Chemical and Biological Control of Mushroom Pests and Diseases

Efficacy

The fungicide Sporgon containing prochloraz-manganese is the one almost universally used by Irish growers. Tests were done in conjunction with disease inoculation trials to determine the efficacy of this fungicide for control of Bubble disease (Verticillium fungicola) and Cobweb (Cladobotryum dendroides). Sporgon application by incorporation in the casing or by drench after casing gave little protection when high inoculum levels were incorporated in the casing. Incorporation of the fungicide in the casing gave good protection from low levels of inoculum applied after casing. Sporgon applied as a drench (1.2 g/m² in 1.8 litres of water) after casing gave protection for a time but disease began to appear in the third flush. This shows that the simple use of fungicides alone will not be sufficient to obtain good disease control. It is extremely important for mushroom growers to ensure that they use clean (pathogen free) casing and that they have a very good programme of hygiene after casing.

Tolerance

In 1994 a serious outbreak of cobweb disease was reported from some areas. It was particularly bad with growers in western counties. An investigation was done to determine whether (a) strains of Cladobotryum dendroides had developed which were tolerant to the fungicides benomyl and prochloraz, commonly used for control. (b) whether more aggressive strains of the fungus had developed. Disease samples were sent to Kinsealy, from various parts of the country, by Teagasc advisers. Isolations of the pathogen were made on to malt agar and discs from these were transferred to agar containing 10 mg/l of either benomyl or prochloraz. After four days growth at 22^oC measurements of the radial growth of the fungus were made. When significant growth occurred sample was deemed tolerant (Table 1).

Table 1: Survey of fungicide tolerance in Cladobotryum dendroides samples causing cobweb disease in mushrooms.

* Variable numbers of samples per county were received per county

The above and numerous other samples tested in succeeding years indicated that the development of tolerance to the fungicides was closely related to the frequency of use of the fungicides. The carbendazim based fungicides (benomyl) were very prone to this.

Where the use of approved fungicide with different active ingredients was rotated then tolerance was slow to develop, if at all. Thus occasional rotation of carbendazim with prochloraz or chlorthalonil would prevent the development of tolerant strains.

Phytotoxic effects

The fungicide Sporgon (prochloraz-manganese) is by far the most commonly used and most effective fungicide in mushroom growing. Growers often comment that they feel that applications of this fungicide may reduce yield. A series of trials were done to determine whether various rates of the fungicide applied either as a drench or incorporated in the casing may have phytotoxic effects on mushrooms. Only the highest rate of incorporation i.e. 9.6 g/m² significantly reduced yield by comparison with untreated. This is eight times the recommended rate. This shows that the fungicide has no phytotoxic effect at normal rates.

Time from inoculation to disease

Experiments were done to test the effect of time and method of inoculation, of the pathogens Verticillium fungicola and Cladobotryum dendroides, on the development of bubble and cobweb diseases respectively, during cropping. Natural inoculum from diseased mushrooms and casing was used.

Inoculum put on the surface of compost, in bags, either at spawning or after spawn-run compost did not result in subsequent disease development. This indicates that spawned compost is unlikely to be a source of either of these diseases.

Application of inoculum to the casing by incorporation or surface application resulted in very rapid disease development. Bubble disease (Verticillium fungicola) developed when mushroom pinheads were formed on the casing in an 8 to 12 day period after casing. Development of cobweb was slower and it generally took 10 - 14 days for it to appear. The level of inoculum used in these trials was quite high and it may be that where a low level of natural inoculation occurs disease development will take longer.

Pathogen survival

Studies were done to determine the survival time of Verticillium fungicola inoculum. A mixture of spores and ground up mycelium were placed in distilled water and stored at room temperature. A sample was plated on malt agar every week from this. The pathogen was still alive after six months.

Disease spread

The epidemiology of the common mushroom diseases was studied on a number of mushroom units both big and small. This was done by means of spore trapping on agar strips, stationary agar plates with selective media and by swabbing structures, equipment and personnel. In addition close observations of procedures and practices in mushroom units were made to determine the major sources of risk. Factors identified are presented here in a cropping sequential format:

Pre-cropping

It is clear from our work that attention to detail at this stage will ensure that disease and pest levels start from a very low base and kept under control with minimal pesticide usage. Very strict hygiene and the adoption of good practice are the key factors at this stage:

• Personnel free of contamination. Anyone coming in contact in any way with a new crop, including filling, lining out and casing, must be free of the possibility of carrying disease spores or insects. A shower or bath plus the donning of freshly washed clothing is the ideal.
• Minimise dust. Dust arising from wind outside or by sweeping dry concrete inside or outside is a possible source of disease spores and must be avoided.
• Minimal bag levelling, by transferring compost from bag to bag, and the use of cacing (spawn-run material) will reduce the spread of compost green mould in particular.
• Protect casing from any possible source of disease pathogens. This includes peat extraction from bogs and subsequent handling by casing companies. Growers receiving a load of casing should cover it unless it is being used immediately.
• Fly control from an early stage. The use of fly monitoring equipment (Figure 1) has been found very beneficial as it rationalises the use of pesticide fumigants. It was clear from our studies that flies (Sciarid and Phorid) were gaining access to commercial production tunnels earlier than hitherto supposed. Also it was commonly found that a large fly population coincided with a disease epidemic. Verticillium, Trichoderma and Cladobotryum were isolated from tunnels in which these occurred.
• Many growers were found to be in the habit of leaving doors open unnecessarily. This negates the benefit of otherwise good practices.

During cropping

In this study it was found that in most cases disease starts at a very low level and then becomes an epidemic by the end of the third or fourth flush. The following factors were identified:

• Detect diseases and pests early. This requires a grower to carefully inspect the tunnel each day for the first signs of disease and pest and to take prompt appropriate action. If removing a patch or piece of disease drape a damp cloth over the affected area and then lift it into a container with liquid. Otherwise spores are released resulting in rapid disease spread. The area can then be covered with salt.
• Mushroom stumps must be bagged and removed shortly after harvest. This also includes mushrooms which fall between bags.
• People moving between tunnels are a serious source of disease spread. We have found by swabbing that disease pathogens are easily carried on hands and clothing. This is usually done unconsciously as the pathogens are microscopic. Pathogens can even be carried to canteen facilities such as tables and chairs which then act as a source of inoculum.
• A major source of inoculum, for disease spread, was identified as crops being kept too long before disposal. Some growers with a fair amount of disease in the third flush tend to keep the crop for a fourth. Usually by the time of disposal there is a huge level of disease, which creates a large inoculum source, that poses an enormous threat to other crops. Diseased crops should be killed off and disposed of immediately after taking the third flush.

After cropping

Our studies have demonstrated that the method of emptying and cleaning out tunnels and of spent compost disposal plays a major role in determining the level of disease in mushroom units. This is particularly so for bubble and cobweb diseases. The following is a logical sequence, with comments, based on findings from our studies.

Procedures

1. KILLING OFF THE BAG SURFACE
   If there is some disease present, the normal procedure is to apply a strong disinfectant to the surface of the bag to kill off surface spores and mycelium. A good drenching spray is required. It must be remembered that this will only kill to a small depth and that there will be an enormous amount of disease inoculum underneath in the casing and compost. Emptying the bag in the unit will therefore release a large amount of disease spores into the air thus undoing the benefit of the disinfectant.
2. VENTILATE
   The tunnel must be cleared of disinfectant fumes before anyone enters to load bags. Failure to do this presents a serious health hazard.
3. LOAD BAG WITHOUT DISTURBANCE
   Ideally bags should be loaded on to a trailer without disturbance of the compost or casing. Emptying bags at this stage or outside in the yard creates a very serious disease hazard, which is difficult to overcome.
4. CLOSE AIR INTAKES
   When any tunnel is being emptied the air intakes and the doors on the rest of the tunnels in the unit should be firmly closed. This will reduce the risk of spores entering clean tunnels.
5. TAKE LOADS DOWNWIND OR COVER DURING TRANSPORT
   Trailer loads of used bags of compost should be taken downwind if at all possible, but this may not be practical. If so the load should be covered with a tarpaulin or sheet of plastic. Driving upwind with an uncovered load of bags with disease will result in a large shower of spores being blown back over the entire unit.
6. CLEANING OUT A TUNNEL
   When the bags are removed the remaining dirt on the floor must be brushed out. Dampen the floor before brushing to ensure that a cloud of dust and spores are not sent into the air. Power hosing - while good for cleaning concrete does not kill spores and may spread them.
7. DISINFECTING TUNNELS
   The floors and walls of the cleaned out empty tunnel should then be sprayed with one of the approved disinfectants such as Formalin or one of the phenolics (Sudol, Environ, Prophyl, Panacide). This will kill any spores or mycelium remaining. If there has been any significant amount of disease in the tunnel then fumigation with formaldehyde is advisable. This will kill any spores in the ventilation duct or radiator or on the fan blades. The air temperature should be raised to over 15^oC and the relative humidity above 50 % with the fan on full recirculation to ensure efficient fumigation.
8. VENTILATE BEFORE ENTRY
   All fumes must be cleared from the tunnel before anyone enters, to avoid a serious health hazard. The controls should be located outside so that ventilation can take place without having to enter a tunnel full of fumes.
9. DISINFECT EQUIPMENT
   Any piece of equipment, which has been used in a tunnel with disease, must be thoroughly disinfected before the new crop is started. This includes hoses, roses, trays, brushes, knives etc.
10. CLEAN PERSONNEL
    Anyone involved in cleaning out a tunnel with disease will be covered with disease spores, including clothes, hair, hands, shoes etc. Such persons must shower and have a complete change of clothes before coming in contact with other crops.

Biological controls

• Steinernema feltiae, an insect parasitic eelworm is one of the most promising non-chemical controls for mushroom flies. It is sold as "Nemasys", "Stealth" or "Entonem". Several experiments with S. feltiae indicated that it gave 60-70% sciarid control when added to the casing. It is less effective against phorids.
• Differences in the level of control given by different commercial brands of S. feltiae were not significant.
• Applying S. feltiae by casing incorporation, as a post-casing drench or either of these treatments augmented by an additional drench treatment one week later did not improve the level of control they achieved.
• Occasional failure of S. feltiae to give any control of sciarids has been attributed to poor quality control by the manufacturer.
• Good exclusion of flies from the growing house improves the performance of S. feltiae.
• Bacillus thuringiensis var israelensis ("Bactimos"), a strain of an insect bacterial disease specific to flies, gave poor control of sciarids and did not augment the effectiveness of S. feltiae.
• Neen seed extract (contains azadirachtin) gave poor control of sciarids and did not augment the effectiveness of S. feltiae.
• Hypoaspis miles, a mite that feeds on the larval stages of all the mushroom pests was assessed for sciarid control. When introduced after spawning it reduced sciarid numbers by 48%: when introduced after both spawning and casing it reduced sciarid numbers by 60-65%.

Cultural Controls

The impact of cultural methods of control on insect populations was monitored on an ongoing basis throughout the duration of the project. The most important of these are:

• Hygiene - precrop cleaning and disinfection of growing tunnels, outside apron, utensils and containers is an important aspect of cecid and tarsenemid mite control. In fact such measures are the only steps one can take to avoid such pests. Discarding severely infested crops prematurely is an integral part of good farm hygiene.
• Exclusion of flying insects - this is a most important aspect of fly control in mushroom houses. Air inlets should be fitted with a mesh with apertures not greater than 0.5-0.6mm. Doors should be seated against an intact rubber seal, like that of a commercial refrigerator. It is important to keep doors closed insofar as possible, particularly during spawn run.
• Quick transport of spawned compost to the house avoids exposing it to egglaying by sciarids and phorids.
• Regulation of human traffic between crops (allowing only traffic from young to old crops) helps to reduce pest problems.
• Regulating house temperature to achieve a quick spawn provides competition for pests for resources in their ecological niche.
• Reducing the production cycle to reduce the potential for pest build-up can be a very useful pest suppression tool-terminate severely infested crops early.
• Pest problems increase with increasing size of the mushroom farm; the biggest problems arise when a number of growers share the same site.
• Using traps to monitor fly numbers increases growers' awareness of low fly populations. Low fly populations especially during spawn run are of major importance as they give rise to the initial infestation which culminates in the high populations that occur later in the cropping cycle and result in economic injury. The Pennsylvania black light trap is highly suitable for monitoring mushroom pests.
• It is also important to continually check crops for pests, determine the extent of the problem, treat as appropriate and evaluate the effect of the treatment.
• If pesticides must be used, use the most appropriate one, apply evenly, apply at the correct dosage, the right time and under the right conditions.
• Avoid routine use of pesticides during times of the year when the pest pressure is low e.g. winter and early spring.