Apple powdery mildew – additional information

Disease status

Powdery mildew is one of the most important diseases of apple in the UK.

All parts of the tree are affected, including fruits and it reduces yield and quality and repeated severe attacks gradually debilitate the tree.
On susceptible varieties, such as Cox, mildew levels of as little as 10% mildewed leaves per season are sufficient to significantly reduce yield and quality.
In the UK most commercial apple orchards receive routine sprays to control mildew.

Other hosts

Podosphaera leucotricha also attacks pear and quince.
There appears to be no host specialisation such that isolates from pear and quince also attack apple.

Distribution

Powdery mildew occurs wherever apples are grown, and is generally always a problem in tree nurseries.

However, economic loss from mildew varies with climatic conditions.
It is generally a serious disease in the UK, particularly the eastern part but usually less of a problem in the west.
Mildew is also not usually a serious problem in Europe, particularly in Northern Europe where the cold winters usually result in death of overwintering mildew.

Varietal susceptibility

Apple varieties vary in susceptibility to mildew.

Cox, Idared, Golden Delicious, Gala, Fiesta, Jonagold, Elstar are very susceptible.
Bramley, Worcester, Saturn are moderately susceptible and Discovery and Grenadier have very low susceptibility to mildew.
Susceptibility to mildew based on mildew incidence alone can be misleading, e.g. the incidence of mildew on Golden Delicious can be higher than on Cox.
However, Golden Delicious appears to be more tolerant of mildew than Cox and therefore the disease would have a much lower effect on yield and quality.
Such information, however, can only be obtained from crop loss studies conducted over several seasons.

Disease cycle and epidemiology

P. leucotricha is an obligate parasite that overwinters on apple as mycelium in dormant buds infected during the previous growing season.

Overwintering potential is limited primarily by temperature. In severe winters infected buds are killed as they are more susceptible to winter cold than healthy buds.
Temperatures near –12^oC can kill mildew mycelium in buds and leave them to emerge healthy.
In UK in recent years the mild winters generally mean that most mildewed buds survive to provide primary inoculum the following season.

Mildewed fruit buds emerge as primary blossom mildew at pink bud.

Conidia produced on this mycelium are spread by wind to initiate the new epidemic, to infect developing rosette leaves, flowers and bourse shoots.
At the end of flowering primary vegetative mildewed shoots emerge when terminal shoots start growth.
Conidia produced on this primary mildew initiate epidemics on the extension growth and start the secondary mildew epidemic which continues throughout the summer, as long as extension growth continues.
Young developing fruitlets may also be infected.
Leaves are susceptible when young and for only a few days after they emerge.
Conidia do not need free water on the leaf to germinate, but do require high humidity 96-100%, although germination can occur at relative humidities as low as 70%.
Optimum temperature is 20‑22^oC and germination is slow below 4-10^oC. Only limited germination occurs above 30^oC.

So, in the UK during summer, provided there is susceptible young leaf tissue, presence of mildew inoculum and it is not raining, every day is a mildew infection day.

Under ideal conditions the time from infection to sporulation is around 4-5 days.
Mildew can therefore build-up very rapidly in an orchard.
Infection of fruit buds takes place within a month of them being formed, before the bud scales suberise, usually in June.
The mycelium then remains quiescent in the bud until the following spring.
Terminal buds on extension shoots become infected at the end of the summer when extension growth ceases.
These remain susceptible to infection for longer than the fruit buds.

Occasionally the sexual state of P. leucotricha occurs as pin-head sized brown/black fruiting bodies among mycelium on infected shoots or leaves.

This form has rarely been observed in the UK in orchards and at present is thought to be unimportant in the perennation of the disease.

Symptoms and recognition

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Primary blossom mildew

Apple leaves, blossoms and fruit can be affected.

Primary blossom mildew

This emerges at pink bud.
Flowers are deformed with pale green or yellow petals and with petals and rosette leaves covered in white mycelium and spores.

Primary vegetative mildew

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Primary vegetative mildew

This emerges when extension growth starts.
These infected terminals are usually stunted, with small leaves also covered in mildew mycelium and spores).
In winter affected shoots appear as silvered shoots.

Secondary mildew

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Secondary mildew on leaf

On leaves infections appear first as whitish felt-like patches of fungal mycelium and spores, usually on the underside.
These lesions may appear as chlorotic spots on the upper leaf surface.
The leaf may also be distorted.
Badly affected leaves usually fall prematurely.
Young fruitlets are also susceptible to infection. Mildew appears on these as a fine network of mycelium resulting in net-like russet.
On some varieties white mycelium may also be obvious on fruit.

Other problems that may be confused with mildew

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Mildew russet on fruit

Mildew symptoms though not always easy to recognise, are fairly distinctive.

Fruit russet may be caused by other factors such as weather or chemicals.

Usually russet caused by mildew is distinguishable by its fine net-like appearance.

Disease monitoring and forecasting

Mildew is always present in the orchard and routine control measures are usually needed from around green cluster until vegetative growth ceases.

Monitoring mildew is essential to rationalise fungicide use and/or to check that control measures are effective, even in a routine fungicide programme, as it is very easy for the mildew incidence to increase unnoticed. Once primary mildew levels are high, achieving successful control is much more difficult.

Assessment of primary mildew

At pink bud stage the level of primary blossom mildew can be estimated by counting the number of infected and healthy blossoms on lengths of branches on at least 10 trees taken at random in the orchard.
The number of trees assessed is dependent on orchard size and time available.
Usually on each tree 10 blossoms are examined on each of four branches.
Record the percentage of mildewed blossom trusses and categorise:

Categories of primary mildew blossoms or shoots

Low = ≤ 0.5%

Moderate = 0.5 – 2.0%

High = >2.0%

At petal fall the incidence of primary vegetative mildew is assessed on emerging terminal buds.

First approximately count the number of new extension shoots on each of a few representative trees in the orchard and calculate the mean number of extension shoots per tree.
Then on at least 10 trees selected at random (the number of trees depends on the orchard area and the time available) in each orchard, record the number of extension shoots with primary mildew per tree.
Using the estimate of total number of extension shoots per tree, calculate the percentage of primary mildewed shoots and categorise as above.
Primary mildew levels below 2% mildewed shoots or blossoms are considered satisfactory, but preferably levels should be less than 1.0%

Assessments of primary mildew provide information on the inoculum level for the coming season and also provide information on the success of the previous season’s programme.

Primary blossom mildew will give an indication of mildew incidence in the early part of the previous season and primary vegetative mildew a measure of mildew control at the end of the previous season.
This may give indications of the need to modify the programme for the coming season.

Assessment of secondary mildew

Assessment of secondary mildew gives a measure of mildew activity in the current season and is an essential part of checking on the efficacy of control measures or as a basis for decision making on chemical control.

For more reliable assessments of secondary mildew, repeat assessments should be made on the same trees in each orchard.
However, in practice this is often too time consuming and as disease assessments are usually combined with pest assessments, there may be a need to examine different parts of the orchard at each visit.
The number of trees sampled again is dependent on orchard size and time available (see below).
In mixed orchards, sample the most susceptible varieties or a mixture of varieties.

Number of trees to sample for assessing secondary mildew in an orchard block

Area of block not more than:		Number of trees to sample
Acres	Hectares	Number of trees to sample
1.5	0.50	10
2.5	1.00	15
4.0	1.50	20
6.0	2.50	25
7.5	3.00	30
10.0	4.00	35

Assessments should be done regularly during the growing season at 7-14 day intervals or as often as a spray decision needs to be made.

On each assessment date, select at random four actively growing extension shoots per tree, avoiding ones with primary mildew or pest problems.
Select the youngest unrolled leaf as the reference leaf. Examine the five leaves immediately below the reference leaf for colonies of mildew, which are often not easy to see.
On each assessment date record the number of either mildewed leaves or mildewed shoots and express as a percentage of leaves or shoots examined. These two measures of secondary mildew can be converted (see below).

Equivalence of percentages of leaves and shoots with secondary mildew colonies

Mildewed shoots	Mildewed leaves	Mildewed shoots	Mildewed leaves
5	1-2	55	18
10	2-3	60	20
15	4	65	23-24
20	5-6	70	26
25	7	75	29-30
30	8-9	80	33-34
35	10	85	38
40	12	90	44
45	14	95	53
50	16	100	80

Levels of secondary mildew are categorised as follows:

Categories of secondary mildew shoots

Low = ≤ 10%

Moderate = 10 – 30%

High = >30%

Cultural control

This is based on removal of primary inoculum by pruning.

In winter prune out silvered shoots.
At pink bud and petal fall prune out primary blossom and primary vegetative mildew.
This must be done rapidly to limit spread of inoculum.
Where primary mildew levels are high, removal of inoculum may be the only way to reduce inoculum.

Mildew management

Using estimates of secondary mildew to make decisions on disease control

Mildew management based on assessments of secondary mildew was developed by Butt and Barlow. In order to make mildew management work it is important to understand apple mildew characteristics that make it a successful pathogen:

Mildew overwinters in the buds so it ensures a source of primary inoculum present in the orchard.
Mildew spores germinate in the absence of liquid water and so can infect almost daily during the growing season.
Apple shoots have a long growing season so the tree stays susceptible for several months.
It is difficult to maintain adequate doses of fungicide to protect rapidly growing leaves, so fungicide cover must be good to maintain protection.

Mildew inoculum level is the key factor in determining the seasonal epidemic. Therefore, control strategies depend on maintaining primary mildew at a low level.

June is a critical time for monitoring and for mildew control as this is the period of rapid extension growth and also when fruit buds are forming and sealing for next spring.
A high mildew incidence at this time will result in high primary blossom mildew next season.
Likewise, at the end of growth in late summer, when terminal buds are sealing, mildew control is important to ensure that mildew carryover in buds is as low as possible.
In some seasons, particularly when the summers are dry, terminal buds restart growth after harvest. It is important to monitor this, as failure to control mildew at this time can lead to high overwintering mildew.

The objective of mildew management is to adopt a flexible approach in which fungicide dose, spray interval and spray volume are adjusted to match the level of epidemic activity. The seasonal activity is measured by regular assessments of secondary mildew levels.

The management tools to control mildew are:

Choice of fungicide (eradicant or protectant)
Fungicide dose (25-100% of label dose)
Spray interval
Spray volume

The decisions are based on the following:

Mildew incidence
Growth stage
Current weather

Management of mildew in this way ensures that disease control is maintained and fungicide use rationalised.

Guidelines for decisions on fungicide use based on secondary mildew assessments

Disease rating	Mildewed leaves (%)	(Mildewed shoots (%))	Action after petal fall
Low	<2-3	(<10)	In cool weather with rainy spells or when shoot growth is slow, take the opportunity to reduce fungicide use by reducing dose (minimum dose = 25%) or extending spray interval.
Moderate	3-9	(10-30)	Maintain control. Consider improving the programme by reducing the spray interval or increasing the fungicide dose (not exceeding the label maximum) especially if the weather is warm and humid and shoot growth is rapid.
Potentially high	>9	(>30)	Improve control immediately especially if shoots are growing, irrespective of weather. Shorten spray interval, increase fungicide dose (not exceeding label maximum), possibly increase spray volume. Consider changing fungicide. Check sprayer is working correctly.

Using ADEM to manage powdery mildew

ADEM is a PC-based system which gives warnings of several apple diseases, including models of apple scab, apple powdery mildew (PODEM), apple canker and fruit rot and fireblight.

The models are driven by weather variables including rainfall, surface wetness duration, ambient temperature and ambient relative humidity.
These are recorded by a data logger or weather station sited in the orchard or at a convenient site on the farm, and downloaded to the PC either directly or via a laptop computer.
The mildew model forecasts the epidemic of secondary mildew by combining the effects of weather on spore production and dispersal, infection and subsequent colony development on young leaves, with varietal susceptibility and the amount of mildew inoculum recorded in the orchard.
The index of mildew risk generated can then be used to assist in decision-making on fungicide use.

Assessments of primary and secondary mildew should be made. These are classified as low, moderate or high and then put into the ADEM model running on the PC, along with varietal susceptibility and weather data.

The mildew risk generated is predictive as it forecasts the amount of mildew in the orchard which is likely to be sporing in 3-4 days time.
Using this information, decisions on fungicide use are made in the same ways as if based on mildew assessments only, but by using the mildew risk derived from ADEM, which gives information on the future progress of the epidemic, the decisions on fungicide use are more robust.

Chemical control

The main means of control in the UK are fungicide sprays combined with cultural control.

Fungicides recommended for control of mildew have protectant, eradicant and anti sporulant properties.
Generally, frequent sprays are required between green cluster and the end of shoot growth in the summer.
In some seasons, particularly after dry summers, terminal buds restart growth after harvest. Additional sprays may then be needed later in the season.
Fungicide programmes should be based on products from different chemical groups to avoid the development of strains of mildew with reduced sensitivity to fungicides.
Generally choice of fungicide pre-bloom and up to petal fall is governed by the need for scab control, which usually has precedence, and the need for an eradicant/anti sporulant fungicide to control primary mildew.
Usually a DMI fungicide such as myclobutanil (Systhane 20EW) or penconazole (Topas, Topenco) is used for this purpose.
After petal fall, during extension growth, other fungicides (see Download list in main Control section on previous page) may be used as an alternatives to DMI fungicides.
Potassium bicarbonate can act as an eradicant or suppress sporulation of powdery mildew and may assist in mildew control. It has no protectant action. Because of its eradicant properties, it is useful early in the season to reduce existing levels of the disease. When used with products which have protectant properties, protection can be maintained into the season.
If mildew is being managed according to Butt and Barlow method or ADEM, then the alternative products listed above may be substituted for a DMI product or one with eradicant properties, where the mildew incidence has increased.

Spray application, spray volume, fungicide dose and mildew control

Control of powdery mildew is dependent on good spray cover. Both spray volume and fungicide dose influence spray cover. Trials conducted over several years in the 1980s both in the UK and abroad reached the following main conclusions:

The average deposit of pesticide was proportional to the rate applied, but the distribution of the pesticide was dependent on the spray volume.
Low volumes tended to give a lower percentage cover and a more variable deposit.
In general the cover achieved with 50 l/ha appeared to be low, whereas that achieved with 100 l/ha and above was satisfactory.
Therefore, based on these results, the mildew control achieved using 50 l/ha and reduced fungicide dose would be poorer than that with medium spray volumes (500 l/ha) or the full dose.

These results were confirmed in orchard trials over several seasons in the1980s, where sprays applied at ULV (50 l/ha) and reduced fungicide dose resulted in poorer control of mildew compared to MV (500 l/ha) or LV (100-150 l/ha).
However the overall incidence of mildew was low, even in untreated plots, so that the control achieved at ULV was acceptable commercially.
None of the replicated trials were continued for long enough to demonstrate the cumulative effects of the poorer control over several seasons.
However, these trials do show that there is scope for reducing both spray volume and fungicide dose for mildew control, which can result in significant savings in fungicide inputs.
It is, however, essential that this approach is combined with careful monitoring and disease management, as outlined above, so that increases in mildew incidence can be responded to rapidly by adjusting fungicide dose and/or spray volume.

Avoiding fungicide resistance

Research has indicated that localised populations of powdery mildew may be less sensitive to DMI fungicides.
However, in most cases failure to control powdery mildew is due to a combination of factors.
Fungicide products currently recommended for control of powdery mildew fall into a narrow range of chemical groups.
Therefore it is important to use products from different chemical groups in a programme to minimise the risk of resistance and maximise fungicide efficacy .

An integrated approach to control

AHDB funded research in Project TF 223 (Improving integrated pest and disease management in tree fruit) investigated ways of integrating novel and alternative control products with conventional fungicide products within powdery mildew spray control programmes. The purpose was to find ways of reducing reliance upon conventional fungicides, whilst maintaining an equal level of control.

Initial work assessed alternatives to conventional fungicides and three products were identified with ability to improve tree health and increase the tree’s ability to resist disease. These included Cultigrow (a biostimulant based on flavonoids), Trident (a silicon-based nutrient) and Mantrac Pro (manganese nutrient).
SB Invigorator (a blend of surfactants) and the adjuvant Wetcit (a natural adjuvant based on alcohol ethoxylate) are used in combination with plant protection products and offererd a physical barrier to powdery mildew infection.
When combined with conventional fungicides in the project in weekly spray programmes, by switching between alternative products and fungicides, similar levels of control to a routine seven-day fungicide programme were achieved in both Gala and Braeburn orchards.
Three spray programmes offered similar control, two based on Cultigrow applied monthly, with either Mantrac or Trident applied every two weeks, the third based on Trident and Mantrac alternating every two weeks. Conventional fungicides were applied in the weeks between the alternative products. SB Invigorator was applied as a separate spray (should not be mixed with other products) in all programmes and Cultigrow was used with the adjuvant Wetcit. Full details of the programmes used are available in the final report of Project TF 223.
The standard seven-day conventional fungicide programme achieved the best early season control for both Gala and Braeburn, but by July, all three alternative programmes were performing as well as the standard.
Starting all programmes with the seven-day standard fungicide programme for the first few sprays would probably have resulted in comparable control throughout the season and any growers considering this approach should follow this experience.
Employing one of the alternative programmes therefore offers similar levels of mildew control and fruit quality but with half or reduced numbers of conventional fungicides.

Biological control

Use of biocontrol agents may offer an alternative approach for control of powdery mildew. Ampelomyces quisqualis is a naturally occurring mycoparasite of powdery mildews, which has been used in other crops e.g. grapes and cucumber with some success. Bacillus amyloliquefaciens (Amylo X) is also approved for use on apple. Experience with this product is limited.

An isolate – AQ10- is available commercially.
A. quisqualis is known to occur naturally in the UK on apple powdery mildew.
Recent experiments with the mycoparasite showed that the AQ10 isolate failed to establish on the apple trees and was not very effective in controlling apple powdery mildew.
There are now other commercially available hyper-parasites of powdery mildew (eg Verticillium leucanii as Vertalec or Mycotal or Pseudozyma flocculosa as Sporodex) which are reported to be more effective and may be worth evaluating in a future research projects.

Apple Best Practice Guide