYST-LR
M CYST- HtyrR
[ D-Aspi-MCYST-HtyrR
Nostoc sp. [ ADMAddaI-MCYST-LR
[ ADMAdda -MCY$T-LHarg
(D-Asp 3 1 ADMAdda -MCYST.LR
[ D- Asp 3 ,ADMAdda - MCYST- LHarg
Aphanizomenon and Coeiosphaerium are reported to
produce peptide hepatotoxins but specific ones have not
been isolated.
Nodutaria spumigena Nodularin
Figure 9. Sources of microcystin (MCYST) and nod ularin (NODLN). Nostoc toxins are
reported by Sivonen et al. (1990b) and Namikoshi et al. (1990).
17
-------
Table 2. Toxicity rating chart. 1
Toxicity rating or class
Probable lethal or
a! dose for humans
Dosage 2
For Average Adult
1. Practically nontoxic
> 15 g/kg
More than 1 quart
2. Slightly toxic
5-15 g/kg
Between pint and quart
3. Moderately toxic
0.5-5 g/kg
Between ounce and pint
4. Very toxic
50-500 mg/kg
Between teaspoonful and ounce
5. Extremely toxic
5-50 mg/kg
Between 7 drops and teaspoonful
6. Supertoxic
<5 mg/kg
A taste (less than 7 drops)
Casarett and Doull’s - Toxicology The basic science of poisons. Third Edition. Macmillan
Publishing Co. New York. 1986. p. 13.
2 See Table 3.
18
-------
Table 3. Comparison of toxicities of some biological toxins.
Toxin Source Common Name Lethal Dose 1
(LD 50 )
BOTULINUM TOXIN-a Clostridium botulinum (BACTERIUM) 0.00003
TETANUS TOXIN Clostridium tetani (BACTERIUM) 0.0001
RICIN Ricinus communis (CASTOR BEAN PLANT) 0.02
DIPHTHERIA TOXIN Corynebact.rium diphtheriae (BACTERIUM) 0.3
KOKOI TOXIN Phyllobates bicolor (POISON ARROW FROG) 2.7
TETRODOTOXIN Arothron meleagris (PUFFER FISH) 8
SAXITOXIN Aphanizomenon flos-aquae and (BLUE-GREEN ALGAE) 9
Alexandrium sp. (DINOFLAGELLATE ALGAE)
COBRA TOXIN Naja naja (COBRA SNAKE) 20
NODULARIN Nodularia spumigena (BLUE-GREEN ALGAE) 50
MICROCYSTIN-LR Kicrocystin aeruginosa (BLUE-GREEN ALGAE) 50
‘.0 ANATOXIN-a Anabaena flos-aquae (BLUE-GREEN ALGAE) 200
ANATOXIN-a(s) A.nabaena floe—aquas (BLUE-GREEN ALGAE) 20
CURARE Chondrodendron tomentosum (BRAZILIAN POISON ARROW PLANT) 500
STRYCHNINE Strychnos nux-vomica (PLANT) 2000
AMATOXIN Amanita p. (FUNGUS) 200—500
MUSCARIN Amanita muscaria (FUNGUS) 1100
PRALLOTOXIN Anianita ep. (FUNGUS) 15002000
SODIUM CYANIDE 10000
The acute LD 50 in ig per kg bodyweight: intra-peritoneal injection: some with mice, some with rats
-------
Table 4. Cases of animal poisonings (actual or suspected) caused by mass occurrenors of cyanobacteria.
Year Location Affected animals Symptoms and findings Organism Reference
1878
1882-
1884
1900
1917-
1918
1918
Q
1928
1930
1933
1933
Hogs, horses, cattle,
poultry, wild birds
I Sheep, 17 hogs and
about 50 chickens
About 20 cattle
About 40 cattle
9 cattle
More than 21 sheep and
chickens
45 turkeys, 4 ducks and
2 geese, 6 days later cows
pigs, horses and poultry
3 cattle
Number of cats
4 ducks, wild birds, carps,
snakes, salamanders, a calf
Hurried respiration,
staggering gait, rigors
No pathological findings
No description
Rapid death (15 mm or more)
Death after one and half h,
no findings in autopsy
Rapid death (minutes with
gwnea-pigs) no gross
pathological findings
Rapid death (few minutes)
Rapid death, prostration
convulsions
Paralysis of hind limbe,
degeneration of liver
Rapid death (minutes)
no lesions
Aphanizomenon flos.aquae
“Blue-green algae”
C k pk kuetzingianum
Ana6wia Jk -aquae
Anatraena
Anatiaena !emmermannii
Micrrxystis flc -aquae
Microcystis aeruginosa
Micncystis fli:s-aquae
Micmcystis fl -aquae
Anabaena flcs-aquae
Aphanizomenon fios -aquae
Micrucystis flcs-aqzsae
Anabaena flos-aquae
Blue-green algal bloom
Anabaena flos-aquae
Francis, 1878
Porter; Arthur,
Stalker ref. in
Fitch et aL, 1934
Nelson, ref. in
Fitch et al., 1934;
Olson, 1960
Gillman, 1925
Fitch et al., 1934
Howard and Berry,
1933
Hindersson, 1933
Fitch et al., 1934
Fitch et al., 1934
Fttch et al., 1934
Fitch et al., 1934
Vinberg, 1954
Deem and Thorp,
1939
Sheep, horses, dogs, pigs
Cattle, horses, hogs
Sevei l cattle
Stupor, unconsciousness,
Rapid death (30 mm or
more)
No description
Nodularia spumigena
Glorotrichia &iinulata
L. Alexandnna;
Australia
Minnesota; USA
Minnesota; USA
Alberta; Canada
Minnesota; USA
Ontaria; Canada
L. Vesijârvi; Finland
Minnesota; USA
Minnesota; USA
Minnesota; USA
Minnesota; USA
L. Juksa; USSR
Colorado; USA
1933
1934
1939
-------
Affected animals
Thousands of cattle, sheep
and other animals
Sheep
37 hogs, 4 sheep, 2 cattle,
3 horses and several dogs,
cats, squirrels, chickens,
turkeys and songbirds
A horse, several calves
two pigs and a cat
Cattle and deer
Cattle deaths
Few dogs
Horses, a dog and wild birds
Cattle deaths
A a)w, horses, pies, dogs,
turkeys, geese, chickens
and wildbirds
Heavy mortality of wild
ducks
A horse, 9 dogs
Symptoms and findings
Liver damage,
photosensitivity
Death after few hours
Rapid death (4-12 mm
mice and guinea pigs)
Muscular weakness
paralysis
Hepatotoxicity +
photosensitivity
No descnption
Distress, a)nvulsions
paralysis (death after
I h 40 mm, rabbit, oral)
Typical algae poisoning
Rapid death (minutes)
Partial paralysis,
Liver mottled
Rapid death (45 mm)
Muscular weakness paralysis,
death within one hour
“Water bloom”
“Water bloom”
Aphanizomenon flos-aquae
Anabaena fl -aquae
Microcystis aeruginosa
Microcystis aeruginosa
Anahaena Spp.
Microcystis
Aphanizonzenon flos-aquae
Microcystis aeruginosa
Aph. flos-aquae (99%)
A. flos-aquae (0.9%)
M. aeruginosa (0.1%)
Table 4. (oontinued)
Year
Location
1913-
1943
Free State and
Transvall; S. Africa
1943
Montana; USA
1944-
1945
Iowa; USA
1945
Manitoba; Canada
1946
North Dakota; USA
rs
—
1945
1948
Bermuda
Iowa; USA
Organism
Microcystis to.xica
(= M. aeruginosa)
Algae
AnoJxzaa flos-aquae
1948
1948-
1949
1950
1949-
1951
1951
Minnesota; USA
Ontario; Canada
Alberta; Canada
Manitoba; Canada
Manitoba; Canada
Reference
Steyn, 1943, 1945
Quin, 1943
Rose, 1953
McLeod and
Bondar, 1952
Brandenburg and
Shigley, I94’
Prescott, 1948
Rose, 1953
Olson, ref. in
Scott, 1952
Stewart et al., 1950
MacKinnon , 1950
O’Donoghue and
Wilton, 1951
Bossenmeyer et al.,
1954
McLeod & Bondar,
1952
-------
Table 4. (Continued)
Year Location Affected animals Symptoms and findings Organism Reference
1952 Iowa; USA Thousands of Frankling’s Rapid death (minutes) Anabaena flc -aquae Firkins, 1953;
culls , 560 ducks, 400 coots . Rose, 1953
00 pheasants, 50 fox
squiriels 18 muskrats, 15
dogs, 4 cats, 2 hogs, 2 hawks,
1 kunk and 1 mink
1953 L. Semehovichi; USSR Deaths of cata dogs and No description Microcystis aeruginosa Vinberg, 1954
water fowl
1954 Saskatchewan; Canada Pigs died, cattle unaffected No description AnaL*ww flos -aquae Hammer, 1968
1956- Texas; USA Fish, frogs , chickens, ducks, Death within 2 h Nosfoc rivulare Davidson, 1959
turkey and cattle died or enlarged liver (mice i.p.)
became ill
,.. 1959 Alberta; Canada 14 beef cattle Enlarged liver “Blue-green algae” MacDonald, 1960
1959 Saskatchewan; Canada Apprc c. 30 dogs, I goose Gastroententis with bowel M. aeruginosa/flos-aquae Senior, 1960;
horses and cattle haemorrhage, livers A. floc dqiW2 Dillenberg and
engorged and mottled Aphanizomenon Dehnel, 1960
1961 Saskatchewan; Canada 3 different lakes; 20 dogs; Mouse tests showed neum- Anabaena flos -aquae Hammer, 1968
3 cattle, perch; wild ducks toxicity in case of two lakes
1962 Alberta; Canada I horse, 8 a ws died, No description “Blue-green algae” O’Donoghue, ref.
60 wws were sick in Gorham, 1964a
1962 Saskatchewan; Canada 3 dogs No description “Algae” Hammer, 1968
1963 Rügen; GDR About 400 ducks Liver damage Nodularia spumigena Kalbe and Teiss,
1964
1964 Saskatchewan; Canada 5 dogs Haemorrhagic enteritis Analiaena flc6 -aquae Hammer, 1968
1964 Saskatchewan; Canada 20 calves siclc I died Haemorrhagic enteritis AnaLv ena, Aphanizomenon Hammer, 1968
Nodularia
1964 New Hampshire; USA Tons of fish died after No description Aphanizomenon flos-aquae Sawyer et al., 1968
CuSO 4 treatment
-------
Table 4. (Continued)
Year Location Affected animals Symptoms and findings Organism Reference
1965 New South Wales; 20 lambs Hepatocellular necrc is Anacystis cyanea McBarron & May,
Australia (= M. aerugin a) 1966
1965 Saskatchewan; Canada 17 cattle No description Anabaena flc -aquae Hammer, 1968
Aphanizomenon and
Microcystis aeruginosa
1966 New South Wales; 16 sheep died and 50 Enlarged liver Anacystis cyanea McBarmn & May,
Australia wete sick (= M. aerugincsa) 1966
Waipukurau; Lambs Engorged, friable liver Microcystis aeruginosa Flint, 1966
New Zealand haemorrhagic enteritis
1966 Saskatchewan; Canada 2 calves and 1 dog Mouse test showed Analiaena flos-aquae Hammer, 1968
neurotoxicity
1967 Saskatchewan; Canada 25 pigs Vomiting, convulsions Anatraena Hammer, 1968
1971 New South Wales; Deaths of honey bees Rapid death (minutes Anatuena circinalis May & McBarron
with mice i.p.) 1973
1972 Alberta; Canada 3 calves Rapid death (8-15 mm, Anabiena flos-aquae Carmichael et al.,
mouse, i.p.) 1977; Carmichael
and Gorham, 1978
1972 Alberta; Canada 12-15 cattle Hypersensitive to noise, Anabaena flos-aquae Carmichael et al.,
staggering, weak, convulsions 1977; Carmichael
and Gorham, 1978
1973- Hartbeespoort Dam; Cattle deaths Microcystin poisoning Microcystis aeruginosa Toerien. et al., 1976
1974 S. Africa
1974- South Western and 34 sheep, 52 lambs Hepatic necrc is Nodularia spumigena Main et al., 1977
1975 Western Australia
1975 New South Wales; 20 lambs Trembling, salivation, stag. Anabaena circinalis McBarmn et al.,
Australia gering leg weakness, collapse 1975
(liver changes with chickens,
oral adm.)
-------
Table 4. (Continued)
Year Location Affected animals Symptoms and findings Organism Reference
1975 Saskatchewan; 34 cattle Staggering, convulsions M. aeruginosa (95%) Carmichael et at.,
Canada A. flos-aquae (5%) 1977; Carmichael
and Corham, 1978
1975 Danish Coast of 30 dogs were sick, 20 died Hepatic necrosis Nodularia spumigena Lindstrøm, 1976
the Baltic Sea
1976 Washington; USA 4 dogs died, 7 dogs, one Prostration, convulsion, Analiaena flos.aquae Soltero and
horse and one cow were sick respiratory failure (mice) Nichols, 1981
1977 Montana; USA 8 dogs and 30 cattle Anatoxin-a poisoning Anabaena Jkrs-aquae Juday et al., 1981
1977 Oklahoma; USA Several cattle Nausea, abdominal pain, Micracysiis sp. Zin and Edwards,
diarrhea, muscular tremors, 1979
dyspnea, convulsions, death
1978 Rogaland; Noiway 4 heifers Micmcystin poisoning Mici xysIis aeruginosa Skulberg, 1979
1978 Cheshire England 3 cows Acute haemorrhagic enteritis Oscillatoria a,gardhii Reynolds, 1980
1979 South Africa 3 rhInoceroses Necrosis of the liver Microcystis aeruginosa SoIl and Williams,
1985
1980 Vaal Dam; S. Africa Cattle Microcystis poisoning Micmcystis aeruginosa Scott et a!, 1981
1981 illinois; USA 10 sows Trembling, violent shaking. Anabaena spiroid Beasley et al., 1983
death with one-half hour
1982 Swedish Coast of 9 dogs Hepatic necrosis Nodularia spumigena Lind et al., 1983;
the Baltic Sea Lundberg et al.,
1983; Edrer et at.,
1985
1983 German Coast of 16 young cattle Death 6-18 h, convulsions, Nodularia spumigena Gussmann et at.,
the Baltic Sea haemorrhage in the cardiac 1985
region
1984 Finnish Coast of I dog and 3 puppies Vomiting. weakness, Nodularia spumige’na Persson et a!, 1984
the Baltic Sea liver damage
-------
Affected animals
11 cattle
Appr. 1000 t ts, 24 mallards
and American wigeons
9 cows died, 11 were sick
9 dogs
Number of fish, birds
and muskrat deaths
16 WS
5 ducks; 13 pigs died
5 cows were sick
4 cows, 6 calves, 18 pigs
and 7 ducks died
Deaths of 20 sheep
and 14 dogs
Symptoms and findings
Rapid occurren of death
Anatoxin-a shown in the
green slime from carcasses
Hepatotoxicosis
Anatoxin-a(s) poisoning
Liver fibrosis and gill
damage (fish)
Anatoxin-a poisoning
(possibly other amines present)
Anatoxin-a(s) poisoning
Staggering, salivation, muscle
tremoN, bloody diarrhea
Heapto- and neurotoxicosis
Microcystin-LR poisoning
Organism
Analtaena flos-aquae
Micracystis atruginosa
Aphanzzomenon flos-aquae
Anafraena flos-aqua€
Microcystis aeruginosa
Anatxaena flos-aquae
Oscillatoria a ardhii
Not indicated
Anabaena flcs-aquae
Microcystis aeruginosa
Microcystis aeruginosa
Anatiaena flos.aquae
Microcystis aeruginosa
Reference
Spoerk2 and
Rumack, 1985
Pybus et al., 1986
Galey et al., 1987
Mahmood et al.,
1988
Eriksson et al.,
1989
Smith & Lewis,
1987
Cook et al., 1989
Kerr et al., 1987
Short & Edwards,
1990
Report of The
Nati. River
Authorities
United Kingdom -
1990
Yong, et al., 1989
Carmichael, 1991
Table 4.
Year
1984
1985
1985
1985
1985
1986?
(1
1986
1987
1988
1989
(Continued)
Location
Montana; USA
Alberta; Canada
Wisconsin; USA
South Dakota; USA
Aland, Finland
Alberta; Canada
Illinois; USA
Mississippi; USA
Oklahoma; USA
Rutland Water
United Kingdom
1989 Saskatchewan; 16 cattle died Neurotoxicosis
Canada
1990 Indiana; USA 2 dogs died Anatoxin-a poisoning
* Updated from Sivonen, K. (1990) Ph.D. Thesis; University of Helsinki, Finland.
AnaL*zena sp.
Anabaena flos.aquae
-------
Table 5. Systematic surveys of the incidence of toxic waterblooms for a given geographic
area has not been a regular part of the documentation for toxic cyanobacteria. It is difficult,
and for the most part impractical, to sample all the water bodies in a geographical area for
the presence of toxic cyanobacteria. Where systematic studies have been done, the percent
incidence of waterbloom toxicity (number of sites with toxic waterblooms/number of sites
with waterblooms sampled) has ranged from about 50-100. Areas where these studies have
been conducted include: Minnesota (Olson 1960), Wisconsin (Repavich 1990), Alberta,
Canada (Gorham 1962), Saskatchewan, Canada (Hammer 1968), Japan (Watanabe and
Oishi 1980; Watanabe et al. 1988), German Democratic Republic (Henning and Kohl 1981),
Netherlands (Leeuwangh et al. 1983), United Kingdom (Richard et al. 1983; Pearson 1990),
Scandinavia (Berg et al. 1986), Sweden (Mattsson and Willén 1985), P.R. China (Carmichael
et al. 1988), Greece (Lanaras et al. 1989), Finland (Sivonen et al. 1989, 1990a).
In assigning toxicity to a waterbloom which is a mixture of more than one cyanobacterial
species or genus, it is often necessary to look at the level of toxicity in a chemical or
biological assay and assign the toxic species responsible based on its dominance in the
waterbloom sample. For example, if a waterbloom sample containing predominantly
Micro cystis aeruginosa has an LD 50 intraperitoneal mouse of about 50 mg/kg with
hepatotoxic signs of poisoning, it can be concluded that M. aeruginosa is most likely the toxic
organism involved. If a waterbloom sample with an approximately 1:1 ratio of Anabaena
flos-aquae and Microcystis aeruginosa has an LD 50 intraperitoneal mouse of 100-200 mg/kg
with neurotoxic signs of poisoning, it can be concluded that Anabaena is responsible for the
toxicity observed, and the Microcystis component is not contributing to the toxicity observed.
Not all cyanobacteria suspected of being toxic have been isolated and grown in the
laboratory. Only species and strains within the genera Anabaena; Aphanizomenon,
Microcystis, Nodularia Nostoc and Oscillatoria have had toxins chemically identified. Work
in this area is continuing in several laboratories around the world most notably in the
United States. Based on the Report of the National Rivers Authority - United Kingdom
(Pearson 1990), the cyanobacteria species listed in Table 6 are the confirmed toxic
cyanobacteria species known.
FORMATION OF CYANOBACTERIA WATERBLOOMS AND SURFACE SCUMS
Multiple interacting physical, chemical, and biotic factors lead to the formation of
cyanobacteria waterblooms (defined as the visible coloration of a water body due to the
presence of suspended cells, filaments and/or colonies) and in some cases subsequent
surface scums (surface accumulations of cells resembling clotted mats or paint-like slicks).
Planktonic cyanobacteria are a natural component of the phytoplankton in most surface
waters of the world. In northern latitudes like N. America and Europe waters supporting
cyanobacteria growth have a sequence of algal dominance, generally being diatoms in the
spring, then green algae followed by cyanobacteria in the summer and often into the
autumn. It is generally agreed among aquatic microbiologists and limnologists who study
waterbloom formation that 1) nutrient loading, 2) retention time of water within the water
body, 3) stratification, and 4) temperature are the main factors influencing bloom formation
and intensity.
Cyanobacteria owe their name of blue-green algae to the presence of accessary
26
-------
Table 5. Case report: toxic cyanobacteria (blue-green algae)*
DATE
LOCATION
CYANOBACItRIA
TOXIN
COMMENTS
REFERENCES
Hearid-Press of
Huntington,
Indiana - Sept. 30
and Oct. 1, 1990
Summer 1990
Pond near
Huntington, indiana
Anabaena (los-
aquae
anatoxin-A
Neurotoxic poisoning of
2 family dogs
Summer 1990
Clear Lake,
California
Microcystis
aeruginosa
microcystin
Toxicity based on
bloom samples and
drinking water
samples. Assayed
using ELISA
antibody
California Dept.
of Health,
Sacramento
Summer
1989-90
Dahli Lake, near
Manjouli, Inner
Mongolia, P.R.
China
Microcystis
hepatotoxin
Hepatotoxic poisoning
of over 60 cattle -
waterbloom not
bioassayed
Personal
Communication,
Baolin Li, Director,
Dahli Lake Fisheries
Science Center
(August 1991)
December 1989
American Lake near
Tacoma, WA
Anabaena circinalas
anatoxin-A
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intrapentoneal mouse =
25mg/kg
Tacoma-Pierce Co.
Health Department,
Tacoma, WA
September 1989
McDonald Lake,
Colville Indian
Reservation,
Washington
Microcystis sp. and
Aphanizomenon
microcystins
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 200 mg/kg
College of Pharmacy,
Washington Stale
University, Pullman
flos-aguae
Duley Lake, Colville
Indian Reservation,
Washington
Microcystis
aeruginosa
m icrocystins
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 75 mg/kg
College of Pharmacy,
Washington State
University, Pullman
September 1989
-------
Table 5. (Continued)
DATE
LOCATION
CYANOBACTERIA
TOXIN
COMMENTS
REFERENCES
August 1989
Ft. Peck Lake,
Montana
Anabaena sp.
microcystins
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperitoneal mouse =
approx. 100 mg/kg
U.S. Army Corps of
Engineers, Omaha
District, Omaha, NE
June-Oct. 1989
Lake Okeechobee,
Florida
Mixture of
Anabaena sp. and
Microcystis sp.
not identified
No hepatotoxins or
neutotoxins - signs
of poisoning
indicated a contact
irritant
South Florida
Water Management,
W. Palm Beach
October 1988
Charlie Lake,
British Columbia
Microcystis
aeruginosa
not identified
No hepatotoxins or
neurotoxins
signs of poisoning
indicate contact
irritant
Prov. of British
Columbia;
Ministry of
Environment -
Water Management
September 1988
Lake Istokpoga,
Florida
Microcystis
aeruginosa and
Anabaena sp.
unidentified
neurotoxin
Signs of poisoning
in lab mice indicated a
neurotoxin. LDSO
intraperitoneal mouse =
approx. 300 mg/kg
body weight
South Florida
Water Management,
W. Palm Beach
August 1987
Lake Okeechobee,
Florida
Microcysti
aeruginosa and
Anabaena circinalis
microcystins
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 100 mg/kg
body weight
South Florida
Water Management,
W. Palm Beach
July 1987
Superior, Nebraska
Anabaena
flos-aguae
anatoxin-A(s)
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperitoneal mouse =
approx. 50 mg/kg
Animal Hospital,
Superior, Nebraska
-------
Table 5. (Continued)
r..
0
DATE
LOCATION
CYANOBACrERIA
TOXIN
COMMENTS
REFERENCES
September 1986
Farm Pond near
Griggsville, IL
Anabaei ,
fIos-agua .
anatoxin-A(s)
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperitoneal
mouse = approx.
50 mg/kg
Univ. 1 Illinois,
College of Vet.
Medicine, Urbana, II.
Cook, W.O. et al.
1989. Envir. lox.
Chem. 8: 915-922
August 1986
Farm Pond near
Tolono, IL
Anabaena
flos-aguae
anatoxin-A(s)
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperitoneal
mouse = approx.
50 mg/kg
Univ. of Illinois,
College of Vet.
Medicine, Urbana, IL
Cook, W.O. et al.
1989. Envir. lox.
Chem. 8: 915-922
October 1985
Lake Sissobogoma
near Stone Lake, WI
Microcystis sp. and
Anabaena sp.
hepatotoxin
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intraperitoneat mouse =
100 mg/kg
Cottage owner, Lake
Sissobogoma, WI
September 1985
Farm Pond near
Monroe, WI
Microcystis
aeruginosa
microcystins
Signs of poisoning in
lab mice and an Angus
heifer indicated a
hepatotoxin. LD5O
intraperitoneal mouse =
10 mg/kg
F.D. Galey ci al,
J. of Vet. Res.
48(9): 1415-1420,
1987
September 1985
Lake Sak.akawea,
North Dakota
Microcystis
aeruginosa plus
Aphanizomenon
microcystins
Signs of poisoning
in lab mice indicated a
neurotoxin and a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 100 mg/kg
U.S. Army Corps of
Engineers, Lake
Sakakawea Office,
Riverdale, ND
flos-aguae
-------
Table 5. (Continued)
DATE
LOCATION
CYANOBACTERIA
TOXIN
COMMENTS
REFERENCES
August 1984
Canyon Ferry
Reservoir, Montana
Aphanizomenon
unidentified
neurotoxin
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperiloneal mouse =
approx. 100 mg/kg
Montana Dipt. of
Health
Environmental
Sciences
flos-aguae..
Anabaenp fibs-
aguae. and
Microcystis
aeruginosa
August 1983
Lake Erie at
Toledo, Ohio
Microcystis
aeniginosa
microcystins
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 50 mg/kg
Univ. of Toledo,
Dept. of Biology,
Toledo, Ohio
September 1981
Pine Creek near
Pinedale, WY
Anabaena sp. and
Microcystis sp
neurotoxin
Field reports of dog
poisoning indicated a
neurotoxin. L050
intraperitoneat mouse
not determined
Vet. Services,
Pinedale, WY
Bioresources Center
Desert Research
Institute, Reno,
Nevada
September 1981
Lake Lahonton,
Nevada
Apharüzomenon
microcystins
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperitoneal mouse =
approx. 180 mg/kg
flos-aguae
September 1981
Homer Lake near
Urbana, IL
Microcystis
aeruginosa
microcystins
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intrapentoneal mouse =
approx. 50 mg/kg
Univ. of Illinois
College of Vet.
Medicine, Urbana, If.
July 1981
.
Harvey’s Lake near
Wilkesbarre, PA
Anabaenasp.
neurotoxin and
hepatotoxin
Signs of poisoning in
lab mice indicated a
neurotoxin and a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 100 mg/kg
Bureau of Water
Quality
Management,
Wilkesbarre, PA
-------
Table 5. (Continued)
(A
DATE
LOCATION
CYANOBACTERIA
TOXIN
COMMENTS
REFERENCES
August 1980
Moore’s Pond,
Durham, NH
Aphanizomenon
saxitoxin and
neosaxitoxin
Signs of poisoning
similar to paralytic
shellfish poisoning.
LD5O intraperitoneal
mouse = approx.
30 mg/kg
Dept. of Zoology.
Univ. of New
[ lamps hire,
Durham, Nil
flos-aguae
.
July 1980
Pocono Highlands
Lake, Pike Co., PA
Anabaena sp.
hepatotoxin
Signs of poisoning in
lab mice indicated a
hepatotoxin. LD5O
intraperitoneal mouse =
approx. 50mg/kg
Bureau of Water
Quality
Management.
Storoudsburg, PA
July 1980
Nelson Reservoir,
Montana
Anabaena
flos-aguae and
Aphaniiomenon
anatoxin A
Signs of poisoning in
lab mice indicated a
neurotoxin. LD5O
intraperitoneal mouse =
approx. 1500 mg/kg
Montana Dept. of
Health
Environmental
Sciences
flos-aguae
July-August
1977
Hebgen Lake,
Montana
Anabaena fibs-
aguae.. Microcysijs
aeruginosa and
Aphanizomenon
anatoxin A and
microcystins
.
Signs of poisoning in
lab mice indicated a
neurotoxin and a
hepatotoxin. LD 50
intraperitoneat mouse =
approx.50 mg/kg
Gallatin Co. Health
Dept., Bozeman,
Montana
fios-aguae
* Reported to or investigated by the author. Also see Table 4.
-------
photosynthetic pigments called phycobilins. These pigments can make the cells and hence
the waterblooms and surface scums blue-green to brownish-red. These accessory pigments
allow cyanobacteria to utilize low light intensities by absorbing light over a wide-band of the
visible spectrum. Thus cyanobacteria can grow at lower depths and overall lower light
intensities.
There is a reasonable consensus in the literature that water temperatures below 20°C
are unfavorable for the mass development of the common waterbloom forming genera
Anabaena, Aphanizomenon and Microcystis (Paerl 1987). Slower growth rates at lower
temperatures mean that longer water retention times are required for cyanobacteria to
achieve substantial increases in population. Even under optimal growth rates, determined
by laboratory studies, doubling rates of some nuisance cyanobacteria are similar to other
phytoplankton such as green algae and diatoms (Table 7). This means that waterblooms
and surface scums are more common to lakes, ponds and reservoirs where retention times
are longer than in rivers where dilution rates tend to be higher.
Waterblooms of cyanobacteria are often observed in water bodies undergoing increased
nutrient enrichment especially those water bodies whose nutrient status can be classed as
either eutrophic to hypereutrophic (hypereutrophy is defined as the condition where nutrient
inputs exceed the nutrient demands of phytoplankton). There are three soluble inorganic
nutrient species considered to be of major concern with respect to phytoplankton growth
including the cyanobacteria. These include nitrate-nitrite (N0 3 /N0 2 ), ammonia
(NH 3 /NH 4 4 ) and orthophosphate (P0 4 3 ) (Paerl 1987). While the requirements for these
nutrients by cyanobacteria are not necessarily greater than other phytoplankton,
cyanobacteria appear to employ other factors to assist them in becoming dominant and
persisting in the water body. These involve 1) the ability to store phosphorus within the cell
making them capable of cell division when phosphorus becomes limiting, and 2) fixation of
atmospheric nitrogen by several of the toxic bloom forming filamentous cyanobacteria
especially Anabaena, Aphanizomen, Nodularia and Nostoc. If other nitrogen sources are
depleted, these cyanobacteria have an advantage over other planktonic algae and can
dominate for long periods. Microcystis and Oscillatoria, which do not fix nitrogen, require
eutrophic to hypereutrophic conditions regarding nitrogen to become dominant. It has been
popular to describe ratios of the availabilities of nitrogen (N) to phosphorus (P) which might
favor cyanobacteria growth over other phytoplankton. It has been shown that a lower ratio
of N:P favors cyanobacteria (10 to 16 N:1 P) over most other algae (16 to 23 N:1 P). These
ratios only apply when these nutrients are in limited supply. Under limited nutrient
conditions phosphate is considered to be the best predictor of cyanobacterial abundance.
Most waterblooms that cause acutely lethal poisonings occur when conditions of eutrophy
to hypereutrophy prevail; thus N:P ratios are of minimal use in predicting presence of
potentially toxic bloom situations (Pearson 1990).
Other factors that influence cyanobacterial dominance in waterblooms concern their
consumption by aquatic invertebrates and their ability to regulate cellular buoyancy. While
many planktonic algae are a major food source for microcrustaceans (i.e. Daphnia),
copepods and protozoa, the cyanobacteria are not extensively eaten (Hanazato and Yasuno
1987; Hanazato 1991). There are several exceptions to this trend of cyanobacteria being
32
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Table 6. Freshwater blue-green algae in blooms implicated in poisoning incidents:
confirmed toxic blue-green species and purified toxins.
As Bloom
Species Components
As pure
cultures
Cells
Purified toxin
Anabaena circinalis + + +
Anabaena flos-aquae + + +
Anabaena lemmermanii + nd na
Anabaena solitaria + nd na
Anabaena spiroides + nd na
Anabaena venenosa + nd na
Anabaenopsis mullen + nd +
Aphanizomenon flos-aquae + + +
Coelosphaenum kutzingianum + nd na
Cylindrospermopsis raciborskii + + na
Cylindrospermum sp. + + +
Gloeotnichia ecinulata + + na
Gloeotnchia pisuni + nd na
Gomphosphaeria lacustiis + nd na
Gomphosphaeria naegeliana + nd na
Microcystis aeiuginosa + + +
Microcystis incerta + nd na
Microcystis viridis + + +
Microcystis wesenbergii + nd na
Nostoc sp. + + +
Osdilatoria agardhii + + +
Oscillatona agardhii var. isothrix + + +
Oscillatona rubescens + nd na
Oscillatonia sp. + nd na
Synechocystis sp. + nd na
+ = toxic in mouse bioassay
nd = not determined
na = not available
From: Report of The National Rivers Authority. 1990. United Kingdom.
33
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Table 7. Laboratory-determined optimal growth rates of a variety of nuisance blue-green algal
species as well as diatom and chlorophycean species. Included are data from species
isolated from the Neuse River (Paerl 1987) as well as selected (cited) studies.
Species
Doublings/day
Citation
Microcystir aenaginosa (blue-green alga)
0.75-1.20
(Paerl 1987)
Aphanizomenon flos-aquae (blue-green alga)
0.85-1.50
(Paerl 1987)
Anabaena jlos-aquae (blue-green alga)
Lake Windermere
1.13
(Foy et al. 1976)
Anabaena jlos-aquae (blue-green alga)
Lake Windermere
0.96
(Fay & Kulasooriya
1973)
Oscillatona agardhii (blue-green alga)
1.25
(van Liere 1979)
Scenedesmus spp. (chlorophycean)
0.55-0.75
(Paerl 1987)
Chlo rella spp. (chlorophycean)
0.50-0.85
(Paerl 1987)
Cycloella meneghiniana (diatom)
0.65-0.95
(Paerl 1987)
34
-------
poor food sources. A number of flagellates, amoebae and ciliates can act as predators on
cyanobacteria (Dryden and Wright 1987). Studies on Lake Kasumigaura, Japan have shown
that the rotatorian Phiodina e ythrophthalma and the oligochaete Aeolosoma hemplichi can
degrade Microcystis blooms (Inamori et al. 1987, 1988). In addition, the ciliate Na.ssula has
also been shown to be a voracious consumer of planktonic cyanobacteria especially toxigenic
Oscillatoria , Aphanizomenon and Anabaena (Canter et al. 1990). It has also been observed
that A. hemplichi and P. etythrophthalma can dominate even in the presence of toxic
Microcystis. This observation is being exploited in Japan where those invertebrates are used
on “bioflims” to remove cyanobacteria and their toxins in water treatment processes (Sudo
and Aiba 1984; Inamori et al. 1987, 1988). This reduced grazing by aquatic invertebrates
gives the planktonic cyanobacteria another advantage in their competition with other
phytoplankton. Indeed the production of toxins by cyanobacteria, to inhibit grazing
pressures by zooplankton, may be one of the main ecological roles for these compounds.
Studies have shown that cyanobacteria may be inhibitory or toxic to diatoms (Keating 1978),
zooplankton (Stangenberg 1968; Porter and Orcutt 1980; Snell 1980; Lampert 1981; Infante
and Abella 1985; Nizan et al. 1986; Fulton and Paerl 1987) and crustaceans (Lightner 1978;
Gentile and Maloney 1969; Sasner and Ikawa 1980).
More recently Demott et al. (1991) have shown acute lethality in four species of
zooplankton to the heptapeptide microcystin-LR and the pentapeptide nodularin.
Survivorship of the zooplankters in the presence of toxic Microcystis cells was strongly
influenced by the ability of different zooplankters to discriminate toxic cells from nontoxic
cells (i.e. the green alga Chiamydomonas). The authors concluded that zooplankton have
evolved both physiological and behavioral adaptations which enhance their abilities to
coexist with toxic cyanobacteria. This would suggest that toxicity of cyanobacteria is a
common phenomena and occurs at all times (or much more often than revealed by animal
poisonings). Acute lethal or chronic exposure by mammals is largely a phenomena of heavy
waterbloom and surface scum occurrences.
Heavy waterbloom formation leading to surface scums of cyanobacteria is a consequence
of the buoyancy regulating behavior of the common planktonic cyanobacteria. Of the main
toxic genera only Oscillatoria does not regulate its buoyancy. Buoyancy regulation is an
active process in cyanobacteria. Cell inclusions called gas vesicles inflate and deflate in an
effort to regulate the cell at an optimum depth for nutrient and light availability. Cells
receiving too little light become more buoyant and float upwards. When too much light is
received by the cells, buoyancy is lost allowing the cells to sink. Gases for buoyancy
regulation by these gas vesicles comes from photosynthesis. Therefore, carbon availability
(expressed as dissolved inorganic carbon) in the form of C0 2 , HCO 3 (bicarbonate) and CO 3
(carbonate) is important not only for photosynthesis but for buoyancy regulation as well.
Buoyancy regulation by planktonic cyanobacteria is influenced greatly by the mixing of
waters within a water body. Energy input from the sun warms water near the surface so that
it tends to float (stratify) on top of the deeper colder water. If wind energy is not great
enough to mix the water, this thermal stratification can last for a few hours, days or for
much of the summer. Stratification tends to induce rapid dominance by buoyant populations
of cyanobacteria if conditions of nutrient availability also exist. Thus the low wind days of
summer and fall lead to unhindered thermal stratification and buoyancy regulation. As
35
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biomass of the cyanobacteria increases, the light penetration will decrease. This forces the
cyanobacteria population to increase their buoyancy moving closer to the surface. Even if
wind action mixes the population of cells, light penetration is reduced by the biomass
present, and the cells continue to increase their buoyancy. At night the cells have no
reference point for light with which to decrease their buoyancy and eventually the cells are
“overbuoyant” and form surface scums. These surface scums tend to clump together due
to the gelatinous nature of material surrounding the cells and filaments. As long as the low
wind pattern persists the scum becomes thicker and thicker. Gentle wind and wave action
aids in scum formation and will carry the cells inshore especially on the lee side of a water
body. Thus scums can appear literally overnight and can persist for as long as wind and
wave action do not redisperse the cells throughout the mixing zone. These surface scums
inshore represent the greatest threat to animals including humans. Humans, however, are
naturally “averse” to these surface scums (both their visual appearance and their smell) and
do not willingly make contact with the potentially toxic cells. Even if wind action is able to
move the scum away from the shoreline, the strength of the wind may not be enough to mix
the cells back into the water. Under these conditions mats of scums can be moved about
a water body as rafts of cells. This phenomenon is not common but has been observed in
Hartbeesport Dam, a massively hypereutrophic reservoir in South Africa (Zohary and
Roberts 1990; Zohary et al. 1990). If these scums are not remixed, the cells become
stressed releasing their contents including toxins into the water. When the scums pile up
on filters of a water treatment facility, high levels of toxins can be released into the water
distribution system for consumption by humans (Berg et al. 1987).
Once a population of cyanobacteria such as Microcystis is established in a water body it
continues to create waterblooms and scums on a yearly basis. Reynolds et al. (1981) has
described such a cycle for the toxigenic genus Microcystis. In the winter, vegetative cells of
Microcystis survive on the surface layers of the sediments. In the spring to early summer a
short series of cell divisions leads to cell clusters that begin to develop gas vesicles and thus
buoyancy regulation is established. As nutrient and temperature conditions, continue to
improve, growth is increased and waterblooms can form. Throughout this period the action
of nutrient availability, buoyancy regulation, overbuoyancy conditions and stratification
determine the extent and duration of waterblooms and surface scums. As winter approaches
gas vesicle collapse occurs and rates of sedimentation exceed those of cell positive buoyancy.
CONTROL OF CYANOBACTERIA POPULATIONS
Waterblooms of cyanobacteria are a natural occurrence in many freshwater bodies. The
natural aging process leading to eutrophication, followed by waterblooms and surface scums
is a common phenomena in many lakes not subject to cultural eutrophication. The main
problem with cyanobacteria waterblooms and their toxins arises in those cases where natural
or cultural eutrophication leads to the presence of waterblooms and/or scums in
recreational waters or those waters used as a drinking water supply. Thus the need to
eliminate or control waterblooms will be greatest for reservoirs, lakes and rivers with high
human and/or animal use value. In many cases elimination of cyanobacterial populations
once they have established themselves in a water body is neither practical nor appropriate.
36
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Factors important to the occurrence of cyanobacterial blooms include 1) nutrient input,
2) water retention time, 3) grazing pressure, 4) buoyancy regulation and 5) stratification.
Of these, nutrient deprivation has the highest probability of providing long term control
benefits for cyanobacteria. It is also one of the most expensive. In a study on the Neuse
River, North Carolina, Paerl (1987) recommended that a 30-40% reduction in spring loading
of N0 3 had the best chance of minimizing Microcystis aeruginosa as a competitive and
ultimately dominant phytoplankter. In North America some emphasis has also been placed
on reducing phosphates discharged to sewage treatment plants by reducing the use of
polyphosphate-based detergents. It has been pointed out, however, that these detergent
based phosphates account for only 25% of the load to sewage treatment plants and that the
bulk of phosphates is derived from human wastes. As a result emphasis in Europe has been
on phosphate stripping as a means of controlling phosphorus and thus waterblooms. In any
attempt at nutrient input control, consideration must also be given to the internal loading
of nutrients. Years of nutrient buildup in the sediments particularly phosphorus means that
some consideration needs to be given to removal of sediments, a procedure whose ease
depends on the size and depth of a water body. Controlling factors such as physical
(reducing light, destratification and scum corrals), biological (planktivorous organisms) and
chemical (algicides) might prove useful in managing cyanobacteria waterblooms. While light
removal is an obvious way to eliminate photosynthetic cyanobacteria from a water body, it
is seldom practical to cover a water body unless it is confined and well defined such as some
constructed reservoirs (Sykora et al. 1980). Destratification of a water body, provided it is
deep enough to become thermally-stratified, can be an effective control of waterblooms and
surface scums. Permanent destratification will depress growth of buoyant cyanobacteria but
only where mixed depths exceed, by about a factor of two, the depth of water through which
light penetrates (Pearson 1990).
Biological control of cyanobacteria populations can involve the use of planktivorous fish,
planktonic zooplankton, cyanobacteria lysing bacteria and cyanophages. Planktivorous fish
are sometimes used to control cyanobacteria populations, or more often control is achieved
along with the raising of these fish for food. The author’ s experience over the past several
years in China has found that high rates of clearance and thus control of cyanobacteria is
achieved by the use of Silver Carp (Hypop/zthalmichthys molitrix), Grass Carp
(Ctenopha yngodon idellus), Bighead Carp (Aristichthys nobilis) and Telapia (Telapia nilotica
and T mossambica). In fish ponds and even lakes of significant size, these fish easily
remove the larger colonies of Microcystis and in the process leave smaller unicellular and
flagellated species which are a better food source for zooplankton. The author has also
noted that the Microcystis blooms fed upon by these planktivorous fish are toxin producers.
The fish appear not to be affected by consumption of the toxic algae. In fact the author has
observed fecal pellets composed entirely of Microcystis colonies, from these fish, floating on
the surface of fish ponds in several areas of China. When collected and bioassayed these
pellets are found to contain high levels of microcystin hepatotoxins. Based on these
observations it would be worthwhile to investigate use of these fish for the control of toxic
cyanobacteria. The introduction and use of exotic species of planktivorous fish to control
toxic cyanobacteria waterblooms would of course require careful consideration of the
environmental effects these introductions might make. It can be noted, however, that Grass
Carp are already being used in the United States to control macrophyte growths (Leslie et
al. 1987) and Telapia is being raised in Canadian farm dugouts as a summer “put and take”
37
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form of fish farming (H. Peterson, Saskatchewan Research Council - personal
communication).
The use of zooplankton or cyanophages has not received as much attention as
planktivorous fish. Occasionally cyanobacteria populations have been observed to collapse
as a result of grazing by the ciliate Nassula (Canter et a!. 1990). In addition, the Japanese
are using a rotatoria and oligochaete to control waterblooms of toxic Micro cyst is.
Conversely, there is also good evidence showing that toxic Microcystis, Nodularia and
Anabaena have very detrimental effects on the crustacean Daphnia and the copepod
Diaptomus (Demott et a!. 1991).
Microbiological control of cyanobacteria populations using bacteria or cyanophages has
been advocated for some time (Safferman and Morris 1964, 1979; Burnham and Fraleigh
1983). These studies tend to show that it is difficult to maintain stocks of the lytic organisms
for ready application to a waterbloom and the lysing organism’ s host may be too specific
to control a random bloom of toxic cyanobacteria. However, there is some merit to further
study of these forms of cyanobacteria population control.
In some instances it may be desirable to remove the surface scum of cyanobacteria or
to prevent it from coming inshore by the use of floating booms. This limits animals and
humans from having direct access to high concentrations of cells and toxins. This has been
used at times on small farm ponds to prevent livestock from watering in a surface scum
(Carmichael and Schwartz 1984). The use of booms, such as used to collect oil slicks, are
also being tested in areas of Europe. The booms are used to corral the surface scum so that
it can be pumped off the surface and removed from the lake (Pearson 1990). Obviously
timing is important in using these booms, as surface scums are often dispersed within
minutes. There also needs to be careful disposal of the collected scum especially if it is
toxic.
Another potential, although not often recommended, method to control cyanobacteria
populations is the use of chemicals. While there are several compounds that will kill algae,
there are few which are specific to algae or to cyanobacteria. The short term solution to
cyanobacteria in fresh water is to add copper, usually as copper sulfate, to the lake, reservoir
or farm pond. This is done by towing sacks of copper sulfate round a lake by boat, or
spreading copper sulfate from aircraft. The costs of this treatment are considerable, as it
needs to be repeated each time the cyanobacteria begin to bloom. Some water supplies may
have to be treated several times during a single summer. Copper is used in the water to kill
the cyanobacteria. The consequence of this cell death is the release of cell contents,
including toxins if present, into the water. For this reason, copper sulfate is best applied as
the bloom is forming. This minimizes the taste, odor and toxicity that are released into the
water. If an alternative water source is available, the treated water supply should be
disconnected for 5-7 days to allow the copper content of the water to drop and taste and
odor from the cyanobacteria to decrease. As would be expected, small farm ponds and
dugouts are easier to control than larger lakes and reservoirs. It is also generally impractical
(and ecologically unsound) to use copper in flowing water bodies such as rivers or streams.
Use of algicides in many states of the United States as well as in other countries may be
regulated by the Department of Natural or Environmental Resources, or other regulatory
38
-------
agencies, and an aigicide permit may be required. Copper sulfate (CuSO 4 ) can be
purchased in granular or block form (sometimes called bluestone). When CuSO 4 (CuSO 4 5
H 2 0) is used, the recommended concentration is from 0.2 to 0.4 ppm with an upper limit
of 1 ppm (mg/i). This is equivalent to: (a) 4 to 8 lb per million gallons of water (upper
limit 20 ib), (b) 0.65 to 1.3 ounces per 10,000 gallons of water, (c) 1.4 to 2.8 lb per acre-foot
of water or (d) 20 to 40 g per 50,000 liters of water (Beasley et al. 1983).
Livestock should not be watered from copper-treated water sources for at least five days
after the last visible evidence of a surface bloom. However, there is no way to guarantee
the absence of toxins in the water even after this time. Since sheep are particularly
susceptible to copper poisoning, they should not be allowed access to treated water until the
copper has sedimented out. Other aigicides are available, for example quinones and other
organic herbicides (Fitzgerald et al. 1952). They are not widely used and in some countries
are prohibited from use in water. However, development and approval of organic aigicides
may become necessary if copper resistance by the cyanobacteria develops requiring alternate
chemical controls.
HEALTH EFFECTS OF CYANOBACTERIA
Since most of the waterbloom and surface scum forming cyanobacteria are capable of
producing toxins, their presence in a water body used for recreational or drinking water
purposes should be of concern to animal and human health.
Hazards to Wild and Domestic Animals
The most life-threatening situation occurs when overbuoyant cells form surface scums
and accumulate along a shoreline in calm or low wind weather conditions. The
accumulation of these scums along shorelines or in bays presents watering animals with
potentially lethal concentrations of cells and toxins. Published reports of animal deaths from
cyanobacteria blooms extend back more than a century (Francis 1878). These reports have
documented losses of cattle, sheep, pigs, horses, ducks, geese, and chickens. Wild animal
poisonings from cyanobacteria include amphibians, snakes, water fowl, rodents, bats, bees,
zebras and rhinoceros (Table 4). In many of these older reports of animal deaths the
conclusion that cyanobacteria toxins were responsible rests on the presence of a waterbloom
along with the observation that animals were watering from the bloom followed by illness
or death. The more recent reports include collection of bloom material and verification of
the bloom’ s toxicity followed by isolation and characterization of the toxin.
Two groups of animals, aquatic invertebrates and fish, do not show the same
susceptibility to the cyanotoxins as do mammals and birds. Fish kills, occurring during
periods of heavy cyanobacteria blooms, have happened although there is not a lot of direct
evidence to show that fish are widely susceptible to the toxins. Some cases do exist, for
example, fish killed in blooms of hepatotoxic Oscillatoria in Scandinavia showed liver
damage consistent with the effects of microcystins. Intraperitoneal injections of microcystins
into rainbow trout (Phillips et al. 1985), the common carp (Cyprinus carpio) (Eriksson et al.
1986), and anatoxin-a injection (oral and intraperitoneal) into goldfish (Carmichael 1974)
39
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resulted in mortalities with the same signs of poisoning as in mammals. As stated earlier
in this report, the planktoniverous fish such as silver carp, grass carp, bighead and telapia
appear resistant to the microcystins. It is not known whether this resistance is related to
lack of absorption, detoxification or lack of toxin receptors by this group of fish. It may
explain, however, some of the variability observed with fish deaths by cyanobacteria, and it
also points up the possible use of these fish as biological control agents for cyanobacterial
populations.
Toxicity variation in zooplankton may in part be explained by the recent work of Demott
et al. (1991). They found that survivorship of the microcrustacean Daphnia and the copepod
Diaptomus to toxic Microcystis cells or purified toxin was strongly influenced by both
physiological sensitivity and feeding behavior. Relatively good survivorship by Daphnia
pulicaria was associated with low sensitivity to purified toxin and rapid feeding inhibition in
the presence of toxic cells. In contrast, poor survivorship by Daphnia pulex was associated
with greater physiological sensitivity and low inhibition of feeding on toxic cells.
Intermediate survivorship by the copepod Diaptomus birgei was associated with food
selection capabilities coupled with physiological sensitivity and uninhibited feeding on toxic
cells. The results suggest that zooplankton have evolved physiological and behavioral
adaptations which enhance their abilities to coexist with toxic cyanobacteria. These new
laboratory experimental results may explain some of the previous observations obtained on
aquatic microorganisms.
Toxicity in zooplankton is not always associated with mouse toxicity from the hepato-
or neurotoxins (Mills and Wyatt 1974; Nizan et al. 1986). The rotifer Branchionus
calyciflorus can maintain high populations during blooms of hepatotoxic M. aeruginosa
(Fulton and Paerl 1987) or neurotoxic An. ftos-aquae (Starkweather 1981). Maloney and
Carnes (1966) did not find any effects of a hepatotoxic bloom of M. aeruginosa on fish,
microcrustaceans or diatoms. It is possible that aquatic microorganisms and aquatic
invertebrates, as well as fish, have evolved physiological and behavioral adaptations which
allow them to coexist with toxic cyanobacteria. It does appear that these adaptations could
be stressed and break down when heavy waterblooms and scums of toxic cyanobacteria are
present in a water supply. Under these conditions, species with low adaptations to the
toxins or toxic cells could be reduced or eliminated, shortening food chains and upsetting
the ecological balance of a natural water body. As already mentioned, the primary types
of toxicosis that pertain to wild and domestic animal poisonings are acute hepatotoxicosis
and peracute neurotoxicosis. Most poisoning by cyanobacteria involves hepatotoxicosis
caused by the structurally similar group of small molecular weight cyclic peptides called
microcystin or nodularin (Figures 5, 6, 8).
Of the peptide toxin producing genera, Microcystis is the main worldwide offender, and
of the three toxic species identified to date, i.e. M. aeruginosa, M. viridis and M. wesenbergii,
only M. aerugfrzosa has been used in clinical hepatotoxicosis studies. Animals affected by
the hepatotoxins may display weakness, reluctance to move about, anorexia, pallor of the
extremities and mucous membranes, and at times mental derangement. Since all animals
in a herd, group or flock often drink from the same water supply, most or all of them will
be affected within a similar time period. Death occurs within a few hours to a few days and
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is often preceded by coma, muscle tremors and general distress (Galey et at. 1987). It is
generally agreed at this time that death results from intrahepatic hemorrhage and
hypovolemic shock (Falconer et al. 1981; 1988; Theiss et a!. 1988).
Upon necropsy, animals show hepatic enlargement (increases in liver weight of 2-3x are
common) and often intrahepatic hemorrhage. Hepatic necrosis begins in the centrilobular
region and proceeds periportally. Hepatocytes are initially rounded and dissociated, later
they are necrotic. With time course studies in laboratory animals, dissociated hepatocytes
can appear in the central veins and eventually pass into the pulmonary vasculature (Theiss
et at. 1988; Hooser et al. 1989). Ultrastructurally, in the rat and mouse model, intact cells
retain their nuclei and mitochondria although these organelles are swollen. Rough
endoplasmic reticulum becomes vesiculated and degranulated (partial or total loss of
ribosomes from the vesicles) (Dabholkar and Carmichael 1987).
Animals, especially cattle, that survive an acute cyanobacterial hepatotoxicosis may
experience photosensitization. This photosensitization may be so severe that cows refuse
to nurse their calves (Stowe et a!. 1981; Carmichael and Schwartz 1984).
In general, therapies for algal toxicosis in livestock have not been investigated in detail.
The most likely beneficial agents are powdered charcoal (Stowe et al. 1981) and
cholestyramine (Questran, Mead Johnson, Evansville, IN) (Dahlem et al. 1988). Although
the cholestyramine is more effective, activated charcoal is more readily available and less
expensive. Therapeutic support measures in poisoned animals might also include
administration of whole blood and glucose solutions (Beasley et a!. 1989). Certain chemicals
have also been used experimentally to prevent microcystin hepatotoxicity in laboratory
animals. These include cyclosporin-A (Hermanskey et al. 1990a, 1991), rifampin
(Hermanskey et al. 1990b, 1991), and silymarin (Merish et al. 1991). These antagonists have
been most successful when given prior to or coadministered with the toxin. At present it
is not known how these antagonists might be affecting microcystin toxicity, but it is thought
to involve inhibition of toxin uptake by the hepatocyte.
A summary of field and laboratory studies involving wild and domestic animal
hepatotoxicosis is given in Table 8.
The final type of cyanobacterial animal toxicosis to be considered concerns
neurotoxicosis due to the alkaloid anatoxins and aphantoxins. Cyanobacterial neurotoxicosis
results from ingestion of toxicAnabaena flos-aquae, An. spiroides, Aphanizomenonflos-aquae,
and Oscillatoria (Carmichael 1988; Sivonen et al. 1989a). Although these genera may also
produce peptide hepatotoxins together with the neurotoxins, the neurotoxins are more
rapidly acting, and therefore, dominate the field and clinical syndromes.
Produced by strains of Anabaena and Oscillatoria, the alkaloid neurotoxin antx-a (Figure
1) is a potent postsynaptic depolarizing neuromuscular blocking agent (Carmichael et al.
1979). This toxin causes death within minutes to a few hours depending on the species, the
amount of toxin ingested, and the amount of food in the stomach (Carmichael 1988).
Clinical signs of antx-a poisoning follow a progression of muscle fasciculation, decreased
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Table 8. Animal hepatotoxicosis by cyanobacterial toxins.
Animal Clinical signs and lesions References
Cattle, hepatotoxicosis - clinical signs: Steyn (1945);
sheep recumbancy/weakness, diarrhea, tachypnea/dyspnea, Dillenberg and
trembling, photosensitization, aberrant behavior, Dehnel (1960);
ataxia, pale mucous membranes, algae on skin/ Senior (1960);
hair, weight loss, tachycardia, anorexia. Konst et a!. (1965);
Lesions include: liver-enlarged, congested, Main (1977);
mottled or friable; enteritis/hemorrhage, Skulberg (1979);
edema, anemia, algae in digestive tract, Reynolds (1980);
diffuse centrilobular hepatocyte degeneration. Stowe et a!. (1981);
Jackson et a!. (1984);
Kerr et al. (1987);
Galey et al. (1987)
Dogs hepatotoxicosis - clinical signs: abdominal Senior (1960);
discomfort, recumbancy, diarrhea, vomiting, Dillenberg and
secretions from the eyes and mouth, anorexia, Dehnei (1960);
ataxia, coma. Lesions include: swelling! Edler et a!. (1985)
mottling of the liver, hemorrhagic enteritis,
pulmonary edema, algae in the intestine.
Birds hepatotoxicosis - clinical signs: restlessness, Steyn (1945);
(turkeys, eye blinking, defecation, clonic spasms. Brandenberg and
ducks, Lesions include: hepatic enlargement/ Shigley (1947);
geese) hemorrhage, pulmonary edema, enteritis; algae Dillenberg and
in digestive tract. Dehnel (1960);
Konst et al. (1965);
Jackson et al. (1986)
Fish hepatotoxicosis - clinical signs: nontoxic Phillips et a!.
(rainbow when fish were immersed in a culture of M. (1985)
trout) aeruginosa; died following i.p. administration
with hepatic necrosis.
Monkey hepatotoxicosis - clinical signs: no prodromal Tustin et a!.
(vervet) signs from oral dosin before death. Lesions (1973)
include: liver necrosis and hemorrhage.
Rhinoceros hepatotoxicosis - lesions include: hepatic Soil and Williams
enlargement, hemorrhage and necrosis. (1985)
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movement, abdominal breathing, cyanosis, convulsions and death. In addition, opisthotonos
(rigid “s” shaped neck) is observed in avian species. In smaller laboratory
animals death is often preceded by leaping movements, while in field cases larger animals
collapse and sudden death is observed (Smith et al. 1987). No known therapy exists for
antx-a, although respiratory support may allow sufficient time for detoxification to occur
followed by recovery of respiratory control (Valentine, personal communication).
More recent neurotoxicosis involving cyanobacteria have become associated with a
potent cholinesterase inhibitor termed anatoxin-a(s) (Figure 1) (s = salivation factor). Antx-
a(s) is a guanidinium methyl phosphate ester (M/Z 252) (Matsunaga et al. 1989). To our
knowledge this represents the first example of a naturally occurring organophosphate
anticholinesterase. Antx-a(s) is very toxic (i.p. mouse LD 50 20 pg/kg) but is somewhat
unstable and becomes inactivated with elevated temperatures (>40°C) and under alkaline
conditions. Toxicosis associated with antx-a(s) has been observed in the field (Mahmood
et al. 1988; Cook et al. 1989).
Clinical signs of antx-a(s) toxicosis in pigs include hypersalivation, mucoid nasal
discharge, tremors and fasciculation, ataxia, diarrhea, and recumbency. In ducks the same
symptoms occur plus regurgitation of algae, dilation of cutaneous vessels in the webbed feet,
wing and leg paresis, opisthotonos, and clonic seizures prior to death (Cook et al. 1989).
Laboratory rodents appear tolerant of antx-a(s) when dosed intragastrically but susceptible
by the intraperitoneal route (Cook et al. 1988). Clinical signs in mice include lacrimation,
viscous mucoid hypersalivation, urination, defecation, and death from respiratory arrest.
Rats exhibit the same clinical signs plus chromodacryorrhea (red-pigmented “bloody” tears).
At the LD 50 , survival times are 5-30 minutes (Mahmood and Carmichael 1987; Cook et al.
1988).
Therapy for antx-a(s) toxicosis has not been investigated thoroughly. Mahmood and
Carmichael (1986b) found that atropine would antagonize the muscarinic effects of anatoxin-
a(s), but at the dose given animals still died. Because antx-a(s) does not appear to cross the
blood-brain barrier, it may be possible to use a cholinergic blocker such as methyl atropine
nitrate (Metropine-Pennwalt, Rochester, NY) or glycopyrrolate (Robinul-V, Al-I Robbins
Co., Richmond, VA) (Beasley et al. 1989). Hyde and Carmichael (1991) found that in vivo
pretreatment with physostigmine and high concentrations of 2-PAM were the only effective
antagonists against a lethal dose of anatoxin-a(s).
Some strains of Aph. fios-aquae, so far found only in the state of New Hampshire,
produce the potent paralytic shellfish poisons (PSP) saxitoxin and neosaxitoxin (referred to
as Aphantoxin II and I respectively) (Mahmood and Carmichael 1986a) (Figure 1). These
sodium channel blocking agents inhibit transmission of nervous impulses and lead to death
by respiratory arrest. For such toxicosis, therapy is best approached by trying to limit further
absorption from the gastrointestinal tract by using activated charcoal, and a saline cathartic
plus artificial respiration when needed.
Hazards to Human Health
Cyanobacteria cause health risks not only to wild and domestic animals but also to
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humans (MacKenthan et a!. 1964; Schwimmer and Schwimmer 1964, 1968; Bourke and
Hawes 1983; Stein and Borden 1984; Carmichael et al. 1985; Gorham and Carmichael 1988;
Codd and Poon 1988; Falconer 1989). Reports over the past 60 years have provided case
reports on the adverse effects of cyanobacteria in freshwater to human health. These
reports come from the USA, India, Canada, Zimbabwe, Norway, the Baltic coast, USSR,
Australia, and the U.K. In almost all cases little or no attempt was made to critically
evaluate the reports and carly out proper epidemiological studies. In addition, none of the
reports document human deaths. This probably has a lot to do with the lack of follow-up
studies by public health officials. The reports that have occurred can be divided into those
involving allergic reactions and skin irritations and those where gastroenteritis and
hepatoenteritis are the result of ingestion of cyanobacteria. Infrequent, but recurrent, cases
involve swimming, bathing or showering in water containing a cyanobacteria waterbloom.
Symptoms include allergic reactions, asthma, eye irritation, rashes and blistering around the
mouth and nose (Heise 1949, 1951; Cohen and Rief 1953; Mittal et a!. 1979; Graves and
Arnold 1961). These reports came from Brazil, China, Europe, Norway, USA, and the UK.
All other etiological agents such as bacteria, fungi or protozoa were ruled out as probable
causes of the symptoms.
The earliest public health report implicating cyanobacteria in gastroenteritis afflicting
a population drawing water from a common source occurred on the Ohio River in 1931.
Low rainfall caused stagnation of flow and cyanobacterial accumulation in a side branch of
the river used as a water source. When rain caused water to move from the affected side
branch to the main river, reports of gastroenteritis were reported in towns downstream from
the side branch. The toxin(s) responsible for the illnesses were not identified, nor were the
species of cyanobacteria (Tisdale 1931; Veldee 1931). More recently in Sewickley,
Pennsylvania, a widespread outbreak of gastroenteritis was attributed to the cyanobacterium
Schizothrix caicicola which occurred in that city’s uncovered water supply (Lippy and Erb
1976; Sykora et al. 1980). Toxin or toxins produced by this filamentous cyanobacterium was
the apparent cause of an illness that struck about 62% of the population served by the
Sewickley water utility. Characteristics of the outbreak included diarrhea, abdominal cramps
and other gastrointestinal type symptoms. No definitive toxin was identified as the causative
agent. It was suggested by subsequent laboratoiy studies with S. calcicola, that
lipopolysaccharide endotoxins could have caused the gastrointestinal problems (Keleti et al.
1979, 1981). However, it is also possible that had the cyanobacterial cyanotoxins, i.e.
microcystins, been tested for, they may also have been found to be present. While no
confirmed toxic cyanobacteria was found to be responsible for the outbreak, the reservoir
was covered (preventing growth of the photosynthetic cyanobacteria) and no further
outbreaks have occurred.
An abundant organism in water supply reservoirs, Microcystis aeruginosa, has been
implicated in repeated outbreaks of seasonal gastroenteritis among children in Salisbuiy,
Rhodesia (now called Harare, Zimbabwe). Several supply reservoirs provided water to
different regions of the city, but only the reservoir containing blooms of Microcystis supplied
water to the affected population. The gastroenteritis occurred when the bloom naturally
lysed at the end of summer (Zilberg 1966). Since microcystins are normally confined within
the cyanobacterial cells, and do not enter the water until lysis or cell death, the relationship
between the age and condition of a bloom and the public health consequences is particularly
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important. Water treatment by flocculation and sedimentation, together with sand filtration,
will remove live cyanobacterial cells and debris, but not toxins in solution.
In a retrospective epidemiological study undertaken in Australia, the effects of a
Microcystis bloom on a public drinking water supply were investigated. The bloom had been
carefully studied as part of an ongoing survey of toxic cyanobacteria in water supplies, so
that the dates when the bloom developed, its toxicity and the time when the water supply
authority lysed the bloom with 1 ppm copper sulfate were accurately known. Liver function
data for all patients tested in the surrounding region during the time prior to the bloom,
while the bloom was occurring including its treatment phase, and after the bloom, were
analyzed by computer. Measurements of liver enzyme concentrations in human serum were
sorted by date of sample and geographical location of the patient’ s home. A statistically
significant increase in gamma glutamyl transferase (GGT), indicative of toxic injury to the
liver, occurred only in the population supplied by the affected reservoir, and only at the time
of the bloom (Falconer et al. 1983). There was no evidence of infectious hepatitis affecting
this population, or of alcoholic festivity at the time.
A severe outbreak of hepatoenteritis requiring hospital treatment of over 140
individuals, was also attributed to toxic cyanobacteria present in an Australian water supply.
In this case, severe injury was caused to a large number of children, requiring intravenous
fluid replacement for up to two weeks before recovery. In this instance only individuals
drinking reticulated water from a single dam were affected, and the clinical cases began a
few days after a heavy cyanobacterial bloom on the reservoir was lysed by the addition of
copper sulfate (Bourke et al. 1983). Cyanobacteria cultured from this reservoir were later
identified as Cylindrospermopsis raciborskii, and their toxicity assessed. The dry cells had an
LD of 64 mg/kg by intraperitoneal (i.p.) injection in mice. Unlike Microcystis orAnabaena
toxins, which kill within 15-60 minutes of i.p. injection of a lethal dose, mice given this
material had an average survival time of 19 hours. Histopathological changes included
massive hepatocyte necrosis, plus necrotic tissue injury to lungs, kidneys, adrenals and
intestine (Hawkins et a!. 1985). C. raciborskii is a tropical species, and the island on which
the outbreak occurred is located off the Queensland coast of Australia. Nothing is known
of the chemistry of the toxin involved. Cyanobacteria produce detectable endotoxins of the
lipopolysaccharide type which may have implications for public health, especially in infants
and the sick (Keleti 1979). However, their low oral toxicity indicates they are unlikely to
cause major problems in normal drinking water (Keleti et a!. 1981). As contaminants of
dialysis fluids they may be pyrogenic (Hindeman et al. 1975). They also cause turbidity in
soft drinks prepared from water containing cyanobacteria.
In general, it has been found that the cyanotoxins are not removed by conventional
water treatment procedures of coagulation-sedimentation-rapid sand filtration-chlorination
(Wheeler et a!. 1942; Hoffman 1976; Falconer et a!. 1983, 1989; Keijolu et a!. 1988;
Himberg 1989). These same groups have found that active carbon treatment is effective if
properly used. In addition, ozonization (Keijola et a!. 1988; Himberg et al. 1989) effectively
eliminated toxicity, probably by a cleavage of the double bond on the ADDA component
of microcystin.
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Diarrhea associated with p cvanobacteria-like organism --- a new cyanobacterial health
threat ?
Most reports of gastroenteritis and diarrhea associated with cyanobacteria waterblooms
are from known members of the planktonic cyanobacteria. In recent years there have been
several outbreaks of diarrhea accompanied by anorexia, fatigue and myalgia involving> 100
patients in Southeast Asia and the U.S. (Long et a!. 1990). In all cases the causative agent
has been a cyanobacterium-like organism (CLO) which has not been identified (Long et al.
1991). If the agent is found to be a cyanobacterium, it will be the first proven case of a
cyanobacteria capable of infecting and persisting in the human intestinal tract. At this time
it is not known whether the CLO produces any type of toxin.
Carcinogenic. teratogenic and tumor promotion studies in the laboratory: Implications for
long term effects on humans .
In agricultural regions, or heavily populated areas, there may be continuous water
blooms of toxic cyanobacteria in drinking water reservoirs. While water supply authorities
often control these blooms, the conventional method of copper sulfate treatment lyses the
organisms, releasing toxic cell contents into the water. It is therefore important to evaluate
any long-term public health consequences of chronic ingestion of low concentrations of th
lysed organisms.
The chronic administration of Microcysris extract at low concentration in the drinking
water of mice resulted in increased mortality, particularly in male mice, together with
chronic active liver injury. The deaths were largely due to endemic broncho-pneumonia,
indicating an impairment of disease resistance. Only 6 tumors were seen in the 430 mice
killed at intervals up to 57 weeks of age. However, four of the six tumors were in females
ingesting the highest Microcystis concentration (Falconer et a!. 1988). This result led to an
investigation of the tumor-promoting activity of orally administered Microcystis in mice to
which dimethylbenzanthracene had been applied to the skin. Results of these trials showed
that there were significant increases in the growth of skin papillomas in mice given
Microcystis but not Anabaena to drink (Falconer and Buckley 1989; Falconer 1991).
The finding that microcystin activated phosphorylase a (Runnegar et al. 1987) has led
to some studies which show that microcystin-LR, YR, RR and nodularin are potent
inhibitors of protein phosphatases type 1 (PP1) and type 2A (PP2A) (Adamson et a!. 1989;
Honkanen et al. 1990; MacKintosh Ct al. 1990; Matsushima et al. 1990; Yoshizawa et a!.
1990). This finding is important since inhibition of PP indicates that microcystins are tumor
promoters.
Because microcystins are preferentially taken up by hepatocytes, it is expected that the
main health threat as a tumor promoter would be in liver tumor promotion. Nishiwaki-
Matsushima et a!. (1992), working at the National Cancer Institute in Tokyo, Japan 1 has just
completed a two stage tumor promotion study which demonstrates tumor formation in rat
liver by microcystin-LR. These types of experiments clearly indicate that microcystins are
a health threat in drinking water supplies.
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The threat from microcystins as liver tumor promoters in humans is given further
support from a report recently published by Yu (1989). The report states that in China
primary liver cancers (PLC) rank third for men and fourth for women in the overall cause
of cancers. The report also states in several areas of China the rates of PLC do not
correlate with PLC causing agents such as aflatoxin and hepatitis B virus. Instead, for the
high rate regions most people drank pond and ditch water, while in low-rate regions, even
within the same county or only a Street apart within the same village the people drank water
either from wells or a river. Further long term epidemiological studies continued to show
that people who drank pond and ditch water had a higher risk of PLC than people who
drank well water. The association between use of stagnant surface drinking water and liver
cancer was noticed in the counties of Qidong, Haimin, and Nanhui. After 1973 the
inhabitants of Qidong County were encouraged to dig wells and give up drinking pond and
ditch water. As a result, by 1979 the rate of PLC had stabilized for the County. In
neighboring areas of the county where ditch and pond water continued to be used for
drinking water, the PLC rates were continuing to increase.
These studies did not address the question of whether the ditch and pond waters
contained cyanobacteria or the liver tumor promoting microcystins. However, the author ‘5
work over the past 5 years in collaboration with the Hydrobiological Institute in Wuhan,
Hubei, P.R. China clearly show that a very high number (> 80%) of all ponds sampled
throughout southern, central and northeast China had high cyanobacterial populations
during the summer and fall periods. In addition, most of these populations were Micro cystis
aeruginosa and, of the Microcystis samples tested, 100% produced moderate to high levels
of the liver tumor promoting cyclic peptide microcystins (Carmichael et al. 1988a,b; Zhang
et a!. 1991; Carmichael et al., unpublished data). It is expected that further studies will be
done on the question of drinking water sources, PLC and microcystins in these and other
areas of China.
The marine cyanobacterium, Lyngbya majuscula, causes skin irritation on contact and
contains the well characterized tumor-promoting toxins, lyngbyatoxin A (Fujiki et al. 1984)
and aplysiatoxins (Fujiki et al. 1985). These marine blue-green toxins have only been tested
by skin application so that little is known about their oral toxicity. Other cyanobacterial
species that cause skin irritations occur in both marine and fresh waters. Epidemiological
and experimental research is therefore needed on possible tumor promotion in human
populations by cyanobacterial extracts in water supplies. Until now, however, no studies
have demonstrated cancer initiation by cyanobacterial extracts or toxins.
Teratogenic activity from chronic oral administration of Microcystis extracts has been
demonstrated in mice. Animals of both sexes were provided with a water supply containing
Microcystis extract for 17 weeks prior to mating. This was continued through pregnancy up
to day 5 of lactation. Autopsy of the neonates showed approximately 10% of the otherwise
normal neonatal mice had small brains, exhibited by a gap between the brain and the skull.
Of three such brains subjected to serial sectioning, hippocampal neuronal damage was
evident in one (Falconer et al. 1988).
In summary, whether the tumor-promoting effects or the teratogenic activity of
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cyanobacteria are of public health significance awaits suitable human epidemiological
analysis of cancer deaths and birth defect frequency in populations exposed to this risk.
SUMMARY
An important function of this status report is to provide an analysis of the role that
waterbodies which contain high amounts of cyanobacterial cells and toxins might play in the
health of animals and humans. Clearly, cyanobacterial planktonic populations have been
a part of the ecology of waterbodies throughout geological time. It is conceivable that the
evolution of secondary metabolites such as the microcystins andanatoxins have occurred
along with other adaptations which have conferred competitive advantages for the
planktonic cyanobacteria.
Nutrient enrichment (eutrophication) is also a natural event in waterbodies as they age.
However, human activities have increased the nutrient aging processes of lakes, ponds and
rivers at a rapid rate and on a global scale. Where once a lake or pond might experience
seasonal cycles of phytoplankton that might not have the cyanobacteria dominate for more
than a few weeks a year, these same waterbodies today have nutrient levels such that blooms
of planktonic cyanobacteria occur earlier in the year, persist longer and produce higher
biomasses (including surface scums) than would have occurred even a few years ago. Man-
made reservoirs are particularly subject to the eutrophication process because they have
fewer of the physical and biological characteristics which natural lakes do, and because they
are often situated closer to sources of human activity (agricultural, recreational or
municipal) which contribute more to the process of eutrophication.
Not enough research has been done on the factors which lead to the formation of toxic
waterblooms of cyanobacteria. Whereas it was once thought that there were distinctly toxic
and nontoxic waterblooms, the development and use of more sensitive assay methods such
as EUSA (Chu et al. 1989, 1990; Chu and Carmichael, unpublished data) have shown that
samples testing negative by the mouse bioassay still contain levels of microcystins in the
j. g/g (dry weight cells) range. This lends support to the argument that all the major
planktonic cyanobactena, i.e., Anabaena; Aphanizomenon, Micro cystis, Noduiwia and
Oscilatoria produce cyclic peptide hepatotoxins, and production occurs at all or most phases
of the growth cycle. The factors which result in high levels of toxin, i.e. . 1 mg/g dry weight
cells, should be investigated, since it is these levels which allow enough toxin to be ingested
by watering animals to cause acute lethality.
Many officials remain unconvinced of the need to monitor or regulate cyanobacteria
toxins in municipal or recreational water supplies. The skepticism seems to arise from the
fact that, despite the presence of cyanobacteria toxins in many bodies of water, there are
no confirmed cases of human death or illness from cyanobacteria toxicosis. Several reasons,
which probably act in combination, may explain the lack of reported human toxicity. First,
vectors which concentrate toxins the way shellfish concentrate marine paralytic shellfish
toxins are uncommon in freshwater. Where they do exist, as in Europe or Scandinavia,
people tend not to eat freshwater shellfish, except locally. Second, while the cyanotoxins are
very toxic, and therefore, require only a low concentration to induce lethal toxicity, they also
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have a steep dose-response curve. Specifically, animals must ingest a lethal or nearly lethal
dose before observable signs of poisoning appear. Such high concentrations of toxin occur
only when waterblooms form surface scums. While surface scums are certainly the most
dangerous situation for watering animals, humans tend to avoid them because of their sight
and smell. Third, because of better water quality management and cooler winters, water
supplies in North America and Europe don’ t support high concentrations of toxic
cyanobacteria year round. When waterblooms occur in drinking water supplies, filtration
and dilution reduce levels in the finished water below those that cause acute toxicosis.
Without sensitive detection methods and an understanding of the possible low-dose chronic
health effects in humans, there is a reluctance by public health officials to pursue
cyanobacterial toxins as agents of water-based disease.
Current levels of understanding about the widespread occurrence of toxic cyanobacteria
coupled with more sensitive methods of detection, especially immunoassay, plus the new
evidence showing that the major group of cyanotoxins, the cyclic peptide hepatotoxins, are
potent liver tumor promoters, argues for a prompt reversal of the present lack of effort on
cyanotoxins and water-based disease.
RECOMMENDATIONS FOR RESEARCH AND DEVELOPMENT
1) Continue efforts to develop predictive models to quantify the formation of
cyanobacterial blooms. These models should be developed with thought toward their
use as models to devise management plans for various water bodies.
2) Further research to develop measures to control eutrophication and minimize
development of cyanobacteria waterblooms and scums. These can include: effects of
land use practices and nutrient mn-off; nutrient traps and nutrient stripping methods and
monitoring programs to define the occurrence and distribution of toxic cyanobacteria.
3) Support development of sensitive, rapid and accurate methods for the detection of
cyanotoxins. A likely method for immediate development is the use of ELISA
antibodies for the major group of cyanotoxins -- the cyclic peptide liver tumor promoting
microcystins and nodularin.
4) Support efforts to adopt an existing method or develop a standard procedure for
analytical analysis and purification. This would in turn support efforts to make toxin
standards available for research.
5) Support research leading to an understanding of the transport, fate and ecological role
the cyanotoxins have in aquatic environments.
6) The prokaryotic cyanobacteria can be genetically manipulated and studied with many
of the same techniques available to study molecular and cellular genetics of other
prokaryotes. Therefore support should be given to the study of the physiological and
genetic mechanisms involved in toxin production.
49
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7) Support studies on the taxonomy and classification of cyanobacteria. This information
is critical to effective communication about toxic cyanobacteria and their toxins.
8) Finally, it is recommended that administrative support be developed within the USEPA
to carry out several aspects of the work on cyanobacterial toxins. These include:
a) educating and advising Federal, State and local public health workers, and the
general public on toxic cyanobacteria;
b) linking with appropriate authorities in other parts of the world so that information
can be exchanged and collaborative research projects can be developed and
supported; and
c) developing certain USEPA “in house” research projects on some aspects of
cyanobacteria and their toxins.
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70
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APPENDIX
THE DIRECTORY TO TOXIC
BLUE-GREEN ALGAE (CYANOBACTERIA)
LITERATURE
71
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THE DIRECTORY TO
TOXIC BLUE-GREEN ALGAE (CYANOBACTERIA)
L fERATURE
Wayne W. Carmichael, Ph.D.
Department of Biological Sciences
Wright State University
Dayton, Ohio 45435
Originally Published
June, 1980
Updated
May 1986 - L.A. Carmichael
January 1987 - B. Krejsa & C. Wu
April 1987 - C. Wu
September 1987 - L.A. Carmichael
January 1988 - C. Wu
February 1988 - C. Wu
April 1988 - N. Stephens
July 1988 - N. Stephens
February 1989 - N. Stephens
April 1989 - N. Stephens
August 1989 - N. Stephens
October 1989 - N. Stephens
January 1990 - N. Stephens
February 1990 - N. Stephens
March 1990 - D. J. Douglas
June 1990 - N. Stephens
November 1990 - L.A. Carmichael
May 1991 - L.A. Carmichael
July 1991 - L.A. Carmichael
October 1991 - L.A. Carmichael
December 1991 - L.A. Carmichael
Includes references cited in: Directory j
Toxic Cvanoohvte from Norden .
0. M. Skulberg. 26.11.1986. Norwegian Institute
for Water Research (NIVA), Oslo, Norway
AND
Toksinproduserende blagronnalger i norske
vannforekomster. Rapporter og publikasjoner
NIVA, 31, Januar 1989. O.M. Skulberg
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103. Carmichael, W.W. (1974). Anabaena fkji-aguae toxin : [ f Toxicology and
Mechanism s21 Action . Ph.D. Thesis. University of Alberta, Edmonton,
Alberta, 134 pp.
104. Carmichael, W.W. (1981). Freshwater blue-green algae (cyanobacteria)
toxins--a review. In: W.W. Carmichael (ed.) The Water Environment: Algal
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Toxic Cyanobacteria Reference List -- December 5, 1991
105. Carmichael, W.W. (ed.). (1981). The Water Environment: Algal Toxins and
Health . (Environ. Sci. Res., Vol. 20). New York: Plenum Press, 491 pp.
106. Carmichael, W.W. (1982). Chemical and toxicological studies of the toxic
freshwater cyanobacteria Microcystis aeruginosa, Anabaena flos-aquae and
Aphanizomenon flos-aquae. . . J . j. j :367-372.
107. Carmichael, W.W. (1985). Isolation, culture and toxicity of toxic freshwater
cyanobacteria (blue-green algae) (First American Symposium on Animal,
Plant and Microbial Toxins.). Toxicon (1):25-26. (Abstract).
108. Carmichael, W.W. (1986). Algal toxins. In: J.A. Callow (ed.) Advances jj
Botanical Research . j. . London: Academic Press, pp. 47-101.
109. Carmichael, W.W. (1986). Isolation, culture and toxicity testing of toxic
freshwater cyanobacteria (blue-green algae). In: V. Shilov (ed.)
Fundamental Research in Homo enous Catalysis . j. .. New York:
Gordon & Breach, pp. 1249-1262.
110. Carmichael, W.W. (1988). Freshwater cyanobacteria (blue-green algae)
toxins. In: C.L. Ownby and G.V. Odell (eds.) Natural Toxins:
Characterization, Pharmacology and Therapeutics . London: Pergamon
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111. Carmichael, W.W. (1988). Toxins of Freshwater Algae. In: A.T. Tu (ed.)
Handbook f Natural Toxins . j. ., Marine Toxins and Venoms . New
York: Marcel Dekkar, pp. 121-147.
112. Carmichael, W.W. (1991). Toxic freshwater blue-green algae (cyanobacteria):
an overlooked health threat. Health Environ. Digest . (6):1-4.
113. Carmichael, W.W., Beasley, V.R., Bunner, D.L., Eloff, J.N., Falconer, I.R.,
Gorham, P.R., Harada, K-I, Yu, M-J, Krishnamurthy, T., Moore, R.E.,
Rinehart, K.L., Runnegar, M.T.C., Skulberg, O.M., and Watanabe, M.
(1988). Naming of cyclic heptapeptide toxins of cyanobacteria (blue-green
algae). Toxicon (11):971-973. (Letter to the Editor).
114. Carmichael, W.W., and Bent, P.E. (1981). Hemagglutination method for
detection of freshwater cyanobacteria (blue-green algae) toxins. App!.
Environ. Microbiol . 4.1(6):1383-1388.
115. Carmichael, W.W., and Biggs, D.F. (1978). Muscle sensitivity differences in
two avian species to anatoxin--a produced by the freshwater cyanophyte
Anabaena flos-aquae NRC-44-1. Can . j. Zoo! . fi(3):510-512.
116. Carmichael, W.W., Biggs, D.F., and Gorham, P.R. (1975). Toxicology and
pharmacological action of Anabaena flos-aquae toxin. Science .1 .’L:542-544.
117. Carmichael, W.W., Biggs, D.F., and Peterson, M.A. (1979). Pharmacology
of anatoxin-a, produced by the freshwater cyanophyte Anabaena flos-aquae
NRC-44-1. Toxicon fl:229-236.
81
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Toxic Cyanobacteria Reference List -- December 5, 1991
118. Carmichael, W.W., Eschedor, J.T., Patterson, G.M.L., and Moore, R.E.
(1988). Toxicity and partial structure for a hepatotoxic peptide produced by
Nodularia spumigena Mertens emend. strain L575 (cyanobacteria) from New
Zealand. Apol. Environ. Microbiol . j (9):2257-2263.
119. Carmichael, W.W., and Falconer, I.R. (In Press). Disease related to
freshwater algal blooms. In: LR. Falconer (ed.) Algal Toxins j Seafood and
Drinking Water . London: Academic Press.
120. Carmichael, W.W., and Gorham, P.R. (1977). Factors influencing the
toxicity and animal susceptibility of Anabaena flos-aquae (cyanophyta)
blooms. j. Phvcol . J :97-101.
121. Carmichael, W.W., and Gorham, P.R. (1978). Anatoxins from clones of
Anabaena flos-aquae isolated from lakes of western Canada. Mitt . Jjj .
Verein. Limnol . 2.1:285-295.
122. Carmichael, W.W., and Gorham, P.R. (1980). Freshwater cyanophyte
toxins: types and their effects on the use of micro algae biomass. In: G.
Shelef and C.J. Soeder (eds.) Algae Biomass Production and Use .
Amsterdam: ElsevierfNorth Holland, pp. 437-448.
123. Carmichael, W.W., and Gorbam, P.R. (1981). The mosaic nature of toxic
blooms of cyanobacteria. In: W.W. Carmichael (ed.) The Water
Environment: Algal Toxins and Health . New York: Plenum Press, pp. 161-
172.
124. Carmichael, W.W., Gorhain, P.R., and Biggs, D.F. (1977). Two laboratory
case studies on the oral toxicity to calves of the freshwater cyanophyte (blue-
green alga) Anabaena flos-aquae NRC-44-1. Can . . J. 71-75.
125. Carmichael, W.W., He, J-W, Eschedor, J., He, Z-R, and Yu, M-J. (1988).
Partial structure determination of hepatotoxic peptides from Microcystis
aeruginosa (cyanobacterium) collected in ponds of Central China. Toxicon
2 (12):1213-1217.
126. Carmichael, W.W., Jones, C.L.A., Mahmood, N.A., and Theiss, W.C.
(1985). Algal toxins and water-based diseases. In: C.P. Straub (ed.) Critical
Reviews Environmental Control . j. j . Florida: Chemical Rubber
Co. Press, pp. 275-313.
127. Carmichael, W.W., and Mabmood, N.A. (1984). Toxins from freshwater
cyanobacteria (blue-green algae). In: E.P. Ragelis (ed.) Seafood Toxins .
(ACS Symposium Series 262). Washington, D.C.: American Chemical
Society, pp. 377-389.
128. Carmichael, W.W., Mahmood, N.A., and Hyde, E.G. (1990). Natural toxins
from cyanobacteria (blue-green) algae. In: S. Hall and G. Strichartz (eds.)
Marine Toxins: Origin, Structure, and Molecular Pharmacology . (ACS
82
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Symposium Series, #418). Washington, D.C.: American Chemical Society,
pp. 87-106.
129. Carmichael, W.W., Pinotti, M.H., and Fraleigh, P.C. (1986). Toxicity of a
clonal isolate of the cyanobacterium (blue-green alga) Microcystis aeruginosa
from Lake Erie. Ohio . j. (2):53. (Meeting Abstract).
130. Carmichael, W.W., and Schwartz, L.D. (1984). Preventing livestock deaths
from blue-green algae poisoning. Farmers Bulletin . #2275. Washington,
D.C.: U.S. Dept. of Agriculture, 12 pp.
131. Carmichael, W.W., Yu, M-J, He, Z-R, He, J-W, and Yu, J-L. (1988).
Occurrence of the toxic cyanobacterium (blue-green alga) Microcystis
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132. Carter, D.C., Moore, R.E., and Mynderse, J.S. (1984). Structure of
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133. Chakraborty, T.K., and Joshi, S.P. (1990). Total synthesis of n-phthalayl
ADDA methyl ester: all stereocenters originating from a single chiral
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134. Chamberlain, W.J. (1948). Effects of algae on water supply. Department Qf
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135. Chaput, M., and Grant, G.A. (1958). III. Screening of a number of species.
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136. Chengappa, M.M., Pace, L.W., and McLaughlin, B.G. (1989). Blue-green
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137. Chiang, P.K., Butler, D.L., and Brown, N.D. (1991). Nicotinic action of
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138. Cholnoky-Pfannkuche, K. (1970). Toxizitat III: Experimente mit Microcystis
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139. Christensen, J.H., and Bak, H. (1981). Blagronalger i Himrnelbjergsoerne
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140. Chu, F.S., Huang, X., and Wei, R.D. (1990). Enzyme-linked immunosorbent
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83
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141. Chu, F.S., Huang, X., Wei, R.D., and Carmichael, W.W. (1989). Production
and characterization of antibodies against microcystins. App!. Environ.
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142. Codd, G.A. (1983). Cyanobacterial poisoning hazard in British freshwaters.
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143. Codd, G.A. (1984). Toxins of freshwater cyanobacteria. Microbiol . j.
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144. Codd, G.A., and Bell, S.G. (1985). Eutrophication and toxic cyanobacteria in
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145. Codd, G.A., Bell, S.G., and Brooks, W.P. (1989). Cyanobacterial toxins in
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146. Codd, GA., Brooks, W.P., Lawton, L.A., and Beattie, K.A. (1989).
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147. Codd, G.A., Brooks, W.P., Priestly, I.M., Poon, G.K., and Bell, S.G. (1989).
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148. Codd, G.A., and Carmichael, W.W. (1982). Toxicity of a clonal isolate of the
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149. Codd, G.A., Lawton, L.A., Hawser, S.P., Beattie, K.A., Fawell, J.K., and
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150. Codd, G.A., and Poon, G.K. (1988). Cyanobacterial toxins. In: L.J. Rogers
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154. Cook, W.O., Beasley, V.R., Dahiem, A.M., Dellinger, J.A., Harlin, K.S., and
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155. Cook, W.O., Beasley, V.R., Lovell, R.A., Dahiem, A.M., Hooser, S.B.,
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156. Cook, W.O., Dahiem, A.M., Harlin, K.S., Beasley, V.R., Hooser, S.B.,
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157. Cook, W.O., Dellinger, J.A., Singh, S.S., Dahiem, A.M., Carmichael, W.W.,
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158. Cook, W.O., Iwamoto, G.A., Schaeffe, D.J., Carmichael, W.W., and Beasley,
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159. Costa, A.C.S., Aracava, Y., Rapoport, H., and Albuquerque, E.X. (1988). N,
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161. Cote, L-M, Lovell, R.L., Jeffrey, E.H., Carmichael, W.W., and Beasley, V.R.
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164. Dabholkar, A.S., and Carmichael, W.W. (1987). Ultrastructural changes in
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165. Dabholkar, A.S., Carmichael, W.W., Berg, K., and Wyman, J. (1987).
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169. Dahiem, A.M., Hassan, A.S., Swanson, S.P., Carmichael, W.W., and
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170. Dahlem, A.M., Hassan, A.S., Swanson, S.P., Carmichael, W.W., and Beasley,
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