Journal of Applied Bacteriology Symposium Supplement 1985. 175s-186s

Algal blooms : consequences, and potential cures

M . J . D A F T , J.C. B U R N H A M * & Y O K O Y A M A M O T O ~ Department of Biological Sciences, University of Dundee, Dundee DD1 4HN, U K ; *Department of Microbiology,

Medical College of Ohio, CS 1008, Toledo, Ohio 43699 USA and ?Faculty of Agriculture, Meiji University, Higashimita, Tama-ku, Kawasaki 214, Japan

1. Introduction, 175s 2. Description of experimental sites, 176s

2.1 Chemistry, 176s 2.2 Location and use of the sites, 176s 2.3 Primary production, 177s

3. Isolation of predators and their prey, 177s 3.1 Viruses, 177s 3.2 Fungi, 177s 3.3 Actinomycetes, 178s 3.4 Bacteria, 178s 3.5 Amoebae, 178s 3.6 Cyanobacteria, 178s

4.1 Cyanophages, 179s 4.2 Bacteria, 182s 4.3 Amoebae, 183s 4.4 Actinomycetes, 184s 4.5 Fungi, 184s

5. Discussion, 184s 6. Conclusions, 185s 7. References, 185s

4. Interactions amongst prey and predators, 178s

1. Introduction

In Britain the appearance of high concentrations of algae and cyanobacteria in bodies of freshwater shows a generalized pattern. Pulses or blooms of primary producers occur when many factors coincide to give conditions that favour rapid reproduction and growth of the organisms. Spring blooms of diatoms frequently develop when dissolved nitrogen levels are high and silica concentra- tions are adequate. Cyanobacteria tend to become dominant in summer and in the autumn when temperatures are higher and light conditions sufficient to support photosynthesis at differing depths in the water column. A great deal of work has centred on the physical factors that influence the growth of primary producers such as temperature, nutrients, competition and grazing. Less informa- tion is available on the interactions of microbes that can parasitize, to varying degrees, the primary producers and utilize their extracellular products. Colonization of heterocysts of Anabaena by bac- teria has been illustrated by Pearl (1976) and in their study on algal lysis Daft & Stewart (1973) found large numbers of lytic bacteria accumulated around the heterocysts. Such bacteria have been shown by Fallowfield (1981) to grow solely on the excretion products of cyanobacteria. Reports on the lysis of cyanobacteria by bacteria (Shilo 1970) and by actinomycetes and cyanophages (Safferman & Morris 1962, 1963) indicated similar relationships already known from studies on bacteriolysis (Haska 1974; Gnosspelius 1978). Lysis may be brought about by enzymes produced within the host, exoenzymes, the establishment of direct contact or by the production of antibiotics. More recently Burnham et al. (1981, 1984) have described entrapment and lytic mechanisms involving a Myx- ococcus species and the cyanobacterium Phormidium Euridum. Predation of cyanobacteria by amoebae and their distribution patterns have been discussed by Canter & Lund (1968), Cook & Ahearn (1976) and Yamamoto (1981).

176s M . J . Daft et al. It would appear that primary producers are subjected to a wide range of predators. These pred-

ators cause lysis of the various host cells by many different mechanisms. Such systems have probably co-evolved, normally existing in dynamic equilibrium or showing periodic oscillations in numbers of both prey and predator. This paper describes the development of algal and cyanophycean blooms and some of their microbial predators. We discuss the modes of lysis and speculate on how these predators may be manipulated in order to disturb the normal growth patterns of the primary producers. The sites selected for most detailed discussion are those which have provided either or both of the prey and predators used in our studies.

2. Description of experimental sites

2.1 CHEMISTRY

Each body of water has its own particular chemical and physical characteristics. These factors may vary from year to year and the overall productivity may change also, thus making predictions of the succession within a bloom difficult. Some of the factors that are considered important by most workers are given for five sites in Table 1. These sites, in the past, have proved fruitful for our

Table 1. Chemical characteristics of five freshwater habitats ~~

Alkalinity Total Soluble Maximum Surface (CaCO, nitrogen phosphate temperature Silicate water

mg/l) (mdU (mg/l) (“C) (mgm PH Lintrathen reservoir* 23 0.20 0.02 15 2.0 6.8 Monikie reservoir* 67 0.50 0.03 24 2.0 8.0 Balgavies Locht 94 1.69 0.15 18 3.3 8.5 Forfar Locht 143 4.20 2.62 21 2.8 7.8

- 3.4 3.2

Eglwys Sewage - 4-43 1.30 - - Nunydd 1 Inlets {Stream __ 151 0.08 -

Reservoir! Main outlet - 1.09 0-09 20 3.9 8.5

* Data from Tayside Regional Water Services. t Stewart e? a!. (1977). t Edwards (1972).

comparative studies on pathogens of the Cyanophyceae. Lintrathen Reservoir had the lowest conduc- tivity values and contained least total nitrogen and soluble phosphate. At Monikie Reservoir the values recorded were intermediate with Balgavies Loch. Both Forfar Loch and Eglwys Nunydd Reservoir receive treated sewage and this accounts for their very high nitrogen and phosphate contents. Silicate contents at the time of sampling were similar for all sites.

2.2 LOCATION A N D USE OF THE SITES

Lintrathen Reservoir (Nat. Grid Ref. 37/274/539) is the main source of water for the city of Dundee. It has a surface area of 1.8 km2 and the catchment area is mainly coniferous forests (Fallowfield 1981). Originally Monikie Reservoir (Nat. Grid Ref. 37/502/383) served as a water supply to Car- noustie but now forms part of a public recreational park. It has a surface area of 0.32 km2 and the surrounding land area is used for intensive agriculture. Similar land use occurs around Balgavies Loch (Nat. Grid Ref. 533510), surface area 0.21 km2, which is now designated as a nature reserve. Two main uses of Forfar Loch (Nat. Grid Ref. 443502) are sailing and the inflow of sewage from the works serving the town of Forfar. The Welsh reservoir of Eglwys Nunydd (Nat. Grid Ref. 55795850) was built to supplement the local river supplies, which were insufficient in dry periods, to supply the British Steel Corporation Works at Port Talbot. Water is supplied to the reservoir via the Castle Stream and the River Kenfig, and both sources contain treated sewage. The reservoir has a surface area of 1 .O 1 km’.

Algal blooms 177s 2.3 P R I M A R Y PRODUCTION

In general primary production is governed by the availability of nutrients. In the spring and summer periods the concentration of nitrogen, in most forms, decreases in the photic zone. In the autumn release of nitrogen from the sediments can replenish this deficit and a major source of combined nitrogen to the water systems in agricultural areas is nitrate. Phosphorus, however, presents different conditions as the phosphate ion in soil is comparatively immobile. Hence phosphate may limit growth in aquatic systems if the surrounding soils have high phosphate-fixing capacities. Water run off, domestic and agricultural wastes are major sources of phosphorus, and detergents in domestic sewage may significantly increase the levels of phosphate. With the input of the elements necessary for mass culture of the primary producers other factors play an important part in the total yield. Grazing by rotifers, crustaceans, benthic invertebrates, insects, fish, crocodiles and mammals reduce yields in different parts of the world (Frost 1980; Goldman & Horne 1983).

Temperate regions often show spring blooms consisting of Asterionella and Melosira. Asterionella is a holoplankton which has a minimum light requirement and needs a particular concentration of nutrients for optimum growth. It can store up to 100 times its own requirements for phosphate as polyphosphate granules. This may reduce the apparent phosphate levels in the water to low levels. Melosira often shows a less rapid growth rate but can persist for long periods and, coupled with its ability to remain dormant in sediments, it possesses several attributes that enhance its competi- tiveness. At Lintrathen Reservoir algal cell counts only varied between 9.5 x 103/ml and 3.5 x lo2/ ml throughout one year of sampling (Fallowfield 1981). Asterionella formosa comprised more than 70% of the algal population in early spring, then decreased during the mid-summer months and was detected at much lower concentrations in the autumn. In the same reservoir Melosira granulata was a dominant species during the winter months, less numerous in the early spring and apparently absent from the water column in the summer months. A different pattern for both algae was found by the latter author at Monikie Reservoir. Asterionella formosa contributed little to the spring diatom bloom but was a major component of the autumn and winter populations. In the summer and early winter months M . granulata accounted for a major portion of the algal biomass and then declined to minimal levels by mid-winter.

In their comparative studies on lochs Stewart et al. (1977) found that species diversity was mark- edly less in Forfar than in Balgavies Loch. In Forfar Loch the Chlorophyceae and Bacillariophyceae predominated but the Cyanophyceae, namely Microcystis Jlos-aquae was dominant in Balgavies. The reservoir at Eglwys Nunydd showed algal succession well known at many other eutrophic sites. Diatoms, Tabellaria Jlocculosa, Asterionella formosa and Fragilaria crotonensis made up the spring bloom and Microcystis aeruginosa and Aphanizomenon Jios-aquae the summer to autumn bloom (Edwards 1972).

3. Isolation of predators and their prey

3.1 VIRUSES

Strains of cyanophage LPP-DUN1 (Daft et al. 1970) were originally isolated from water samples taken from Forfar Loch. The plaques produced on lawns of Plectonema boryanum and from lysed liquid cultures of this susceptible cyanobacterium were purified using the standard techniques (Stewart & Daft 1977). Aphanotheca stagnina was the host used to isolate the cyanophage Aph-1 from a water sample taken from a drainage ditch near to the River Ganges at Banares, India by Professor H.N. Singh. Both cyanophages were maintained by serial transfer and when required were isolated from single plaques after filtration through a bacteriological membrane.

3.2 FUNGI

A filamentous fungus, identified as a species of Cephalosporium was isolated from the Farmoor reservoir. near to Oxford.

178s M. J. Daft et a\.

3.3 A C T I N O M Y C E T E S

Both water and soil samples contain species of actinomycetes that cause lysis of a wide range of hosts (Daft 1981: Al-Tai 1982). Once isolated from the Iysates these actinomycetes can be maintained on standard solid media.

3.4 B A C T E R I A

Plaques on cyanobacterial lawns yielded several bacterial isolates from sites in Scotland and England (Daft & Stewart 1971). These bacteria are probably members of the genus Lysobacter (Christensen & Cook 1978). In the USA Burnham and co-workers (Burnham et al. 1981, 1984) have isolated M y x - oewciis that have an entrapment and lytic mechanism for the lysis of cyanobacteria. These M y x - OCOCCILS have been isolated from farm drainage ditches (Burnham et al. 1981). They can be maintained on algal broth medium which contains tryptone.

3.5 A M O E B A E

Since the isolation of the protozoan Asterocaelum algophilum by Canter (1973) amoebae have been shown by Yamamoto (1984) to be important members of the planktonic benthic communities. The algophorus amoebae were isolated on double-layered plates containing a suspension of the prey (Yamamoto 1978).

3.6 C Y A N O B A C T E R I A

During the development of a bloom, net samples were collected and the components used as soon as possible for experimentation. In some instances the members of the phytoplankton were separated under a binocular microscope and then subcultured for a short period in half-strength ASM-1 medium (Gorham et a/. 1964).

4. Interactions amongst prey and predators

Figure 1 outlines the interactions amongst the cyanobacteria and the various predators.

Higher fungi

\ Extraceilulor products

C yanophages

I /

Extrocellulw I

internal lysis

I enzymes

Primary producers; Ent- - Cyanobocteria - Myxococus sp

\ I / (ontibiotics)

Lower fungi lnternol

(Chytrids) parasites (Prey species)

Extracailular enzymes / // Engulfment Exhaxlldm \ \tact

anttbtotics \ (CP-I type) Actimycetes

Amoebae iym!miw (CP-I type)

Fig. 1. Interactions amongst cyanobacteria and their predators.

Algal blooms 179s 4.1 C Y A N O P H A G E S

In 1970 Daft et al. suggested that populations of Plectonema, or closely related cyanobacteria, and cyanophages are in equilibrium within certain aquatic habitats. Furthermore this cyanobacterium may not be a major bloom former because of its susceptibility to infection by phage. However, several phages have been reported to lyse cyanobacteria that cause blooms but not all have been purified and classified.

Phages appear to be attractive agents for controlling nuisance growths of cyanobacteria. They have a rapid rate of multiplication. The generation time of LPP-DUN1 is 10 h and the burst size is about 100 phage particles for each infected cell making up the filament. The burst size for Aph-1 cultured in the unicellular Aphanothece stagnina is slightly lower at 80 particles per cell (Daft & Stewart unpublished). Morphologically, several of the recognized types of bacteriophages (Bradley 1967) are now known for cyanophages (Stewart & Daft 1977). The effects of phage infection on photosynthesis of the host have been discussed by the same authors. Figure 2 shows some of their modified data from an experiment using P. boryanurn and LPP-DUN1 in a batch culture. Photofixa- tion of CO, was not significantly reduced whilst viral replication took place, but after 24 h there was a rapid fall off with a rise in virus titre.

I I ?\.-.*- 0 J \

12 24 36 48 60 Hours after inoculation

Fig. 2. 0, Multiplication of LPP-DUN1 (pfu/ml); X, photosynthesis of control and 0, infected Plectonerna boryanum.

If the lysate is kept under suitable illumination for about 14-21 d a phage-resistant population develops within the flask. This development was investigated by Cowlishaw & Mrsa (1975) and Barnet et al. (1981). In continuous culture using two cyanobacteria-cyanophage systems the latter authors found reciprocal oscillations in cyanobacterial and phage numbers (Fig. 3). In each system an equilibrium was established and the components or protagonists appeared stable. At the end of the experiment the A. stagnina was apparently resistant to the phage Aph-1. Two types of resistant Plectonerna were isolated, PR1 and PR2, wild-type LPP-DUN1 did not lyse PR1 but these cells were susceptible to the mutant phage (D,,,). PR2 was not affected by the phage and grew slower than the wild-type Plectonema. These findings may be of interest in understanding the maintenance of both prey and predator in nature. The complete lysis of wild-type Plectonema by the mutant phage with no recovery of the host after 30 d (Fig. 4) suggests that mutant phages may present a method for the control of cyanobacteria. Different mutant phages could be isolated and used to lyse the wild-type hosts completely.

103 I 1 I I I I I I 0 10 20 30 40 50 60 70

Time ( d

Fig. 3. Cyanobacteria-cyanophage interactions in chemostats. (a) PIectonema boryanum plus LPP-DUN1 ; (b) Aphanothece stagnina plus AS-1 ; 0, cyanobacteria; 0, phage. (Modified from Barnet et al. 1981).

I I i 0 10 20 30

Time ( d )

Fig. 4. fnteraction of 0. wild-type Plectonema boryanum and 0, mutant phage. Dilution rate 0.034. (Modified from Barnet Y Z a/. 198 1 ) .

Algal blooms

I-

8

2 lo4-

0

C c e

10'-

181s

I 0

to9 c

I 1 I I 10 20 30 40 I 03t,

Time ( d 1 Fig. 6. The effect of particulate material (0.01% w/v) on the lysis of Plectonema boryanum by cyanophage LPP-DUN1 (0, without and 0, with particulate material). Modifed from Barnet et al. 1984).

182s M . J . Daft et al. TabIe 2. Degree of cyanobacterial lysis induced by virus infection measured as percentage change in

optical density at 665 nm after 24 h

Temperature ( C)

Virus Host 18 22 25 37 43

LPP DUN1 Plecronema horjanum - 13.9 -24.4 -56.9 f 3 0 . 6 f8 .33 Aph-1 DUN Apltanothece stagnina - 12.2 -31.4 -694 -27-5 -30.6 AS DUN Anacystrs nidulans -40.6 -68.7 -40.6 f137.5 f75.0

For each host and cyanophage system there is an optimum temperature range (Table 2). Lysis is inhibited at 37' C for PlectonemalLPP-DUN1 but not for Aphanotheca stagnina/Aph-1 where lysis continues above 43-C. The third system, Anacystis nidulans/AS DUN has the lowest temperature optimum (22'C). These results probably reflect the source of the cyanophages, i.e. Scotland and India.

Another factor that may play an important role in the survival of cyanobacteria in nature is the protective nature of silt. Silt appears to reduce lysis of the cyanobacteria. How effective this process can be is shown in Fig. 5 from the data of Barnet er al. (1984). The normal oscillations discussed earlier are damped down, delayed or even lost when infected cells are continuously cultured (Fig. 6 ) in the presence of silt.

4.2 Bacteria

Bacteria that lyse cyanobacteria exhibit several modes of attack. The Myxobacter 44 isolated by Stewart & Brown (1969) produces a number of extracellular enzymes which may break down the cell wall of the host. It is perhaps questionable if this type of lysis is significant in nature as the enzymes released by the bacterium would become diluted in the water very rapidly and their activities lost. A much more efficient mechanism for predation is found in the Myxococcus first isolated by Burnham et cri. (1981). The colonial spherules entrap the cyanobacterial prey and then lyse the cells by the release of a '1ysozyme'-like enzyme. This entrapment confines the prey and the lytic enzymes are not lost to the environment. Lysozyme production is limited by the quantity of combined nitrogen in the medium. Using continuous cultures we have found that supplying a tryptone-based medium at the rate of 40 mlih gave lysozyme activities three times that of cultures supplied at the rate of 10 ml/h. This could indicate that the lytic eficiency of the Myxococcus may increase in denser blooms of cyanobacteria. On the other hand these predators can also be effective at dilute inoculum levels. Starting from an initial absorbance at 630 nm of 0.5 the addition of M . fuluus (lo5 cells/ml) to Phvrrnidium luridum reduced the absorbance to 0.1 within 2 d. The cyanobacterium then showed fluctuations between 0.25 and 0.1 over a period of 32 d. Repeated inoculation of P. luridum (lo6 cells,ml) with a 1 % (vjv) inoculum showed that there was no loss in potential of the predator. The unique entrapment and lytic efficiencies over a long period at high and low prey densities make these My.xococcus species potentially very good control agents for cyanobacteria in situ.

Another interesting feature of these bacteria is their range of morphology. We found that the bacteria have a great tendency to adhere to the surface of the culture vessel producing long 'feathery' growths. These growths were also efficient in entraping and lysing P. luridum added to the culture pot. By modifying the culture conditions we were able to grow the M.fuluus on glass beads contained within a glass tube. Additions of P. luridicm to these columns showed that the bacterium was still an effjcjent l y t k agent. This type of attached growth may be similar to that which is common in flowing water. Any free-floating bacteria or cyanobacteria could act as a source of food after entrapment.

The contact mechanism for lysis of cyanobacteria, possessed by the Lysobacter (Christensen & Cook 1978) and the CP isolates of Daft & Stewart (1971) is another method that conserves the active lytic compounds. No tytic extracellular products are produced by the CP isolates but within 20 min of establishing contact the host cell is disrupted (Daft & Stewart 1973) presumably by the transfer of enzymes across the adjacent cell walls. The establishment of the contact between prey and predator depends on the movement of the medium and on the relative concentrations of each micro-organism.

Algal blooms 183s CP-1, when added at concentrations of lo6 and 103/ml to cultures of Nostoc ellipsosporum, caused lysis within 50 and 100 min, respectively. No detectable lysis took place in comparable cultures containing only 10 CP-1 cells/ml. Surface material surrounding the bacterium may assist in the establishment of the contact as Daft & Stewart (1971) found that acetylene reduction rates were reduced immediately unwashed cells were added to a N . ellipsosporum culture, whereas washed cells of CP-1 took 8 h before there was a fall off in this physiological activity.

It appears that more than one enzymatic system is involved in lysis of cyanobacteria by CP-1. By producing a cell-free extract of CP-1, Daft & Browning (unpublished) found that in combination with ethylenediamine tetra-acetic acid (EDTA) cyanobacteria were lysed rapidly and this lysis could be inhibited by the addition of calcium ions. Presumably the calcium ions chelated with the EDTA making it unreactive. An explanation of these results may be that the EDTA acts as a solvent for part of the cell wall of the host and enzymes from within the CP-1 cells are then able to bring about complete lysis. Paradoxically ecological studies on the distribution of CP-1 type bacteria and bloom- forming cyanobacteria show a positive correlation. This was clearly shown by Stewart & Daft (1975) at the reservoir in Port Talbot when high concentrations of Microcystis aeruginosa were detected along with high numbers of plaque forming units, most of which were identified as types of CP-1. Two factors may be significant here. Firstly, high concentrations of cyanobacteria tend to reduce the oxygen levels and the CP isolates are highly aerobic organisms, this would reduce their lytic func- tions. Secondly, cyanobacteria release many compounds into the aquatic habitat, some of which are toxic to other organisms yet others can sustain all the growth requirements of associated bacteria. This is the case for the CP type of bacteria. Fallowfield (1981) found that acetate, glutamic acid, histidine, asparagine, cysteine, tryptophan and arginine are the minimum growth requirements for CP-1 and all of these compounds are ‘leaked’ by cyanobacteria (Fogg & Nalewajko 1963; Fog 1966). Hence the CP isolates can utilize compounds released into the medium after the prey cell has been lysed or from extracellular products of the potential prey. These two abilities make CP-1 a parasite, assuming contact is made between the two cells, or, a saprophyte. This suggests close co-evolution.

4.3 AMOEBAE

Some protoza can control the abundance of planktonic algae in lakes. Canter & Lund (1968) found that within 7-14 d more than 99% of a bloom can be reduced by protozoans. Centric diatoms provide food for Asterocaelum algophilum, a trophic amoeba that produces cysts and resting cysts (Canter 1973). Yamamoto (1981) has isolated algophorus amoeba in Japan and also in Scotland (Yamamoto & Daft, unpublished). These amoebae belong to the genera Nuclearia and Acantha- moeba, respectively, and are very efficient in reducing cyanobacterial numbers. As with several other predators the rate of prey consumption depends on temperature and the type of prey. The generation times of each amoeba depend on temperature and the consumed prey and this is shown in Table 3. Initially at 5°C and with Phormidium luridum as the prey, the generation time for both species was between 2 and 3 times greater than when Anabaenajlos-aquae was the sole prey. At the highest temperature tested (24°C) the generation times were similar against each prey species although the Japanese isolate reproduced 3 to 4 times more rapidly than the Scottish isolate. In small field

Table 3. Generation times in hours of two amoebae grown at various temperatures and with two cyanobacteria as prey

Amoebae and code

Nuclearia sp. Acanthamoeba (4-1) castellanii (ph-2)

Origin Japan Scotland Temperature (“C) 5 11 24 5 17 24 Generation time (h) when prey is

Phormidium luridum 132 56 17 310 85 82 Anabaena Jos-aquae 43 26 22 166 72 13

1845 M . J . Daft et al. experiments, using Phormrdium luridum as the host, the Japanese Nuclearia sp. reduced the optical density of the cyanobacterium by 84Oh and the two Scottish Acanthamoeba species (pH-2 and pH-4) by 74 and 64%, respectively. This experiment was done during July over 6 d with a water tem- perature of 15’C. Continuous laboratory cultures showed a constant decline in the cyanobacterial population with no recovery phases. Such a prey/predator relationship is attractive because genetic variations in the host probably would not influence the ingestion of the cyanobacteria by the amoebae.

4.4 A C T I N O M Y C E T E S

Since the early work of Safferman & Morris (1963) on actinomycetes that are antagonistic towards cyanobacteria few detailed studies have been made. Al-Tai (1982), working in Dundee, found that out of 25 different isolates cultured from Iraqi soil, 25 were active against cyanobacteria, 14 against green algae, 63 against Gram-negative and Gram-positive bacteria and 32 against fungi. One isolate, coded An,,. is particularly effective and the active compounds are released into the medium. This pro- duction of extracellular lytic compounds limits the suitability of these micro-organisms as control agents. Some recent work by Burnham & Daft (unpublished), however, has indicated the possibilities of growing actinomycetes within the colonies of Myxococcus spp. and hence combining the properties of both organisms. By this approach multiple colonies could be developed against a range of nui- sance micro-organisms.

4.5 F U N G I

The spring blooms do not appear to be susceptible to virus or amoeboid predation. The Chytridia- ceous fungi, however, are very specific in their host ranges (Canter & Lund 1953). Most plankton diatoms are infected : Asterionella by Rhizophidium, Chytriomyces, Zygorhizidium and Septosperma; Melosira by Zygorhizidium and Septosperma: and Tabellaria by Chytridium. These parasites appear to be obligate and difficulties in their large-scale culture would make their application to the control of wild diatom blooms doubtful Septate fungi have been described by Redhead & Wright (1980), which produce antibiotics inhibitory to Anabaena Jos-aquae. During a survey of the reservoir at Farmoor near Oxford a similar type of fungus was isolated that lysed 10/12 cyanobacteria (Daft 1981). The lytic activity was associated with extracellular products, however, after subculturing several times the fungus became non-lytic. Even attempts to culture it on cyanobacteria failed to restore its original anti-microbial activity.

5. Discussion

The input to our freshwater systems of nutrients that enhance the growth of primary producers can be controlled if suflicient resources are made available. Farm practices could be monitored and outdated sewage works brought up to an acceptable level of efficiency. One of the best examples of discharge control is the improvement in the water quality and aquatic life of the River Thames (Gameson & Wheeler 1977). It is probabie, however, that large growths of algae and cyanobacteria will remain a problem for many years to come. Their noxious odours, tastes and production of toxic compounds make them a topic for concern. Hence it is worthwhile to speculate on how to manipu- late their natural pathogens with a view to achieving some degree of control. We have discussed some characteristics of several predators and how they act on their specific or general prey.

Table 4 lists some attributes suggested by Huffaker et al. (1976) and others by ourselves that would make an organism a good predator. Micro-organisms that bring about lysis by means of extracellular products appear to be the least attractive. These products may not be released as a specific response to the prey and the dilution factor in the habitat would lessen their effectiveness. Actinomycetes do produce colonies in liquid culture with radiating hyphae that make them fairly eficient in trapping cyanobacteria. The chytrids are potent pathogens of only certain groups and they cannot be cultured outside the host. In having the ability to lyse cyanobacteria, but only after making firm contact, and

Algal blooms 185s Table 4. A comparison of some attributes possessed by six group of agents that predate on bloom-forming

micro-organisms

Predators

Lower Agents producing fungi extracellular

Attributes Amoebae Cyanophages Myxococci Lysobacter Chytrids products

Adaptability to variations in physical conditions + + + - + + + + + + -

Ability to search or trap + + + + + + + + + + + + multiply + + + + + + + + + + + + + + +

Prey consumption + + + + + + + + + + + + + prey densities + + + + + + +

Wide host range + + + + + + + + + + + + + changes in the host + + + + + + + + + +. Good.

+ +, Fair. +, Poor. -, Not known.

Capacity and ability to

Ability to survive low - - -

Ability to respond to - - -

able to utilize only extracellular products from the cyanobacteria (Fallowfield 1981) the Lysobacter occupy an intermediate position. The cyanophages have a high potential in controlling cyano- bacteria. Unfortunately the numbers available for exploitation are limited but never the less they are easy to mutate and they have rapid rates of multiplication. Both amoebae and the myxococci have the most positive attributes. Care must be taken with some amoebae because they may be pathogenic to man, but the myxococci, with their range of morphological forms and unique entrapment system, need a great deal more investigation so that they can be fully evaluated.

6. Conclusions

In general, primary production is governed by the availability of nutrients. These are added to bodies of water by off water run, domestic and agricultural wastes. The mass culture of primary producers, which results in bloom formation, also provides conditions favourable for exploitation by a wide range of pathogens. Viruses, fungi, actinomycetes, bacteria and amoebae all have the potential for controlling the development of bloom-forming micro-organisms. The various ways in which these pathogens predate on the primary producers has been described along with some experiments that indicate their relative efficiencies. From such studies it may be possible to manipulate the balance between prey and predator in order that development of large concentrations of the primary pro- ducers are reduced to acceptable levels.

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BURNHAM, J.C., COLLART, S.A. & HIGHISON, B.W. 1981 Entrapment and lysis of the cyanobacterium Phormidium luridum by aqueous cultures of Myx- ococcus xanthus PC02. Archives of Microbiology

BURNHAM, J.C., COLLART, S.A. & DAFT, M.J. 1984 Myxococcal predation of the cyanobacterium Phor- midium luridum in aqueous environments. Archiues ofMicrobiology 137, 220-225.

BRADLEY, D.E. 1967 Ultrastructure of bacteriophages and bacteriocins. Bacteriological Reviews 31, 23C 314.

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t86S M . J . Daft et al. CANTER, H.M. 1973 A new primative protozoan

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CANTER. H.M. & LUND, J.W.G. 1953 Studies on plankton parasites. 1 1 . The parasitism of diatoms with special reference to lakes in the English Lake District. Transactions of the British Mycological Society 36, 13-37.

CANTER, H.M. & LUND, J.G.W. 1968 The importance of protozoa in controlling the abundance of plank- tonic algae in lakes. Proceedings of the Linnean

CHKISTENSEN, P. & COOK, F.D. 1978 Lysobacter, a new genus of nonfruiting, gliding bacteria with high base ratio. International Journal of Systematic Bac- teriology 28, 367-393.

COOK, W.L. & AHEARN, D.G. 1976 Natural control of Anobaena blooms by the amoebe Asterocaelum ana- baenophilum sp. nov. Distributional history of the biota of the Southern Appalachian. IV Algae and fungi. ed. Packer, B.C. & Roane, M.K. Charlottsvil- le: University Press of Virginia.

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