Aquaculture, 88 (1990) l-20 1

Elsevier Science Publishers B.V., Amsterdam - Printed in The Netherlands

Review

Cyanobacteria in fish ponds

J. Sevrin-Reyssac and M. Pletikosic

Laboratoire d’fchtyologie G&&ale et Appliquke, M&urn National d’Histoire Naturelle,
43, rue Cuvier, 7.5231 Paris, Ckdex OS(France)
(Accepted 12 October 1989)

ABSTRACT

Sevrin-Reyssac, J. and Pletikosic, M., 1990. Cyanobacteria in fish ponds. Aquaculture, 88: l-20.

In many fish ponds, blue-green algae (cyanobacteria) constitute the greater part of the phytoplank-
tonic biomass during the summer. They sometimes form spectacular water blooms, often with harm-
ful consequences such as massive mortality among the fish, mainly caused by depletion of oxygen
after the bloom collapses. Their specific properties render them better able than other phytoplankton
to adapt to certain conditions usually encountered in fish-ponds: reduced light penetration, nitrogen
depletion in the upper layer. Cyanobacteria which are able to assimilate dissolved atmospheric nitro-
gen gain a selective advantage over competitors when combined nitrogen fails, and many of them are
capable of vertical migration due to buoyancy regulation, this particularity being another competitive
advantage in stratified ponds. Blue-green algae are of poor food value to zooplankton, their large size
making them inaccessible to the filter-feeding entomostraca. The substances produced by many spe-
cies of cyanobacteria are toxic to aquatic plants and animals. The aigicides used to limit their devel-
opment are effective but are often detrimental to the environment. Another solution would be to
increase the N: P ratio to 5 or more, which benefits chlorophyceae and reduces the number of cyano-
bacteria. The use of aerators to break vertical stratification and avoid low concentrations of oxygen
also makes water conditions unfavourable to blue-green algae. In spite of very abundant research on
cyanobacteria, every summer they cause many fish-kills in ponds.

INTRODUCTION

At first classified as algae, cyanobacteria were later considered to be affili-

ated to bacteria, owing to their biology and the absence of a differentiated
nucleus. They now form the cyanobacteria order within the prokaryote divi-
sion (Gibbons and Murray, 1978; Sieburth and Estep, 1985 ) . Although com-
monly known as blue-green algae, cyanobacteria vary in colour according to
the pigment dominant in the cytoplasm. Most frequently they are blue-green
(green from chlorophyll, blue from phycocyanin ), but certain species contain
phycoerythrin which is reddish.

0044-8486/90/$03.50 0 1990 Elsevier Science Publishers B.V.

2 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

They were formerly considered as indicators of waters suitable for com-

mercial fish culture (Arrignon, 1970), but now serious economic losses are
imputed to their massive development. The present study reviews the factors
influencing their growth, the nuisances they cause to the environment and
means of limiting their blooms.

ABUNDANCE OF CYANOBACTERIA AND WATER CONDITIONS

Blue-green algae are widespread. The major factors influencing their growth
are light, temperature, chemical composition of the medium and dissolved
oxygen content (Fogg et al., 1973; Reynolds and Walsby, 1975 ).
In spite of a capacity for heterotrophic growth, their major mode of nutri-
tion is autotrophic. Besides being able to survive the extreme light conditions
at the water surface, they are able to sustain biomass under low-light condi-
tions better than eukaryotic algae. The main reason is their low maintenance
energy requirements at low light levels (Mur and Beijsdorf, 1978 ) . This abil-
ity is a great advantage in eutrophicated ponds.
Planktonic species (Oscillatoria, Aphanizomenon, Anabaena, Coelospher-
ium, Microcystis, Gleotrichia) are supposed to have a preference for warm
water (temperature of 17-20’ C ) . High temperatures seem also an important
factor conditioning the formation of blooms. It is well known that fish farm-
ers encounter these phenomena in summer. According to Fogg et al. ( 1973 ) ,
temperatures optimal for some of the bloom-forming species are probably in
the range 25-35°C. Reynolds ( 1984) indicated that 20°C is the temperature
for optimal growth of most species known in temperate regions and 25 ’ C or
greater for Anabaena, Aphanizomenon, Oscillatoria and Microcystis (Robarts
and Zohary, 1987 ) . Microcystis aeruginosa which generally develops later in
the year than Anabaena and Aphanizomenon seems to be most severely lim-
itedbelow 15°C (Fogget al., 1973).
However, an examination of Iield data around the world indicated that
temperature acts with other factors in this process. The increase in tempera-
ture indirectly promotes better growth of cyanobacteria as it starts off some
conditions influencing their competitive advantage over other species: light
penetration is reduced due to higher phytoplanktonic biomass, water bodies
often become stratified, and nitrogen is depleted in the upper layer. These
factors favour cyanobacteria which are capable of vertical migrations. These
migrations are carried out by means of turgor-pressure-mediated partial col-
lapse and resynthesis of the gas vesicles in the cells, the organisms alternately
becoming heavier or lighter than the surrounding medium, and thereby sink-
ing or floating up (Walsby, 1969). In Israeli fish-ponds, Van Rijn and Shilo
( 1985 ) showed a die1 vertical migration of Oscillatoria, Spirulina and Micro-
cystis populations between the upper layer where they can utilize light and the
water-sediment interface where nutrients usually accumulate. According to
CYANOBACTERIA IN FISH PONDS 3

Reynolds and Walsby ( 1975 ), thermal stratification selects against non-mo-

tile algae (diatoms and many species of green algae) while the buoyant prop-
erties of many species of cyanobacteria maintain them within the most fa-
vourable layer.
Cyanobacteria sometimes predominate in waters poor in nutrients, max-
ima tending to occur some weeks after the nutrient concentrations have de-
creased (Fogg et al., 1973). The reason for this may be that they store previ-
ously available nitrogen which they use under nitrogen-limiting conditions.
However, their abundance seems closely linked to the degree of eutrophica-
tion of the water. In the region Centre (France), cyanobacteria represented
less than 5% of the phytoplankton in unfertilized ponds, but they often con-
stituted the major part of the phytoplankton biomass (over 75%) when fer-
tilizers were added ( Sevrin-Reyssac and Gourmelen, 1985 ) . The numbers of
filaments (Aghanizomenon, Osdutoria) can then reach several thousands
per milliliter, with maxima in the summer period (Fig. 1). Boyd ( 1979) re-
ported that they form more than 90% of the algal biomass in fertilized fish
ponds in Alabama.
Are cyanobacteria favoured by organic nitrogen? From the observations of
Pearsall ( 1932) in English lakes, the growth ofblue-green algae is often attrib-
uted to a high concentration of dissolved organic compounds (Home and
Fogg, 1970; Home et al., 1972). In fact, the role played by organic matter in
promoting blue-green algae abundance remains uncertain (Reynolds and
Walsby, 1975) but the substantial quantity of oxidizable substances in fish
ponds (excrements of zooplankton and fishes, organic fertilizers added) may
be of considerable benefit to cyanobacteria indirectly because it lowers the
concentration of dissolved oxygen and it is known that nitrogen fixation is
improved under such conditions (Fogg, 1971; Stewart, 1971; Fogg et al.,
1973 ) . According to Stewart and Pearson ( 1970)) in the light, blue-green al-
gae grow more rapidly under microaerophilic than under fully aerobic con-
ditions. They showed that nitrogen fixation and photosynthetic carbon fixa-
tion in Anabaenaflos-aquae are inhibited by high levels of oxygen. Hence, the
development of blue-green algae may depend on the ability of the ponds to
maintain low concentrations of dissolved oxygen for long periods (Ganf,
1974).
The massive development of cyanobacteria is favoured by an inorganic ni-
trogen deficiency in the upper layer receiving light. Reynolds ( 1984) noted
the predominance of Anabaena or Aphanizomenon in such conditions. When
nitrogen becomes a limiting factor, the most favoured species are those assim-
ilating atmospheric nitrogen, this process being associated with the presence
of heterocysts (Anabaena, Aphanizomenon, Oscillutoria, Lyngbya) , and the
extent of this assimilation depending on their number (Fay et al., 1968; Stew-
art, 1969; Home and Goldman, 1972). Nitrogen deficiency can also influ-
ence the competitive advantage of other species of cyanobacteria that lack
4 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

:ilaments ml-‘(x10001

30,

I
I
I
20.
I
!
\
\
\
\

10,

Fig. 1. Abundance of cyanobacteria as a function of fertilization. Pond A: fish-farm wastes added

to the water twice (34 kg ha-‘) and a phosphate liquid fertilizer ( 14/48), seventeen times (200
1ha-‘). Pond B: fertilizer containing only superphosphates, added to the water five times ( 190
kg ha-‘). Pond C: untreated (after Sevrin-Reyssac and Gourmelen, 198%)

heterocysts but are capable of vertical migration (buoyancy regulation) and

so can use inorganic nitrogen present close to the water-sediment interface.
According to Eberly ( 1967), it is generally observed that downward move-
ment of population maxima occurs very often in the summer as light intensi-
ties increase and nutrient concentrations decrease in the upper layer.
This remarkable facility to adapt to the physico-chemical conditions gen-
erally found in fish ponds explains why cyanobacteria increase there enor-
mously. They can end up by covering the pond completely with a mat several
millimeters, even several centimeters, thick. These surface water blooms can
be very fleeting or they can last several days. Their occurrence depends upon
the abundance in the medium of buoyant species which can stabilize at the
surface: Coelosphaerium, Gomphospheria, Microcystis, Oscillatoria, Spiru-
lina, Anabaena, Anabaenopsis, Aphanizomenon, Gleotrichia. It depends also
CYANOBACTERIA IN FISH PONDS 5

on hydrological stability and a reduced surface turbulence (Boyd et al., 1978;

Reynolds, 1984). The action of the wind churns up the surface water layer
and disperses the cells in a more or less homogeneous vertical distribution
(Fig. 2). Surface blooms can reform with great rapidity with the cessation of
turbulence. Intense accumulation of the cells at the surface often occurs when
they are unable to correct over-buoyancy during passage to the surface in calm
conditions. Many reasons can explain this deliciency, one being that the cells
are senescent and no longer capable of effecting turgor-collapse (Reynolds
and Walsby, 1975). Samples taken from Anabaena, Aphanizomenon and
Gleotrichia blooms are rarely viable, even under ideal laboratory conditions.
However, according to Walsby ( 1970)) these surface populations are not in-
variably moribund: the formation of large aggregates may have biological ad-
vantages, for example immunity from grazing zooplankton.
Lastly, mention must be made of the indirect effect that the filter-feeding
zooplankton can have on nitrogen concentration in the euphotic layer and
consequently on the abundance of cyanobacteria capable of fixing atmos-
pheric nitrogen. Nilssen ( 1978) suggested that a proliferation of cyanobac-
teria could be helped by a decrease in the numbers of large filterers (Daphnia )
subject to intensive predation by fish and Cyclopoidea copepods. In the sum-
mer, when the small phytoplanktonic forms are not over-deljleted by the pre-
dators, they increase enormously, with the results that nutrients in the envi-
ronment are used up and, at the same time, the water becomes less transparent.
Conditions then may be favourable for the cyanobacteria. On the other hand,
numerous studies have found correlations between the abundance of zoo-
plankton grazers and the timing of cyanobacterial blooms. Haney ( 1987 ) , for

Filaments ml%1000 “d

1347 I3 14 16
APRI L

Fig. 2. Wind effects on the vertical distribution ofAnabaena variabilis in two ponds in Alabama
(U.S.A. ) . Sampling dates are given below each pair of diagrams. Numbers above each pair of
diagrams indicate wind run 24 h preceding sampling (after Boyd et al., 1978 ).
6 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

example, suggested that large grazers such as Daphnia pulex promote the
growth of colonial cyanobacteria by selectively eating competitive phyto-
plankton, cyanobacteria being generally not grazed as rapidly as smaller
phytoplankton.

EFFECTS OF CYANOBACTERIA ON THE ENVIRONMENT

Cyanobacteria play a major role in fish-culture ponds, not only because of

their prolific development, but also due to their effects on the environment
and on aquatic organisms. Like other phytoplanktonic cells, they secrete a
variety of metabolic substances into the medium (Fogg, 1966, 1971) which
have been the subject of a number of studies cited by Dussart ( 1966). These
substances act at very low doses and are responsible for the evolution of pop-
ulations, development cycles or “successions” of different planktonic groups.
They can have an inhibiting effect on other species (hetero-antagonism) or
on the very cells which have secreted them (self-antagonism) (Lefevre et al.,
1952; Pourriot, 1966; Hellebust, 1974). The way a water bloom forms and
then disappears can be explained thus. A cyanobacteria species finds optimal
conditions in a pond and increases until it becomes dominant, eliminating by
its excretions most of the other species, until they are found only sporadically
(hetero-antagonism ) , so that the phytoplankton present is very abundant but
not very diversified (Lef”evre et al., 1952). The active substances liberated
into the medium become so concentrated that the dominant species can no
longer multiply (self-antagonism). These substances then accumulate in the
cells, causing their death, and decomposition by bacteria follows.
The effect of the active substances is a specific one. Inhibiting certain spe-
cies, they can stimulate the development of others. Thus, phormidine issuing
from a culture of the cyanobacterium Phormidium uncinatum inhibits the
development of Scenedesmus quadricauda, a chlorococcal very frequent in
fertilized ponds, whereas it stimulates the development of Ankistrodesmus
falcatus another very common chlorococcal, and the diatom Achnanthes mi-
crocephafa (Lef&re et al., 1952). Some active substances liberated by cyano-
bacteria can halve the division time of desmidiaceae (Lef”evre et al., 1963).
These antagonisms between cyanobacteria and other algae have been ob-
served experimentally (Table 1) . When Aphanizomenon multiples, diatoms
and protococcals are found only sporadically (Lefevre et al., 1952). As for
Oscillatoria planctonica which develops in winter and in spring, it prevents
other species from thriving (Table 1 ), though a compatibility exists between
this species and Aphanizomenon gracile (Lefevre et al., 1952). Sevrin-Reys-
sac and Gourmelen ( 1985) in France and Munawar ( 1974) in tropical ponds
reported that cyanobacteria and diatoms do not cohabit in a mass but other
factors than hetero-antagonism can explain this evolution.
Lefevre et al. (1952) also noted that very abundant species cohabit in
equivalent proportions only if they belong to the same family. This is the case
CYANOBACTERIA IN FISH PONDS 7

TABLE 1

Action of water from ponds containing a large proportion of one of the Cyanobacteria species (Ana-
baena, Microcystis, Aphanizomenon, Oscillatoria) on cultures of various chlorophytes, cyanobacteria
or diatoms (after Lefevre et al., 1952, modified)

Species Anabaena Anabaena Anabaena Microcystis Aphanizo- Oscillatoria

sp. spiroides spiroides jlos aquae menon planctonica
var. minima gracile

Pediastrum ++++ ++ ++++ +-k-t+ ++

Pediastrum boryanum ++++ + +++ ++++ ++ ++++
Scenedesmus + ++++ +++ ++++
quadricauda
Cosmarium lundelii ++++ ++++ ++ ++++ ++++ +-t-++
Phormidium ++++ -I-+ ++++ ++ ++++
uncinatum
Phormidium + ++ ++ +++
autumnale
Nitzschiapalea + + -
Micrasterias lapillifera +++
Chlorella pyrenoidosa ++ ++++ +++

+++ + Complete inhibition with death of the cells.

+ + + Inhibition without death of the cells.
+ + Antagonist effect with delayed multiplication.
+ Slight antagonist effect.
Without influence.
- Favourable influence.

with Anabaena variabilis and Aphanizomenon gracile and with three species
of Microcystis found in practically equal proportions.
The effect of the active substances released by cyanobacteria is not limited
to other phytoplanktonic organisms. The toxic metabolites sometimes have a
harmful impact on zooplankton, e.g. inhibiting nutrition and reproduction
among some rotifers (Erman, 1962; Pour-riot, 1965 ) and certain cladocerans
(Ryther, 1954; Uhlman, 196 1) . Arnold ( 197 1) reported the more or less rapid
mortality rate of Daphnia pulex feeding on unicellular cyanobacteria. The
toxicity of Microcystis extracts was established by Braginskii ( 1955 ) on en-
tomostraca of the genera Daphnia and Cyclops, and that of Microcystis fil-
trates and CoeZosphaerium on Eudiaptomus (Smimov and Feoktistova,
1965 ) . Filtrates of Nostoc muscorum, a soil cyanobacterium, are poisonous
to Daphnia magna (Pourriot, 1966).
Certain cyanobacteria also have a harmful effect on fishes. Some intoxica-
tions, leading at times to massive mortality, particularly among carp, have
long been known (Prescott, 1948; Shelubsky, 195 1). Lefevre et al. ( 1952)
describe mortalities of carp and pike in a Moroccan lake containing a great
abundance of four species of Microcystis, experiments having shown that it is
8 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

not a question of oxygen content but due rather to toxins from cyanobacteria.
For carp injected with a suspension of Microcystis aeruginosa, or with a mix-
ture from other species of Microcystis, Shelubsky ( 195 I ) noted that the first
problems of balance occur after some hours, and are followed by death a few
days later (Table 2 ) .
According to Barthelmes ( 1984), a Microcystis concentration of 0.6 g l- ’
would be lethal for perch less than 1 year old, death occurring a few hours or
days later. With a concentration between 0.03 and 0.3 g l-l, the metabolism
of the fish changes, though without incurring death.
In southern France, Seymour ( 1980) associated a high rate of mortality in
carp with a bloom of Aphanizomenonflos-aquae. This species is, moreover,
held responsible for drastic fish poisoning (Gorham, 1964; Sawyer et al., 1968;
Gentile and Maloney, 1969). Lastly, Lef”evre et al. ( 1952) noticed that the
presence of a large mass of kphanizomenon gracile appeared to coincide with
a dwarfism of roaches. When transported to another pond devoid of cyano-
bacteria, these fishes produced normal-sized offspring.
Toxicity varies greatly from one species to another, and for individuals of
the same species according to the strain. Those considered harmful usually
belong to the genera Microcystis, Anabaena, Aphanizomenon, Oscillatoria and
Gleotrichia (Bishop et al., 1959), among which five species are particularly
toxic: Microcystis aeruginosa, Anabaena jlos-aquae, Aphanizomenon jlos-
aquae, Coelosphaerium kiitzingianum and Gleotrichia echinulata (Fitch et al.,
1934; Grant and Hughes, 1953; Gorbam, 1960). But it is above all Microcys-
tis aeruginosa which causes the most harm (Gorham, 1960). In the summer
of 1988, all the fish died in a Forez region pond (France) following a bloom
of this species. The substance it secretes is a mixture of five polypeptides, only
one of which is poisonous. This may contain seven amino-acids and Gorham
( 1960) gives their proportions.
As for the Aphanizomenonflos-aquae toxin, this seems to be identical to

TABLE 2

Lethal doses of Micvocptis (dry weight ) dn carp of different ages (after Shelbusky, 195 1, modified)

Size of carp

8-log 60-80 g 300-500 g

Weight of Latency Weight of Latency Weight of Latency

dried alga time (h) dried alga time(h) dried alga time (h)
(mg) (mg) (mg)
Microcystis l-2.5 36-48 5-10 48 25-50 48-96
aeruginosa
Microcystis sp. l-2.5 36-48 5-10 48 1O-20 48-96
CYANOBACTERIA IN FISH PONDS 9

the saxitoxin produced by the marine dinoflagellate Gonyaulax with a fast

action resembling that of curare (Champiat and Larpent, 1988 ) .
The harmful effect of cyanobacteria on aquatic animals, and notably on
fishes, can occur in various ways: (i) the fish is contaminated directly by the
substance secreted from cells; (ii) the fish is intoxicated by bacteria associ-
ated with cyanobacteria, for they use the nitrogen substances from their au-
tolysis or some of their metabolites. Among these bacteria, some species, or
their excretory products, are poisonous if ingested (Gorham, 1960); or (iii)
the fish dies as a result of deoxygenation of the water due to the decomposi-
tion of a water bloom (Fig. 3). In fact, it is not absolutely proved that, in the
field, cyanobacterial toxins caused death among the fish. Probably, depletion
of oxygen, after bloom collapses, is the main cause of fish mortality (Abeliov-
ich, 1969; Carmichael, 198 1). Finally, following a bloom, an increase in the
ammonia content can accompany a sharp drop in oxygen. Seymour ( 1980)
observed an NH3 peak a few days after the bloom of a species belonging to
the genus Aphanizomenon. This high ammonia content, especially in combi-
nation with low oxygen, caused serious harm to carp: skin lesions, bleeding at
the skin surface or at the gill level, etc.
Effects due to excretory products and deoxygenation can act simultane-

,2r02(w 1-5

APRIL MAY

Fig. 3. Dissolved oxygen concentrations before and after a phytoplankton bloom. Massive cell
mortality occurred in the afternoon of 29 April. Oxygen concentrations were measured in the
morning at 07.00 h, at the surface and at I and 2 metres depth (after Boyd et al., 1975).
10 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

ously during the last and the most dangerous stage of the water bloom. In-
deed, living or recently dead, cells are found which liberate active substances,
and there is the action of mineralizing bacteria known to be great oxygen con-
sumers. The degree of toxicity of a cyanobacteria bloom depends therefore on
several factors such as the dominant species present, the types and quantities
of associated bacteria, conditions of cell decomposition and finally the im-
portance of the ingestion rate among the animals, i.e. the quantities consumed.
Cyanobacteria can also have an impact on land animals living near the
ponds. Schwimmer and Schwimmer ( 1964) collected a vast amount of dot
umentation on the effects of ectocrine substances produced by Anabaena,
Qngbva, Aphanizomenon and Coelosphaerium, not only on aquatic animals
(crustaceans, fishes, amphibians) but also on terrestrial animals (mammals
and birds). In 1878, a report came from Australia of the death of thousands
of sheep contaminated by water rich in cyanobacteria, and later, in 1940, a
high mortality rate occurred in the Transvaal among sheep and wild animals
which had drunk water full of Microcystis (Lefevre et al., 1952 ) . Rabbits and
guinea pigs injected with 1 ml of this water succumbed within 15 min. There
have been numerous cases of poisoning and death among cattle drinking pond
water containing a Microcystis bloom (Skulberg, 1978). It is worthwhile
pointing out though that domestic ducks are immune to toxic elements pro-
duced by Microcystis, for the cyanobacteria are regurgitated before they reach
the digestive tube (Gorham, 1960).
In man, some species can provoke irritation of the skin and mucosae, acute
dermatosis, conjunctivitis and other allergies, as well as neuro-musclar trou-
bles. When ingested, they can cause gastro-intestinal disorders (Gorham,
1960; Stepanek et al., 1963; Champiat and Larpent, 1988).
In ponds, a fairly long time is required - around several weeks - before all
these active substances are totally destroyed (Lef”evre et al., 1952).
Lastly, some species of cyanobacteria liberate compounds (geosmin, 2-
methylisoborneol, hexanal and heptanal) giving a muddy taste and smell to
the water and to the flesh of fish (Tabachek and Yuzkowski, 1976). Some-
times, these substances are produced by lower fungi of the ascomycete group
associated with cyanobacteria (Lovell and Sackey, 1973; Champiat and Lar-
pent, 1988). This type of nuisance occurs even in winter with the develop-
ment of cyanobacteria (Phormidium) living at the bottom of the pond. When
ingested by fish, they give them this characteristic flavour. The muddy fla-
vour can be easily eliminated by maintaining fishes in cold and clean water
for a few days (Lovell, 1976). For the catIish, lo- 15 days at 15 “C or 6-l 0
days at 22 oC are necessary. However, during this period, the fish lose weight.

CYANOBACTERIA IN THE TROPHIC WEB

Much research has given us an appreciation of the complexity of zooplank-

ton-cyanobacteria interactions. Bogatova ( 1965 ), cited by Lampert ( 1987))
CYANOBACTERIA IN FISH PONDS 11

provided an historical account and concluded that the question of the role of
blue-green algae in the nutrition of planktonic crustaceans is one of the great-
est controversies in contemporary hydrobiology.
The oral aperture of cladocera is too small to let prey larger than 50 nm
pass through, so many cyanobacteria species are too big to be appropriate
food (Champ and Pourriot, 1977). Whether cladocera feed on cyanobacteria
depends essentially on their morphology. Lefevre ( 1944,195O ) observed that
an abundance of Aphanizomenon gracile, with their fine rigid trichomes,
impedes the movement of the daphnids. The filaments, 125 to 850 nm long,
are not eaten by Duphnia magna and Daphnia pulex. They accumulate in the
preoral groove and cannot pass beyond the barrier of the animal’s mandible.
The rigidity of the Aphanizomenon seems to be the cause of this phenomenon.
At first, with the help of claws on their post-abdomen; the daphnia manage to
eject the bundles of algae accumulating in the prebuccal groove, but once again
this becomes clogged up and the daphnia, unable to make use of this abun-
dant but inappropriate food, die of exhaustion and inanition a few days later.
Due to its straight slender form, Anabaena variabilis also clogs up the filtering
apparatus of the cladocera and causes high mortality among them (Lefevre,
1944). Results of laboratory studies (Lampert, 1987) suggest that many co-
lonial cyanobacteria are either not eaten or are a poor food for large zooplank-
ton, particularly Daphnia. Filaments of Anabaena sp. interfere seriously with
the filtering mechanism of Cerioduphnia and Duphnia but Bosmina sp. ap-
pears to be least adversely affected (Bums et al., 1987).
In the field, Sevrin-Reyssac and Gourmelen ( 1985 ) reported that cyano-
bacteria and cladocera do not develop simultaneously. Negative correlations
have also been found between fecundity or development of different species
of Daphnia and cyanobacteria (George and Edwards, 1974; Bums, 1987).
However, when Aphanizomenon gracile, A. flos-aquae or Anabaena spi-
roides produce hormogonias (fragments of t&homes giving daughter colo-
nies ), these become suitable food owing to their reduced size (Lef”evre, 1944).
The cells of Microcystisflos-aquae are also eaten by filter-feeding zooplankton
for they are’ small sized ( < 10 nm ) . Copepods can also consume cyanobac-
teria such as Aphanizomenon j7us-aquae and Lyngbya limnetica (Infante,
1978) or Anabaena sp. (Gras et al., 197 1). Finally, some species of rotifers
(Brachionus) could well eat unicellular cyanobacteria (Ito and Iwai, 1957).
Other planktonic organisms likely to feed on cyanobacteria are protozoa of
the ciliate group (Nassula, Ophyroglena) or the rhizopods (Pelomyxa), par-
ticularly the lilamentous species such as Anabaena or Aphanizomenon (Rey-
nolds, 1984).
According to Lefevre et al. ( 1945 ), cyanobacteria are of interest in the food
chain during two periods: in spring and early summer, when intensive multi-
plication ends with the formation of small hormogonia which can be con-
12 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

sumed by the zooplankton, and at the end of the vegetative period when col-
onies break up into tiny fragments.
Among the fish, the microphytophagous carp (Hypophthalmichthysmoli-
trix) must be mentioned as a consumer of cyanobacteria. When filtering water,
these fishes ingest large quantities and Microcystis aeruginosacan even con-
stitute their main diet. When these carps abound in a pond, Barthelmes ( 1984)
has noted that Microcystis does not develop very much, though he is dubious
about the role of these fishes as regulators of cyanobacteria proliferation. He
considers that a quantitative improvement of the phytoplankton, due to the
presence of this carp, is less important than previously believed. In Lake
Grunz, he reports that numerous filaments of Oscillutoriahad not been con-
sumed or digested. The effect of H. molitrix could have been to change the
phytoplankton population by eliminating Microcystis which was replaced by
Oscillatoria.
Thus, it seems that the influence of these microphytophagous carps on the
abundance of cyanobacteria and, in particular, the faculty they have of re-
stricting the formation of water blooms, has not yet been clearly established.
Although earlier studies have mentioned that blue-green algae are eaten by
roaches (Lefevre, 1940)) the exact part they play in the nutrition of micro-
phytophagous fishes remains to be evaluated.

MEANS OF LIMITING THE DEVELOPMENT OF CYANOBACTERIA

The most frequently used algicides are copper sulphate and simazine which
block photosynthesis.
The inhibiting effect of copper sulphate has been known for some time. In
1948, Prescott reduced the development of cyanobacteria by using doses of
0.12 mg l- ’ (Table 3 ) . He suggested concentrations between 0.12 and 0.5 mg
l- ’ in order to reduce multiplication of the genus Anabaena, and 0.06 to 0.5
mg 1-l for Microcystis aeruginosaand Aphanizomenon sp.
Cyanobacteria have been observed to be more sensitive to Cu than are other
algae. Whether this means there is a specific site that is more susceptible or

TABLE 3

Effects of copper sulphate at a concentration of 0.12 mg 1-l on three genera of cyanobacteria (after
Prescott, 1948)

Genera Number of filaments or colonies per liter

Before treatment 3 days after 9 days after 20 days after

treatment treatment treatment

Anabaena 220 000 88 500 55 400 29 000

Microcystis 150 000 14 600 46 800 42 600
Aphanizomenon 38 400 18 000 11 300 11300
CYANOBACTERIA IN FISH PONDS 13

just that the other competing species are more tolerant is not known (Rueter
and Peterson, 1987).
Not all phytoplanktonic species are sensitive to copper sulphate, as Palmer
( 1962) indicates when establishing a list of the species resisting it and those
which are vulnerable. Among the latter, he includes cyanobacteria belonging
to the genera Anabaena, Microcystisand Aphanizomenon.
The use of copper sulphate has been successful in reducing the abundance
of phytoplankton (Fig. 4), but the effectiveness depends on many factors:
temperature, alkalinity and pH of the water (toxicity is higher with an acid
reaction) and concentration of compounds such as humic substances which
form, with copper, less toxic chelated compounds (Stiff, 197 1).
The doses recommended vary greatly from one author to another: 0.025 to
more than 1 mg l- ’ (Montgomery, 196 1); 0.33 mg l- ’ for an alkalinity below
0.50 mg 1-l and 2 mg 1-l for an alkalinity higher than 50 mg 1-r (Bartsch,

Colonies ml”(xlOOO)
4-

140;
I
120

80

.
60

100
40
20 / \ i\

.
I , _.--.Y', I I

240-

/
200-

July Aug. Sep. Oct.

Fig. 4. Effects of an application of copper sulphate at a dose of 0.84 kg ha-’ in two ponds on the
proliferation ofMicrocystis, a genus of cyanobacteria. Arrows indicate the moment of applica-
tion (after Crance, 1963, modified).
14 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

1954). When alkalinity is 80 mg l- ’ of CaCO,, Sohacki et al. ( 1969) found

appreciably reduced photosynthesis with a dose of 2 mg I- ‘.
Button et al. ( 1977) spread 4 kg ha-’ whereas Crance ( 1963) used 0.84 kg
ha- ’ to reduce blooms. Finally, Bachasson ( 1987), in a manual intended for
ponds managers, recommended doses of 1 g me3 in acid waters and 1.5 g rnp3
in alkaline waters. Copper sulphate is only effective, however, for a very short
time (Fig. 4), so that more has to be added repeatedly.
This treatment sometimes fails, possibly because dissolved organic matter
and humic substances, including polypeptides liberated by the algae them-
selves, produce non-toxic complexes with the copper ion (Fogg et al., 1973 ).
Two different application methods are used: either the copper sulphate is
released directly from a boat into the water or is placed in sacks suspended in
different places, so that it dissolves slowly in the medium. To avoid a bloom,
the latter method is advisable (Boyd, 1979).
Many studies have been made of the harmful effects of copper sulphate on
fish (McKee and Wolf, 1963; Jackson, 1974). Certain species are more sen-
sitive than others. Some authors indicate that the maximal doses tolerated
may be very low, but they do not mention the characteristics of the water
(Prescott, 1948; McKee and Wolf, 1963 ). The concentrations suggested are:
0.14 mg l- ’ for trout, 0.30 to 0.33 mg I- ’ for carp, 0.40 mg l- ’ for catfish and
pike, 0.50 mg 1-l for crucian carp, 0.67 to 0.75 mg 1-l for perch, and 2.0 to
2.1 mg l- ’ for black bass. In fact, the tolerance thresholds indicated vary greatly
within the same species, but these discrepancies are probably due to differ-
ences in the characteristics of the media studied (temperature, alkalinity, ex-
posure time of the fish, etc. ).
In general, the concentrations of copper sulphate used are not toxic for the
fish but cause the death of a great number of invertebrates belonging to the
food chain which leads to fish: rotifera, cladocera (Boyd, 1979).
When eliminating cyanobacteria, copper sulphate destroys at the same time
other phytoplanktonic organisms which are likely prey for zooplankton: green
algae, diatoms, flagellates (Palmer, 1962 ) . The effect of copper sulphate on
the environment also means a drop in dissolved oxygen due to the decompos-
ing algae (Crance, 1963). In any case, copper sulphate is only a temporary
palliative, and the wisdom of repeatedly adding a permanently poisonous
substance to a pond is questionable.
In order to diminish its effects on aquatic animals, copper-based com-
pounds have been developed. For example, when copper forms a compound
with triethanolamine, it becomes less poisonous. Cutrine contains 7.1% cop-
per sulphate associated with triethanolamine and this compound has been
successful in the United States (Boyd, 1979). The dose used in fertilized ponds
is two applications of a dose of 0.25 mg 1-l. Sprague ( 1968) suggested the
use of nitrilotriacetic acid as chelator.
Simazine is a powerful inhibiter of photosynthesis and, when used at doses
CYANOBACTERIA IN FISH PONDS 15

intended for the control of phytoplankton, is not poisonous to fish. Norton

and Ellis (cited by Boyd, 1979 ) indicate that a single application at a dose of
0.25 mg 1-l or at 0.50 mg l-‘, or two applications at a dose of 0.25 mg l-‘,
allow a selective destruction of the blue-green algae. It is advisable to apply
this treatment before the blooms become too dense.
Applications of simazine are also recommended during the draining pe-
riod, at the rate of 11.2 to 16.8 kg ha- ‘, as this method avoids a drop in oxy-
gen following treatment of a full pond (Snow, 1964 ) . Oxygen deficiency can
cause mortality among fish. Boyd ( 1979) reports that the very day after a
simazine treatment, one third of the fish in the pond were killed.
Simazine is not affected by pH (Mauck, 1974) but, as with copper sul-
phate, temperature of the water plays an important role in its efficacy which
is very limited in cold waters. Blue-green algae are not controlled at 12- 13 ‘C
(Walker, 1964). Sutton ( 1965 ) listed two main factors affecting efficacy: the
amount of water flowing from the ponds and the concentration of plants pres-
ent before treatment.
Simazine was found to have relatively low toxicity to aquatic fauna. Its
maximum solubility in water is 5 mg l- ’ and the toxic dose for aquatic orga-
nisms is almost always greater than this value (Mauck, 1974).
With Janick et al. ( 1980), we can conclude that herbicides are expensive,
difficult to administer properly, and potentially damaging to the environment.
According to many experiments, a nitrogen input may advantage the chlo-
rophyceae. Rhee (1978) and Rhee and Gotham (1980) suggested that the
N: P ratio is one of the factors influencing competition between these algae
and the ,cyanobacteria. If it is low, this benefits cyanobacteria fixing atmos-
pheric nitrogen, whereas in the case of a high ratio (equal to or more than 5 ) ,
the chlorophyceae dominate. For example, a relationship exists between an
Aphanizomenon bloom and two types of fertilization in which the N: P ratio
is different. Aphanizomenon prospers in waters where the ratio is 2 : 1, but no
multiplication occurs with a 5 : 1 ratio (Seymour, 1980). Other experiments
demonstrate that a 4: 1 ratio encourages the development of phytoplankton
without, however, a formation of blue-green algae blooms (Swingle and Smith,
1939). In hypertrophic Canadian waters, Barica et al. (1980) increased the
N : P ratio and thereby reduced Aphanizomenon blooms, but laboratory stud-
ies do not clearly link low N:P ratios with cyanobacteria. Certainly, other
factors such as temperature, mixing regime, transparency, iron and carbon
availability may influence cyanobacteria dominance (Pick and Lean, 1987 ) .
In ponds, the best technique would be to add regularly low quantities of nitro-
gen to maintain favourable conditions for chlorophyceae but avoid too in-
tense blooms of these algae. Other experiments are necessary to master this
method.
The use of aerators may be another technique to make water conditions
unfavourable to cyanobacteria: turbulence breaks up the stratification of the
water body and increases dissolved oxygen (discussed above).
16 J. SEVRIN-REYSSAC AND M. PLETIKOSIC

Biological means might reduce blooms but they have to be evaluated, for
example the influence of microphytophagous carps. If, according to Nilssen
( 1978 ) , a proliferation of blue-green algae is favoured by a decrease or a dis-
parity of large filterers, the method proposed by Smith ( 1985 ) and tested in
1000-l tanks, could be applied with success in the field. It consists of main-
taining large lilter-feeding zooplankton by excluding predation by fishes from
part of the water column. This technique is being tested in 400-m* ponds of
the Dombes region (France).
Lastly, Fogg et al. ( 1973) suggested the utilisation of a specific antimeta-
bolite inhibiting the formation of gas vacuoles or the use of ultrasonic waves
to destroy them. It has also been suggested ( Walsby, 1968) that the pressures
generate by detonating explosive devices might be used to collapse gas vacu-
oles in algal blooms and so to destroy their buoyancy.

CONCLUSION

Fish-farmer generally do not notice the presence of cyanobacteria until they

accumulate on the surface of the water, forming blooms. Yet they can be very
abundant in an environment, even representing the main element of the phy-
toplankton biomass in summer time, without the spectacular bloom phenom-
enon necessarily occurring, which is usually dealt with by drastic chemical
treatments. The introduction of fertilizers to increase production in fish ponds
can contribute to the development of cyanobacteria which are of poor food
value and also may impair the environment in various ways such as deoxy-
genation of the medium owing to the decomposition of a water bloom, some
species being potentially toxic to fish.
The cyanobacteria can therefore be considered highly undesirable in fish-
culture ponds. As a result, efforts have been focused on factors controlling
their blooms and on management schemes to reduce their magnitude.
Unfortunately, the processes used to limit their proliferation are often det-
rimental to the environment, causing a drop in the dissolved oxygen content,
toxicity among the invertebrates of the food chain leading to the fish, and
even among the fishes themselves when the doses applied are too strong. One
interesting solution would be to introduce a nitrogen-based fertilizer which
would enhance the rapid multiplication of green algae and so promote com-
petition between cyanobacteria and chlorophyceae, but this treatment must
be performed with caution. If it is to be effective, it would be wise to be aware
of the phytoplanktonic species dominating the environment.
Another solution would be to increase the dissolved oxygen content me-
chanically, thus breaking off vertical stratification of the water body, and to
avoid low concentrations for long periods, conditions very favourable to the
blue-green algae. Aeration also permits elimination of toxic gas (hydrogen
sulphide), as well as greater feeding rates and fish production.
CYANOBACTERIA IN FISH PONDS 17

It is evident that further research must be undertaken in order to master

the techniques inhibiting the development of cyanobacteria, while taking care
not to damage the environment.

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