0 The Incidence of Fairy Ring Turf Grass Disease On Fine Turf in the UK

1. Introduction

Fairy Ring disease is probably one of the best known of all turf grass diseases. It has been causing problems to greenkeepers, groundsmen and gardeners for many years. In STRI journals (1929 and onwards) and other turf management books and publications this disease is regularly discussed and recommendations given for control. However, it is well known that fairy rings are extremely difficult to control and most treatments meet with very little success.

This paper looks at why Fairy rings are difficult to control and the latest recommendations for attempting control in the 1990s. It also investigates associated fairy ring disease symptoms and the turf management problems that they cause.

2. Fairy Ring Fungi

Fairy rings belong to a large group of fungi known as Basidiomycetes. Basidiomycetes are fungi that produce their sexual spores; called basidiospores on a club shaped or tubula spore-producing structure called a basidium. The STRI (York, C. 1998) state that there are numerous fungi that have been recorded as causing fairy rings. Smiley (1987) states that there are more than 60 species of basidiomycete-type fungi that can individually cause turf disease. The fact that there are many different species is one of the main reasons why Fairy rings are difficult to control chemically.

Fungi primarily colonise thatch at the turf base and/or organic matter within the soil. One of the main symptoms of Fairy ring disease is rings of stimulated grass growth. These rings are a result of nitrogen released in the soil by the Fairy rings activity underground, where they are breaking down organic matter to release ammonia, which is processed by soil micro-organisms into nitrates. Sometimes stimulated grass growth is not noted, in these circumstances rings of mushrooms or toadstalls are present. Irregular patches of stimulated grass growth or patches of dead or shrivelled grass have also been associated with Fairy ring fungal activity.

3. Disease Cycle

It is not known whether Fairy rings are initiated by the proliferation of a piece of fungus mycelium or by the germination of a basidiospore produced in the basidiocarp. Attempts to produce fairy rings under experimental conditions have all failed (Smiley1987). It is known that the fungus begins active growth in the soil or thatch and grows radially outwards.
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The initial appearance of the Fairy ring is usually a small ring or arc of stimulated grass or just a cluster of basidiocarps, at this stage the type of fairy ring is difficult to identify. The diameter of the ring may enlarge annually by a few centimetres or by as much as 0.5m. Fairy rings are basically saprophytic living on dead organic matter in the thatch layers or in the soil. It therefore does not cause injury to turf directly, although Vargas (1994) states that some research shows that Type 1 fungi can penetrate cortical cells on grass roots indicating possible parasitic activity. The following looks at the various different Fairy rings in more detail.

4. Fairy Ring Groups

Fairy ring diseases can be classed into two groups: Endaphitic and Lectophilic. Endaphitic fungi primarily colonise the soil, whereas lectophilic primarily colonise thatch and leaf litter. Endaphic fungi can extend mycelia 2 to 3 feet deep in the soil. Lectophilic fungi are associated with superficial fairy ring and thatch degradation.

4.1. Endaphitic Fungi

Type 1

Type 1 Fairy rings are caused by the fungus - Marasmius oreades - The disease typically appears as a ring of dead or stressed turf, bordered on both the inner and outer edges by a band of stimulated grass growth. New rings can appear just as green 'patches'. The fungus can be seen by taking a soil sample from the leading edge of the ring - it has a characteristic 'musty' smell.

Apart from a direct toxic affect on the grass plant (hydrogen cyanide has been detected at the leading edge of type 1 rings) it is thought that the cause of turf death could also be due to mycelium within the soil, coating the soil particles with waxy deposits creating hydrophobic conditions, which in turn leads to lack of available water (Smiley 1987). This physical condition of the soil reduces the chances of effective chemical control of the fungus due to the fact that the applied spray cannot actually reach its target due to the hydrophobic condition; this situation is similar for all fairy ring fungi.

Annual meadow grass (Poa annua) can be severely affected by all types of fairy ring (especially type 1) due to the shallow rooted nature of the species. The deeper-rooted grasses such as Bent (Agrostis spp.) and Fescue (Festuca spp.) are better able to sustain growth in hydrophobic conditions due to their more comprehensive root systems.

The Type 1 ring is prevalent in hot and dry conditions, which indicates that soil moisture may play a part in the development of the fungi. The STRI turf grass Bulletin (spring 1996) stated that we may need to look at 'turf coolants' in the future rather than fungicides!

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Type 2

Many different types of fungi are associated with the cause of Type 2 Fairy ring, these include: Agaricus spp. and Lycoperdon spp. Rings of stimulated grass growth are seen normally without fruiting bodies.

It is rare that excessive damge is caused to the turf, although the stimulated growth obviously affects the playing quality of the affected surface. Lush grass growth can also encourage secondary infection such as Fusarium patch (Microdochium nivale). Symptoms are normally seen during the summer and autumn.

Type 2 Fairy ring on cricket table.

Type 3

The STRI state (York 1998) that Type 3 rings are made by many different types of Basidiomycete - including: Hygrophorus spp. And Psilocybe spp. There are no distinct affects on the turf grass except when the fruiting bodies are present (normally during the autumn) when they form rings of toadstools or puffballs (basidiocarps). This obviously will affect the quality of a sports surface.

4.2 Lectophilic fungi

It is probably this group of fungi that are seen as a greater threat to fine turf quality than the previous group, and occurrence seems to be on the increase (STRI 1998)!

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Superficial Fairy Ring

Superficial fairy rings are regularly seen in the summer and autumn. There are a large number of non-sporing basidiomycete fungi capable of producing superficial fairy rings such as Coprinus spp.

Symptoms include: rings, arcs, or ribbons of pale yellow grass. If the thatch layers of the infected areas are investigated, fungal mycelium is normally present and has a distinct characteristic musty smell. Turf around the affected area can sometimes show stimulated growth as mycelium breaks down organic matter to release readily available nitrogen. Apart from stimulated growth, surface conditions are not severely affected, although aesthetically the surfaces are not normally acceptable on golf or bowling greens etc. However, Annual meadow grass can be severely affected due to the shallow rooted nature of the species. In this situation the deeper-rooted grasses such as Bent (Agrostis spp.) and Fescue (Festuca spp.) are better able to sustain growth in hydrophobic conditions due to their more comprehensive root systems.

Thatch Collapse

An associated symptom is sometimes seen on fine turf known as Thatch collapse or 'Elephants Foot'. It normally occurs on older surfaces such as golf and bowling greens, where a deep thatch layer has built up. As the Basidiomycete mycelium within the thatch layer breaks down the organic matter, irregular patches of turf become 'sunken' or depressed.

This is due to the organic material being broken down and therefore physically removed, thus causing a depression in the turf surface. The author has observed this phenomenon on many golf and bowling greens and it causes severe disruption to the quality of the surface. See photograph below.

5. Dry Patch

It is difficult to ascertain which group of Fairy ring; Dry Patch is associated with. Until recently Dry Patch was not officially connected with fungal activity. For many years 'Dry Patch' on fine turf areas such as golf greens was thought to be purely the result of dry weather and grass stress caused by heavy play. In the summer patches of dry, shrivelled or dead grass are regularly witnessed on golf courses and bowling greens up and down the country (see picture below). However, recent research has shown that Dry patch may be primarily caused by basidiomycete fungi (STRI 1992 and 1993).

Research carried out by Baldwin and York (1993) set out to ascertain the difference between drought stress symptoms and Dry Patch symptoms. They concluded that fungal mycelium was certainly implicated with the Dry patch phenomenon, although conclusive evidence was difficult to ascertain due to the lack of mycelium within the patch (unlike Type 1 Fairy ring where mycelium is present throughout the ring). However, mycelium is present at the interface of the outer part of the patch and the unaffected turf.
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It was surmised that as mycelium moves through the soil it leaves a waxy residue (similar to that described earlier for Marasmius oreades) which creates the hydrophobic soil. They also found that in a survey of golf courses Dry Patch was found to be most prevalent where various different types of fairy ring fungi also proliferated.

Dry Patch symptoms on a golf green.

6. Discussion.

From my experience of visiting various sports grounds and golf courses, it would appear that Endaphitic groups of Fairy ring were not considered to be a significant problem for turf managers. However, I feel that this is really only because these problems are occurring fairly infrequently. When they do occur especially on surfaces such as cricket wickets and bowling greens the Type 1 Fairy ring is seen as the biggest problem. This is due to the fact that turf is killed and the surface is severely disrupted.

Types 2 and 3 are invariable ignored by groundsman or masked with the use of fertilisers or application of sulphate of iron to disguise the different colour of the ring. Type 2 rings can cause problems on cricket wickets, as the lush grass can cause erratic bounce and therefore possible injury to the player. The lush grass can also encourage secondary fungal diseases such as Fusarium patch (Microdochium nivale).

As already stated the Lectophillic group of fungi are on the increase (STRI 1998) and this is a cause for concern for many greenkeepers. The symptoms caused by Thatch Collapse and Dry Patch can be quite devastating and have a long term impact on the quality of turf once it has been affected.
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7. Control

The turf manager should have a thorough understanding of conditions, which favour a particular disease attack, once this area is understood it helps the turf manager to prevent attack in the first place or help to predict likely attacks. The manager should also be able to correctly identify the particular disease and understand how it affects the turf quality in order to carry out the most appropriate type of management. Environmental concerns about chemical safety and persistence, increasingly mean that fungicides (all pesticides) used to control disease development have been subject of close scrutiny over recent years and will continue to be so as European directives try to harmonise the use (or not) of chemicals throughout the EC.

Integrated Pest Management (IPM) programs are frequently talked about now days and turf managers are starting to actively adopt this type of approach to managing disease problems on turf. Whatever the disease, it's development on turf should be managed using all appropriate methods of control. An IPM approach to turf management will consider the following methods of control: cultural, genetic, biological and chemical. One, some or all may be needed for control.

7.1 Cultural Control

The cultural practice recommended most often (Vargas 1994) is fertilisation with nitrogen to stimulate growth of the surrounding grass so that it will mask the grass ring stimulated by the Fairy ring, sulphate of iron can also be used. Another method is to try and drown fairy rings by soaking them for up to 48 hours, although very little success has been achieved using this method.

A wetting agent is sometimes added to the water to try and help break down surface tensions that exist in the soil and waxy deposits created by the fungi. Wetting agents come under the group of chemicals known as Adjuvents. They are not classed as pesticides and there is considerable misunderstanding over the extent to which they are legally controlled under the Food and Environment Protection Act. An adjuvent is described as 'a substance other than water which enhances the effectiveness of a pesticide with which it is mixed' (BCPC 1999). However, this does not apply in this situation as it is used independently to help re wet the soil, effectively making watering more efficient. Scotts Aquanova wetting agent can be used in this situation.

Probably the most effective way of treating Endaphitic Fairy ring is to 'dig' them out (Vargas 1994), although once again rings that have been dug out tend to come back in the same place some time after. For Lectophilic Fairy ring - reducing the thatch layer may help, as this reduces the food source, although this group of fungi are often found in well managed, low thatch level turf.

7.2 Genetic Control

Any given grass cultivar will have a certain genetic make up which will determine all of the grass characteristics, including its resistance to attack by certain pathogens.

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Since Fairy ring fungi are basically saprophytic, the concept of resistant cultivars is unfortunately not applicable at this stage. It is worth noting that the deeper rooting grasses such as Fescue and Bent are better able to withstand attack due to their deeper root system.

7.3 Biological

All living organisms have the potential of being predated by other living organisms. Biological control simply means the use of one living organism to control another. In other areas of horticulture such as under glass grower's etc. biological control has been used for many years, especially to control pests such as Whitefly and Aphid. In turf biological control has not been widely used. However, in recent years more companies such as Symbio have been marketing so called biological disease control agents for use on turf. No such products are available for use on Fairy rings yet but research is continuing especially in America.

Fidanza (1999) states that 'mixing' the soil of the infected area promotes a natural antagonism that is known to exist among fairy rings'. Fairy rings have been known to dissipate when they intersect each other. Maybe this is the area that needs investigating in order to find a natural solution to this problem.

7.4 Chemical

The section on chemical control is stated last to indicate that chemicals should only be used once everything else has been tried or considered. Chemicals do play an important part of an IPM program, although with current environmental and safety issues paramount and strict legislation that now exists, chemicals should only be used as a last resort in order to limit disease activity to acceptable levels.

Approved Chemicals

At the moment there are only two chemicals approved for use on turf to control Fairy Ring, these are Ringmaster - RP Amenity (Ai. Oxycarboxin) and Fairy Ring Destroyer - Vitax (Ai. Triforine).

Oxycarboxin is a systemic carboxamide fungicide. Triforine is also systemic fungicide.

These fungicides have a systemic action. Systemic fungicides are generally translocated through the grass plants vascular system acropetally, although some fungicides are both acropetal and basipetal in action. However, due to the fact that Fairy ring fungi are saprophytic and most of the damage to turf is caused indirectly (eg. hydrophobic soil etc. - see earlier) these fungicides will have limited effect.

The use of wetting agents was discussed earlier for helping water penetration into the affected areas.

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8. Legislation Concerning Pesticides

Before application of any pesticide, application procedures should be fully understood and appropriate qualifications to apply chemicals should be held.

Legislation concerning pesticides should also be fully understood; regulations and relevant procedures should be implemented to ensure the safe use of chemicals. Stated below is a summary of the relevant legislation:

a) The Food and Environment Protection Act 1985 (FEPA)

FEPA came into force on 5th September 1985 and statutory powers to control pesticides are contained within part iii of the Act. Section 16 of the Act describes the intention of controls as being:

'Protect the health of human beings, creatures and plants; safeguard the environment; secure, safe, efficient and humane methods of controlling pests; and to make information about pesticides available to public'.

b) Control of Pesticide Regulations 1986 (COPR)

Control of pesticides is achieved by COPR, which lay down the approvals required before any pesticide may be sold, stored, supplied, advertised or used, and allow for the general requirements set out in the various consents, which specify the conditions subject to which approval is given. Consent A relates to advertisement, Consent B relates to sale, supply and storage, Consent C(i) to use and Consent C(ii) to aerial application of pesticides. The conditions of the Consents may be changed from time to time. Up to date details can be found in Pesticides 1999 which is revised annually, these details are up dated in the monthly publication - The Pesticides Monitor incorporating the Pesticides Register.

c) The Authorisation Directive

European Council Directive 91/414/EEC, known as the Authorisation Directive is intended to harmonise national arrangements for the authorisation of plant production products within the European Union. It became effective on the 23rd July 1993. Under the provision of the Directive, individual member states will be responsible for authorisation within their own territory of products containing active substances that appear in a list agreed at community level. This list, to be known as Annex 1, will be created over a period of time by review of existing active ingredients and the authorisation of new ones. The process of reviewing existing active ingredients is scheduled to be completed by 2003. In the UK requirements to meet the new Directive have been achieved by a series of Plant Protection Products Regulations (PPPR), under which, over a period of time, all agricultural and horticultural pesticides will come to be regulated. Meanwhile existing product approvals are being maintained under COPR, and new ones are granted for products containing active ingredients already on the market by the 25th July 1993.

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Products containing new active substances not on the market at this date may be granted provisional approval under PPPR in advance of Annex 1 listing of their active ingredients.

d) Control of Substances Hazardous to Health Regulations (COSHH)

The COSHH regulations, which came in to force on 1st October 1989, were made under the Health and Safety at Work Act 1974 and are an important means of regulating the use of pesticides. COSSH regulations apply to a wide range of pesticides used at work and they lay down essential requirements and a step by step approach for the control of explosive to hazardous substances. Substances hazardous to health include those labelled very toxic, harmful, irritant or corrosive and substances with occupational exposure limits. They also include harmful micro - organisms, substantial quantities of dust and any material, mixture, or compound used at work, or arising from work activities, which can harm people's health.

The original Regulations, together with all subsequent amendments, have been consolidated in to a single set of regulations: Control of Substances Hazardous to Health Regulations 1994 (1994).

The basic principle underlying the COSHH regulations is that the risks associated with the use of any substance hazardous to health must be assessed before it is used and the appropriate measures taken to control the risk. COSHH assessment forms can be found in the Appendices. These forms show the typical risk assessments that have to be carried out as part of the COSHH assessment on a golf course.

e) Additional Legislation

To assist the compliance with the above legislation the turf manager or grower can obtain Codes of Practice produced by the government. These are the MAFF Codes of Practice for suppliers of pesticides to agriculture, horticulture and forestry (Yellow code) and the MAFF/HSE Code of Practice for the safe use of pesticides on farms and holdings (Green code). A Code of Practice (Orange code) also exists for use in industrial and amenity areas. The Yellow and Green codes are government 'Approved' the Orange Code is only an industry code.

9. Conclusion

Vargas (1994) states that 'turf managers should learn to live with Fairy rings as there are no affective treatments for their eradication'. As we have seen Fairy rings are difficult to control, although in some circumstances Fairy ring activity is totally unacceptable due to the detrimental affect on the turf surface, if the turf manager does not respond to this problem they would not be doing their job properly!

At the moment there are no suitable chemical treatments due to the unique way that Fairy rings affect the turf surface. The fact that most of the damage caused to turf is indirect obviously reduces the affect that systemic fungicides will have on the particular pathogen.
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If contact fungicides were available they may be more effective, however, due to the fact that Endaphytic fungi survive deep into the soil, this makes targeting very difficult. Also, most fungi produce waxy residues, which produce hydrophobic conditions, which inhibit water movement in the affected area.

At the moment cultural methods for control are proving to be the most affective, especially for turf areas affected by Lectophilic types of fungi. Treatments such as masking symptom can be affective. Thatch reduction is especially important, as it will help to reduce the organic matter, which the fungi feed on.

In conjunction with aeration techniques wetting agents are useful products to help water penetrate hydrophobic soil, although recent research (Scotts 1997) has shown that some of these products contain harmful 'Estrogens'. If wetting agents are used products should only be used that have bee shown to be environmentally friendly such as Scotts 'Aquanova'.

Research is currently being carried out (GCSA 1999) to investigate the use of beneficial fungi to inhibit Fairy ring activity, although because there are so many different species responsible for causing damage it is difficult to see how a useable treatment could be formulated.

It is difficult to ascertain why Lectophilic fungal attacks are on the increase (STRI 1998), although it could be down to the fact that there is more pressure on fine turf surfaces than ever before. For example, there have never been so many people playing golf. This is undoubtedly putting stress on the turf grass surfaces and this could explain the increase in diseases such as Thatch collapse and Dry patch. It could also be down to the fact that broad spectrum, non specific fungicides such as Mersil (Mercury based) are no longer available. These fungicides may have controlled Fairy ring fungi.

The above conclusions show how important it is to fully understand how and why a specific turf grass disease affects the turf surface and to consider all forms of control (to acceptable levels) for the disease rather than just responding to attack by reaching for a chemical.
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