Introduction

Black spot is the most important disease of apples and causes substantial crop losses if it is not prevented. The disease is caused by the fungus Venturia inaequalis and is commonly known as apple scab rather than black spot outside of Australia and New Zealand. This fungus infects only apples (different fungi cause black spot of pears and roses), so the spores that cause infection only come from diseased apple trees. Figure 1 shows the life cycle of the black spot fungus. The fungus produces two types of spores, ascospores and conidia. Ascospores develop during winter on dead, fallen leaves that were infected the previous season and they are released into the air by rain from the time of bud burst in spring. Conidia are only produced on living tissue and they cause the build-up of disease during the growing season and cause most of the disease damage to the apple crop.

Fig. 1. Life cycle of the black spot fungus (Agrios, 1969).

The weak point in the black spot disease cycle occurs in spring when the fungus has to become established on the new season's leaves and fruit. This stage is called primary infection and in most situations primary infection is caused only by ascospores. Conidia can sometimes survive through the winter in infected buds, in twig cankers, or on old apple fruit that remain attached to the trees. If this occurs, primary infection can also be caused by conidia. Disease becomes visible on leaves or fruit 2-3 weeks after infection. As soon as lesions appear, conidia are produced and can cause secondary infections during wet weather. Successful black spot management relies on minimising primary infection in spring. To achieve this it is necessary to identify sources of primary inoculum and to understand when, and how, they are likely to be a problem.

Primary infection from ascospores

Management of fallen leaves

Ascospores are produced in the leaf litter during winter and early spring as a result of the sexual reproductive stage of the fungus. The numbers of ascospores produced depend on the amount of disease on leaves at leaf fall and the amount of leaf litter left by the time the spring period of ascospore discharge occurs. In the past "clean up" fungicides have been applied in the autumn, around leaf fall. Benomyl was once widely used for this purpose. This is not recommended for black spot control because fungicide use at the time when sexual reproduction occurs increases the potential for selection of fungicide resistant strains of the pathogen. Autumn benlate applications may have contributed to the rapid emergence of resistance to this fungicide.

Fig. 2. Typical patterns of ascospore release and leaf litter breakdown.

Research carried out over 20 years ago demonstrated that spray application of urea either to leaves just prior to leaf fall, or to leaves on the ground, greatly reduced the numbers of ascospores produced. Urea acts directly as a fungicide against black spot and it increases leaf nitrogen which delays development of the sexual stage of the fungus and encourages microorganisms to break down the leaves more rapidly. Over 90% reductions in ascospore numbers have been demonstrated with 5% urea (5 kg/100 litres) sprayed onto the foliage at about 5% leaf fall. Urea applications to help black spot management are strongly recommended in situations where application of autumn nitrogen does not interfere with the management of tree nutrition.

Ascospore release patterns

The black spot fungus can only produce a limited number of ascospores in a season and not all of these will be mature at once. A typical seasonal pattern of ascospore release is shown in Figure 2. Only a few ascospores will be mature at bud break and numbers peak within a period about ten days either side of full bloom, around the first week in October. In normal seasons, no more spores will be produced after early December. However, in dry seasons maturation can be delayed and ascospores may still be present in early January.

The risk of infection by ascospores depends on the numbers of spores released. When spore maturation is at its peak enormous numbers of ascospores can be released into the air during rain. In excess of 50% of the total numbers of spores available in a season could be released in a single period of rain if temperatures are above about 12^oC and spores have had several days of warm humid weather without rain in which to mature.

When they are mature the ascospores are actively discharged into the air in response to the following environmental stimuli:

1. Leaf litter has to be wetted by at least 0.1mm of rain (discharge peaks with rainfalls in excess of 0.25mm of rain). However, if the surface of the leaves becomes flooded by water to a depth of more than about 0.1mm spore discharge will virtually stop.

2. Leaf litter has to be exposed to light. If leaves become wet at night virtually no spore discharge will occur until day break.

3. Spore discharge is greater when the leaves have been exposed to warm temperatures (15-20 ^oC) or high relative humidities (90-100%) prior to wetting, than if they have been exposed to lower temperatures or relative humidities.

When combined, these factors result in most ascospores being discharged in response to day time rain, or when leaf litter remains wet during the day. Very few spores are discharged during night time rain or as a result of dew. Once they are discharged into the air the majority of spores travel only a few metres before they land and most primary infection will arise from spores that were released within an orchard. There is potential for some spores to be carried several kilometers and spores blowing in from other sources are most likely to be a threat during the period of peak spore release.

Numbers of ascospores in the orchard

Unfortunately, regardless of how good your disease control is, you must assume that there will be sufficient black spot in the orchard for some ascospores to be produced the following spring. Removal of leaf litter before spring seems an attractive idea as it would remove the source of ascospores from the orchard. Unfortunately, there is no way, has yet, to collect and dispose of the tonnes of leaf litter that are produced each season. An example of the amount of leaf litter, its rate of breakdown and the numbers of ascospores produced in an orchard is given in Figure 2. This orchard was seven years old and had a high level of black spot in the preceding season. The number of spores available for discharge in a major rainy period at the time of peak release would have been over 20 billion per hectare! By the end of November this figure had dropped to a mere 80 million per hectare.

As it takes only one spore to land in the right place to establish an infection, what difference is there between millions or billions of spores in an orchard? The answer is that the more ascospores there are present, the greater the chance that some will land on susceptible tissue and cause infection, and the more difficult the task will be for the spring fungicide programme to prevent infection. Any reduction in ascospore numbers will help disease control. HortResearch scientists are currently examining litter breakdown and ways of measuring numbers of ascospores. This will allow better management of leaf litter and allow the time that ascospore release begins in early spring to be determined. This way, fungicide use can be tailored to match the actual numbers of spores and use of unnecessary sprays can be avoided.

Weather and ascospore infection

Fig. 3. Wetness and temperature criteria describing black spot infection risk (Mills' periods).

Once ascospores are discharged they are carried by air currents until they are deposited on apple leaves or fruit. The spores germinate in film of water and once they have germinated they are vulnerable to desiccation until the fungus has actually penetrated the plant tissue and established an infection. The whole process of ascospore discharge, transport, deposition, germination and infection takes several hours, and parts of the process are strongly influenced by temperature.

Mills' periods, which were devised by William Mills in the USA in the 1940's, are the most commonly used infection criteria for black spot. They describe the duration of leaf wetness required at different temperatures for ascospores to establish infection. However, Mills was not aware that the black spot fungus requires light for ascosopre release; this was first demonstrated in New Zealand by Dr Peter Brook in the 1960's. With this in mind, a recent revision of Mills' criteria suggests that ascospores actually need up to three hours less leaf wetness for infection than Mills originally thought. In New Zealand four categories of infection risk are used (Fig. 3) which correspond with the currently accepted version of Mills' criteria. The Marginal category corresponds to the revised version of Mills' original criteria. Conidia require about the same wetness duration as the Marginal criteria for ascospores.

Conidia as primary inoculum

Some fruit remain on trees through the winter and may be a source of primary infection. Spray programmes are usually relaxed after harvest and remaining fruit frequently become infected with black spot. Conidia can be washed from fruit lesions onto susceptible tissue in spring. Because conidia are transported by rain splash, the risk of infection is reduced if diseased fruit are removed during winter and dropped to the ground. It is preferable to remove diseased fruit rather than rely on the use of autumn or winter fungicide applications because it is difficult to eradicate established disease with fungicides, and attempting to do so increases risk of fungicide resistance. It is also possible for conidia to overwinter as lesions on the previous season's wood or in buds, but in New Zealand this is not common. Conidia from these sources are likely to be a problem in susceptible varieties where there were high levels of black spot the previous season.

Black spot risk prediction

The monitoring of Mills' periods alerts growers to when infection has occurred. Even though the warnings are after the event, they can be used to predict black spot outbreaks because of the 2-3 week incubation period between the time infection occurs and the appearance of black spot symptoms. Successful use of infection period warnings for black spot management depends on use of curative fungicides, which for black spot are mostly of the DMI type. It is not possible to determine black spot infection periods by guesswork, and weather data with hourly time resolution are required.

HortResearch has developed a national network of electronic weather stations to monitor infection risk according to standardized criteria. The system is fully commercialized in some districts and is at an advanced stage of testing in others. Growers can buy access to weather stations nearest to their orchards and buy PC software to ring up the weather stations and to interpret black spot infection risk. In some districts daily facsimile reports on infection risk are available. The system will continue to be developed and improved for some time to come, but it already offers high quality hourly data with the full research back-up of HortResearch.

Weather forecasts are also an important part of black spot risk prediction and fungicide management. HortResearch has done several years of research with the New Zealand Meteorlogical Service on the development and use of black spot weather forecasts and these are proving to be a vital part of black spot management. Although forecasts of rain are not accurate enough to allow growers to only apply protectants when rain is predicted, forecasts of extended fine periods are accurate enough to safely delay some protectant applications that would otherwise be applied on a weekly basis. Obviously there is greatest scope for use of this approach in drier districts where extended fine periods occur frequently, such as Hawkes Bay, Canterbury and Otago. Black spot weather forecasts are being commercialized in several districts and HortResearch is involved in teaching growers how to make best use of them.

Fungicides and black spot control

The prevention of primary infection is crucial to effective black spot management. During the period of high infection risk (bloom) it is advisable to maintain a good protectant fungicide cover and to rely on the curative action of a DMI fungicide after an infection period has been monitored. Unfortunately the time of greatest fungicide need is also the time of russet sensitivity and of chemical thinning effects from fungicides like Thiram. In addition, New Zealand research has shown that over use of the dithiocarbamate fungicides (e.g. Polyram, Manzate, Mancozeb) can disrupt integrated mite control (IMC) programmes. To further complicate the situation, use of the DMI group of curative fungicides (e.g. Nustar, Rubigan, Systhane, Topas, Bayleton) has to be minimised to reduce the risks of pathogen resistance development.

Here are some rules that can be applied to help manage the compromise between obtaining black spot control, maintaining IMC, not russetting fruit, not inducing DMI resistance and not blowing the budget on chemicals:

1. DMI curatives need to be mixed with a protectant fungicide to help reduce risk of resistance. Even as mixtures, it is recommended that no more than four DMI applications are made each season. Given the expense of mixed applications and he restrictions on DMI use, protectant fungicides (which need to be applied before infection occurs) should form the basis of the black spot spray programme.

2. Protect mite predators by avoiding dithiocarbamate fungicides except from pink/early bloom to mid November, when russet sensitivity demands their use.

3. Every dithiocarbamate fungicide application made will increase the disruption of IMC. Do not just apply these protectant fungicides on a calendar schedule. Watch the weather forecasts and if you are confident that it is going to be fine delay application of protectants. The closer a protectant is applied prior to an infection period, the better its effect will be. Re-application of protectants by themselves straight after infection periods is pointless unless another infection period is anticipated immediately.

4. Access to monitored black spot infection period information will assist decisions as to whether or not curative fungicide applications are required.

5. Use of curative/protectant fungicide applications after an infection period should be limited to the time when large numbers of ascospores are likely to be present (mid September to late October).

6. Calcuation of curative fungicide "kickback" activity should be taken from the time that a wet period started. The sooner a curative is applied after an infection period, the better the curative effect is likely to be.

7. Ensure that sprayers are correctly calibrated and that adequate spray coverage is obtained even in the tops of trees.

In the event that infections do occur and sporulating lesions are visible on leaves and/or fruit there are four points to follow:

1. Avoid any further use of DMI fungicides, as application to established infections will encourage selection for fungicide resistance.

2. If russet risks are acceptable, apply two to three dodine sprays about a week apart to reduce spore production and hence the risk of new infections.

3. Maintain a regular protectant fungicide programme, e.g. captan, until pre-harvest.

4. Apply leaf fall urea sprays to reduce overwintering black spot and disease risk in the following season.

The Complete Black Spot Management System

HortResearch is currently researching many aspects of black spot management. Development of the national orchard weather station network has been accompanied by several years of fungicide spray timing experiments in Canterbury, Hawkes Bay and Otago. These trials have been conducted in both conventional and organic production systems. The results show that 20-50% reductions in fungicide use are possible, particularly in dry seasons, but that there is the risk of black spot control failure if mistakes are made in fungicide timing. High quality weather information is necessary and a thorough understanding of black spot biology and fungicide performance are also required before reductions in fungicide use can be attempted.

Developing ways of getting infection period warnings out to growers is HortResearch's top priority at the technology transfer end of this research. We have examined phone-in services in Hawkes Bay and Otago, radio broadcasts in Otago, daily fax messages in Canterbury, and sending information directly to growers' computers in Hawkes Bay. Software is now available from HortResearch for growers who have PC's to access weather stations directly and to determine infection risk for themselves. Monitoring ascospores so that information on the time that spore release starts in the spring, when it peaks, and how long it persists into the summer is also being investigated.

Ultimately we aim to integrate all the information known about black spot into a disease management system. Such a system will include:

1. Access to hourly weather data from electronic weather stations and daily weather forecasts.
2. Estimates of ascospore numbers and the time of peak, first, and last release.
3. Standard guidelines for assessing disease in the crop and appropriate guidelines for control actions.
4. Monitoring of fungicide resistance on individual properties with appropriate fungicide use recommendations.