A review is presented on the occurrence and role of cyanobacteria and eukaryotic algae in sports turf, especially golf curses, and on the problems arising when ...
Journalof Applied Phycology 4: 39-47, 1992. ( 1992 Kluwer Academic Publishers. Printed in Belgium.
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Cyanobacteria and eukaryotic algae in sports turf and amenity grasslands: a review N.A. Baldwin ' & B.A. Whitton 2 ' Sports Turf Research Institute, Bingley, West Yorkshire BD16 IA U, UK 2 Department of Biological Sciences, University of Durham, South Road, Durham DHI 3LE, UK Received 1 September 1991; revised 11 October 1991; accepted 29 October 1991
Key words: cyanobacteria, Phormidium, eukaryotic algae, Cylindrocystis, sports turf, golf course, black layer
Abstract A review is presented on the occurrence and role of cyanobacteria and eukaryotic algae in sports turf, especially golf curses, and on the problems arising when these organisms become abundant. The literature depends largely on observations in only a few countries, mainly Canada, New Zealand, U.K. and U.S.A., but problem growths are probably widespread. The genera reported to be conspicuous at times include Nostoc, Phormidium, Coccomyxa, Cosmarium, Cylindrocystis, Klebsormidium, Mesotaenium and Zygogonium. Conspicuous surface growths are probably most often related to unsatisfactory drainage or irrigation practices, but other factors such as fertilizer treatment (especially excess ammonium sulphate) have been implicated. These surface growths sometimes incorporate copious mucilaginous 'slime', which can be a serious hazard by causing people to slip. U.K. observations suggest that this is especially likely under acidic conditions, where Coccomyxa, Cylindrocystis and Mesotaenium are among the probable culprits. Some literature indicates that cyanobacteria are also associated with a subsurface black layer, which can cause serious problems for turf management where sandy soils are subject to unsatisfactory drainage. It seems likely, however, that cyanobacteria are largely, if not entirely, absent from the subsurface layer, but may form a dark layer at the turf surface overlying the position of the subsurface black layer. The dark surface layer is probably due largely to narrow filamentous cyanobacteria, whose growth may enhance the poor drainage and thus reinforce the conditions favouring the black subsurface layer associated with anoxic conditions. The soil algal vegetation of sports turf may also be expected to exhibit beneficial effects known to occur in soils of other types of community, such as nitrogen fixation by some cyanobacteria and the binding of particles. However, little study on such effects has been directed specifically to sports turf. Introduction Eukaryotic algae are probably ubiquitous in soils (Metting, 1988) and cyanobacteria have been recorded from most soils which are not highly
acidic. In grassland communities they are typically a relatively minor component of the ecosystem. There are nevertheless many comments about algae and algal nuisances in the sports turf literature. These are mostly short notes written by
40 people concerned with turf management and there are almost no accounts by phycologists. The aim of the present review is to bring together and assess the scattered information. For simplicity, the term alga is used for cyanobacteria as well as eukaryotic algae, since growths often contain both groups and many authors fail to distinguish which are present. There are a number of records for natural or semi-natural grassland communities of visually obvious algal growths on the soil surface, such as with Zygogonium ericetorum on acid soils (West & Fritsch, 1927) and cyanobacteria (mainly Nostoc) at a late stage in old-field succession on prairie soils (Booth, 1941). They can also sometimes occur attached to the lower parts of grass stems, as with N. commune var. flagelliforme (Whitton et al., 1979). In well maintained lawns, sports turf and other types of amenity grassland, where the sward is dense and growing vigorously, algae are seldom visually obvious, though they may occasionally be so in wet tropical regions. At least in temperate regions the organisms do not occur in sufficient abundance to cause problems and consequently, in many situations, are considered of little practical concern. However, under conditions of poor grass growth, where the sward has thin or bare areas, algae may cause problems with respect to visual attractiveness and, in the case of sports turf, the playing qualities of the sward. Free-living algae are of course not the only organisms that can occur in such conditions, because thin areas may also favour growth of lichens, moss protonema or leafy shoots and some weed species. The conditions of poor drainage, low fertility and sometimes also acidity, which often favour turf colonization by algae, also promote the development of moss, lichens and dicotyledonous weeds (Dawson, 1968). Thus conditions which favour algae may also enhance competition from these other plant groups. Three types of problem have been reported, the formation of a surface 'scum' due to abundant algal growths, production of copious mucilaginous 'slime' and possibly also the hindrance of water infiltration through the turf profile by what is commonly referred to as a 'black layer' (see
below). Clearly the first two categories often overlap, but their recognition by sports turf managers reflects the fact that algal growths may or may not include species which produce mucilage of a type and amount to cause a risk of people slipping on them. This review describes the symptoms of turf colonization by eukaryotic algae and/or cyanobacteria, the conditions which favour their occurrence and current turf management practices recommended for control. The literature on soil algae (e.g. Metting, 1988) indicates that soil algae can also have important beneficial effects on higher plant vegetation, including grasses (see below), though few studies have sought to quantify these effects for sports turf. Conversely, the prairie grass Aristida oligantha is apparently inhibitory to some cyanobacteria (Parks & Rice, 1969).
Algae recorded in sports turf and amenity grassland Problems associated with algae in turf are mentioned briefly in many texts dealing with general turf management (e.g. Dawson, 1968; de Thabrew, 1972; Beard, 1973; Evans, 1988, 1991) and texts relating to pests, weed or disease management in turfgrass (e.g. Shirtleff etal., 1987; Smiley, 1983; Baldwin, 1990). However, only a few studies have identified the causal algae present. Among the cyanobacteria, several reports mention Nostoc spp. (probably mostly forms of N. commune) as being abundant and problematic (Greenfield, 1962; Dawson, 1968; Shildrick, 1990). Oscillatoria (probably a range of narrow filamentous cyanobacteria) has been recorded as a slime-producer on U.S.A. golf green (Hodges, 1987a,b). In a study of slime-producing algae in six turf areas on four sites in northern England, six genera of green algae were recorded (Baldwin, 1988): Cosmarium, Cylindrocystis, Dactylothece, Klebsormidium, Mesotaenium, Ourococcus. All except Klebsormidium and Ourococcus can produce copious mucilage (Bourrelly, 1966); Klebsormidium, which is perhaps the most widely distributed of all filamentous terrestrial green algae, is fre-
41 quently present in algal associations dominated by other genera.
Conditions which favour algal colonization of turf It is generally accepted that algal colonization of turf is an indication of unsatisfactory cultural conditions for turf maintenance (Sprague, 1976; Baldwin, 1989b). Whilst there have been few experimental studies on the relationships between cultural and environmental conditions in the turf and colonization by algae, many observations have been recorded concerning the conditions which favour their development. Algae generally occur where there are bare areas in the turf (Musser, 1962; Beard, 1973; Vengris & Torello, 1982; Daniel & Freeborg, 1979; Baldwin, 1988; Shildrick, 1990) or the sward is thin and weak (Beard, 1973; Beard, 1975a; Shiels, 1984). A major factor in algal colonization of turf is water status. Problems due to algae occur where the turf surface is wet (Smiley, 1983) or waterlogged (New Zealand Turf Culture Institute, 1961; Beard, 1973, 1975a; Daniel & Freeborg, 1979; Sports Turf Research Institute, 1983), poorly drained (Voroney & Marcille, 1987) or flooded (Beard, 1973, 1975a). Several workers have suggested reasons for the association between surface wetness and colonization by algae. There include situations where there is poor grass growth and the drying rate is slow due to shading from sunlight (Daniel & Freeborg, 1979; Smith & Parchan, 1986; Porter, 1987; Baldwin, 1989a), shelter from the wind, i.e. poor air movement over the turf surface (Baldwin, 1989a) and continuous downpour of water droplets from overhanging trees (Pycroft, 1980). In the U.K. it has been observed (Baldwin, 1987, 1988, 1990) that the colonization of turf by algae often occurs on sloping ground, particularly on golf course fairways. This is due presumably to excess surface water running across the turf surface rather than downwards through the soil profile. It has also been suggested that algal colonization of the turf surface is favoured by high levels of sunlight (Beard, 1975a) and cold (i.e. winter) conditions
(Sports Turf Research Institute, 1983). Soil compaction is also known to favour problems due to algae, partly due to adverse effects on overall turfgrass growth and also to poor water infiltration through compact turf areas (Wise, 1961; Dawson, 1968; Crockett, 1978; Pycroft, 1980; Baldwin, 1988). The role of soil fertility in algal development in turf has been studied briefly by several workers as part of turfgrass nutrition trials. Beard (1975a) states that high soil fertility favours colonization, especially if organic fertilizers are applied (Madison, 1971). However, this is contradicted by Decker and Decker (1988), who state that algal colonization of turf is favoured by low fertility conditions. In a field trial comparing N sources for turfgrass in New Zealand, Robinson (1980) found that a low application rate of ammonium sulphate (240 kg ha- yr - ' N) led to the development of algal slime. No slime was produced in plots fertilized with other N sources (urea, calcium ammonium nitrate). Whilst the untreated control contained high amounts of algae, plots treated with sulphur at application rates between 56 and 224 kg ha- ' yr- remained free of 'black' algae during the trial. Inhibition of black algae by elemental sulphur has also been recorded by Goss et al. (1977). Soil pH also has an effect on colonization (Waddington, 1969). In a recent fertilizer trial on a pure sand rootzone at the Sports Turf Research Institute, the application of acidifying fertilizer (ammonium sulphate) treatments lowered rootzone pH to 4.2 which led to the production of a thin sward (Lawson, pers. comm.). Markedly acidic rootzones have led to a deterioration of ground cover and sward quality (Colclough & Canaway, 1989). In this trial highly acidic turf was colonized by slime-producing algae, whereas less acidic turf with a dense sward showed no visually obvious algal community. This community consisted almost entirely of green algae and was dominated by Coccomyxa and Cylindrocystis (authors, unpublished). In field trials evaluating experimental fungicides for disease control, it has been observed that certain treatments may increase the development of
42 algae in the sward (Dernoeden & Kackley, 1983; Dernoeden & Fry, 1985; Parish et al., 1986). No explanation for this phenomenon was presented.
Nitrogen fixation by algae in turf and other grass communities The occurrence of visually obvious growths of the nitrogen-fixer Nostoc in some turfs suggests that cyanobacterial nitrogen fixation may sometimes make a quantitatively important contribution to the nitrogen economy, but quantitative data appear to be lacking. Sheets or colonies of freeliving Nostoc are probably most frequent on calcareous soils, but also occur on other soils in at least some types of grassland. For instance, a cyanobacterial community dominated by Nostoc formed a 32% cover between bunches of grass at a late stage in prairie old-field succession (Booth, 1941). Cyanobacteria on leaf scales of moss under tall fescue (Festuca arundinacea)have also been
suggested to contribute to fixed nitrogen (Giddens, 1982) and laboratory studies (Reddy & Giddens, 1981) have indicated that this may be due to a close Nostoc - moss relationship. How-
ever, a domestic lawn in South Africa with a cyanobacterial community dominated by Phormidium spp. did not show (Jones, 1977) evidence of nitrogen fixation (acetylene reducing activity).
Symptoms of turf colonization by algae Algae may cause problems in turf at any time of the year, but they are recorded most frequently during wet winter weather. The symptoms have been described generally as scum, slime or black surface layer; colours range from green through brown to black, or sometimes blue-green for Nostoc (Dawson, 1968). Unidentified algal 'scum' or 'slime' have been described in many colours including green (Beard, 1975a; Shildrick, 1990), dark green (New Zealand Turf Culture Institute, 1963), green-brown (Shirtleff etal., 1987) and black (Baldwin, 1987). The failure to identify in each individual report the organisms responsible
makes it difficult to identify causal algae from visual symptoms only, although cyanobacteria or Zygogonium probably play an important role in most dark 'scums' on the surface. Wet 'scum' have a sticky (Wise, 1961) or rubbery (Daniel & Freeborg, 1979) texture. When dry, it may form a parchment-like crust (Beard, 1975a; Decker & Decker, 1988), which later may crack, peel and loosen from the soil (Shirtleff & Randall, 1978). 'Slimes' have been described as a gelatinous layer (Pycroft, 1980) or mass (Baldwin, 1990) or jelly resembling frog spawn (Sports Turf Research Institute, 1983). Greenkeepers commonly refer to the problem as 'squidge', alluding to the sound made when turf colonized is walked upon. Black layer, sometimes referred to as black plug layer, is a turf condition affecting golf greens constructed with a rootzone consisting predominantly of sand. Affected turf areas turn bronze in colour and generally thin out (Hodges, 1987a, 1987b). A core taken from an affected area reveals the black layer, a zone of stagnant material through which grass roots do not penetrate (Smith, 1990). Although not always providing supporting evidence, a number of researchers have suggested that algae are at least partially responsible for black layer formation (Scott, 1986; Chaltas, 1987; Woehrle, 1988), because they have been observed to be present as a dark surface crust on turf areas affected by the black layer below the surface (Berndt & Vargas, 1987a, 1987b). It has been suggested (Kershasky, 1987) that organic substances such as mucilage produced by algae bind sand particles together and fill pore spaces, thus reducing water infiltration through the turf profile. Algae have also been implicated (Hall, 1987) in that dead algae trapped in the turf profile may lead to the formation of false water tables, leading to waterlogging and thus anoxic conditions. Another possible explanation (Weeds, Trees and Turf, 1987) is that algae may attach themself to the calcareous sand sometimes used in golf green construction, creating a layer which anaerobic bacteria may use. The most convincing explanation for the black layer is that it is an impermeable layer formed by
43 bacterial (Pseudomonasand Actinobacter)growths (Lindenback & Cullimore, 1989; D. R. Lindenback pers. comm. to H. B. Couch), that anoxic conditions may occur in the vicinity of the layer and that the colouration is largely due to metallic sulphides (Berndt et al., 1989); under extreme conditions the anoxic layer may reach to the surface. Cyanobacteria may be abundant at or just below the surface layer. Cyanobacterial isolates from a core with an underlying black layer made by C. F. Hodges and sent to B. A. Whitton were Oscillatoria, Lyngbya and Phormidium. Growths of these cyanobacteria often appear very dark, so might also get called a black layer. Experiments with sand columns (Hodges, 1989) have shown that the development of a surface cyanobacterial community can subsequently be followed by the formation of a subsurface anoxic black layer. It seems likely, however, that in nature the bacterial layer usually develops first. Nevertheless, the surface cyanobacterial community might enhance the conditions favouring the black plug layer beneath the surface. In spite of the numerous reports and comments during the 1980s about black layer, there is still a need for detailed studies on the chemical and microbial features during the development of the layer. It would be useful to compare the processes involved with those occurring in certain intertidal sand communities which also show a marked vertical zonation from surface cyanobacteria down to anoxic bacteria (see Whitton & Potts, 1982; Cohen & Rosenberg, 1989).
Problems caused by algae To date, there has been no recorded case of direct parasitism by algae on a species of turfgrass; algae affect the overall turf surface indirectly. The scum algae have been implicated in sealing the turf surface mechanically (Beard, 1973), which excludes soil moisture (Musser, 1962) and generally reduces water infiltration and percolation rates through the turf profile (Beard, 1973). Although not dealing with turf, experimental studies of clogging by Phormidium mats in groundwater recharge basins in Israel (Katznelson, 1989)
appear to provide the only experimental information on factors influencing infiltration through algal mats. Infiltration was found to be reduced when cyanobacterial mats were not allowed to dry thoroughly between floodings. Dense surface growths of algae (Madison, 1971) can not only reduce infiltration, but also soil aeration (Beard, 1973). In drier weather, when a surface crust is formed, this may smother the turfgrasses (New Zealand Turf Culture Institute, 1963), creating a barrier through which grass shoots cannot penetrate. Other reported effects of scum formation are yellowing of the grass, which Madison (1971) suggested was probably due to iron chlorosis or the production of root toxins. Slime-producing algae produce mucilage, which blocks air spaces and leads to black layer formation, as described above. The slime makes the turf surface very slippery, which presents a hazard to those walking on it (Baldwin, 1990). The green 'speed' may also be affected i.e. rolling distance of the ball and thus have a direct effect on the playing quality of the turf surface.
Control of algae in turf Algal control in domestic lawns and sports turf has been the subject of many general articles (e.g. Sports Turf Research Institute, 1983; Smith & Parchan, 1986; Lefton, 1988), some being specifically on chemical control (e.g. Ashburn, 1985; Hartman & Williams, 1976). It has been recognized that long-term control or alleviation of problems caused by algae may only be achieved by rectifying the conditions which favour their development (Baldwin, 1989a). Before deploying a chemical control method it is thus necessary to determine the underlying cause (Decker & Decker, 1988). Chemical control methods give only temporary alleviation of the problem (Decker & Decker, 1988). The spread of algae on the turf surface may be limited by cleaning mowers and other mechanical equipment (New Zealand Turf Culture Institute, 1961). However, the most effective control methods for algae forming a surface scum or slime are
44 usually based on improvements in the relationship between water and the turf surface. Rapid removal of surface water may be achieved by improving overall drainage (New Zealand Turf Culture Institute, 1961; Escritt, 1978; Decker & Decker, 1988), particularly by unblocking drains if this is the cause of surface wetness (Decker & Decker, 1988). Changes in the turf irrigation schedule may also be necessary (Daniel & Freeborg, 1979). In situations where water is moving across a sloping surface rather than downwards through the turf profile then mechanical surface aeration by splitting or spiking may be effective (New Zealand Turf Culture Institute, 1961). The application of hydrated lime as a desiccant may also dry the turf surface (Daniel & Freeborg, 1979). The removal of shade trees may also reduce the severity of the problem (Beard, 1975b). If a severe slime or scum problem occurs, the initial treatment is often to break up the surface scum by raking or, in the case of slime, removing excessive material by brushing (Baldwin, 1989a). These operations remove the smothering effect of the algae on the sward and in the case of the slime problem allow the operation of aeration machinery on what was previously a hazardous, slippery surface (Baldwin, 1989a). Surface top dressing (Daniel & Freeborg, 1979), particularly with a coarse sand (Baldwin, 1988), may also help to create a drier turf surface. Many publications on turf maintenance recommend chemical control of algae (e.g. Dawson, 1968; Beard, 1973) and this has also been the subject of many articles (e.g. New Zealand Turf Culture Institute, 1961, 1963; Sports Turf Research Institute, 1983). In only very few cases, however, are advice and recommendations on choice of chemical and application rate based on the findings of field experimentation. In fertilizer trials several authors have observed that treatment with elemental sulphur inhibited algal growth (Brauen etal., 1975; Goss etal., 1977; Rieke & McElroy, 1986). Hydrated lime has been recommended, applied either as a desiccant or to raise the surface pH (Wise, 1961; Pycroft, 1980; Vengris & Torello, 1982; Decker & Decker, 1988). There are widespread recommendations for the
use of toxic chemicals for algal control in turf, but most are based solely on the experience of greenkeepers and groundsmen. In trials on a golf course fairway in the U.K., a range of chemicals were evaluated for control of slime-producing algae (Baldwin, 1988). Repeated applications of ferrous sulphate, cresylic acid or dichlorophen gave some control of 'squidge' in replicated trials, although marked turf scorch was noticed in plots treated with ferrous sulphate or cresylic acid. Control of slime-producing algae with dichlorphen has also been reported for New Zealand (Evans, 1984). Several fungicides have been suggested as also possessing algicidal activities, including thiram (New Zealand Turf Culture Institute, 1961), manganese-based fungicides (Daniel & Frebourg, 1979), lawn sand (Crockett, 1978) and chlorothalonil (Dernoden & Kackley, 1983). In New Zealand potassium permanganate has also been recommended (New Zealand Turf Culture Institute, 1961), as has sodium hypochlorite in the U.S.A. (Madison, 1971), although these proved ineffective in U.K. field trials (Baldwin, 1987). The two most widely recommended chemicals for control of algae in turf are ferrous sulphate and copper sulphate. The former is commonly and routinely applied to turf for various beneficial effects such as moss control and improvement of turf colour, but has also been reported as a control for algae (Dawson, 1960, 1968; Escritt, 1978; Pycroft, 1980; Shiels, 1984; DiPaola, 1990; Shildrick, 1990). Copper sulphate, although not applied to turf for any other purpose, is recommended widely for control of both algal slimes and scums in turf (Dawson, 1960; Wise, 1961; Beard, 1975b; Sprague, 1976; Crockett, 1978; Escritt, 1978; Pycroft, 1980; Shiels, 1984; Rieke & McElroy, 1986; Decker & Decker, 1988; DiPaola, 1990), this being an extrapolation of its use for control of algae (especially cyanobacteria) in ornamental waterbodies. Discussion In view of the sparse taxonomic information about the organisms causing particular examples
45 of nuisance, it is worth considering the organisms likely to be involved and the implications for control measures. At least 125 genera have been identified from soil (Metting, 1981), including (in decreasing order of importance) Chlorophyta, cyanobacteria, Bacillariophyta, Xanthophyta, Euglenophyta and Rhodophyta. There is a huge literature, including an important component in Russian, yet the lack of detailed experimental studies makes it difficult to assess this literature critically. Many of the micro-algae require cultural studies for identification and even then may be difficult to name. The widespread filamentous algae growing on the soil surface have probably often been misidentified; confusion between Klebsormidium and Ulothrix and between Mougeotia and narrow forms of Zygogonium are especially likely. At least in temperate regions, relatively few species are likely to be the main cause of turf problems, but other species can become associated with the mucilaginous masses and it may not always be clear on casual inspection which are the organisms really responsible for the nuisance. Although they do not produce abundant mucilage on soils, filamentous green algae can produce mats detachable as a whole. These can become very conspicuous in the case of Zygogonium ericetorum, but only at pH values (
