Fifty years of apple-scab research

A summary of historical South African research on apple scab starting in 1970 with the work of Dr Wolf Schwabe. By Anna Mouton.

Schwabe conducted extensive research on apple scab while with the Fruit and Fruit Technology Research Institute — now the ARC Infruitec — in Stellenbosch. His work is still widely cited today.

Age-related resistance

Plants or parts of plants can become more disease-tolerant or -resistant with age and maturity. Schwabe experimented on 2–5-year-old MM.109 rootstocks. He exposed leaves of known age to either ascospores — spores generated sexually during winter — or conidia — spores generated asexually during summer. Leaf age was measured in days starting from the day on which the leaf was fully unfolded and flat.

Schwabe counted the number of scab lesions per leaf 2–4 weeks post-infection. Leaves developed the largest number of lesions when exposed to conidia 1–3 days after unfolding, or when exposed to ascospores 3–5 days after unfolding.

However, the number of lesions is only part of the story, because younger leaves are smaller than older leaves. When Schwabe compared the number of scab lesions per unit area of leaf, he found that leaves suffered the greatest infections when exposed to conidia before unfolding, or when exposed to ascospores 2 days after unfolding.

Leaves of normally fertilised trees became almost completely resistant to scab 12–13 days after unfolding, when leaf expansion stopped. But exposure to ascospores or conidia could still cause lesions after 13 days. Leaves of trees that were not fertilised became resistant from 7 days onward — an observation that has also been reported by other researchers.

Fruit likewise become more resistant to infection as they mature. Schwabe found that, after exposure to high numbers of spores, fruit developed light infections after infection indices of 120 at 1 week after full bloom, 260 at 5 weeks, 370 at 10 weeks, 455 at 15 weeks, 525 at 20 weeks, and 590 at 25 weeks.

Interpreting infection index

The infection index is the leaf-wetting period in hours multiplied by the mean temperature in °C. The relationship between the leaf-wetting period, temperature, and apple-scab infection has been studied for nearly a century. American plant pathologist Wilfred Mills developed the eponymous Mills table in 1944 as a tool for predicting infection risk using temperature and leaf-wetting-period data.

The Mills table was soon adapted for use in other parts of the world. Schwabe investigated its performance under South African conditions. He mostly experimented with 1–4-year-old MM.109 rootstocks, but also worked with White Winter Pearmain on M.7 rootstocks, and Granny Smith, Golden Delicious, Starking, and Dunn’s Seedling, some on own roots and some on M.793 rootstocks.

Schwabe found that the minimum wetting period required by ascospores to cause infection was shorter than that required by conidia at temperatures of 4–25 °C. He also found that, although the relationship between minimum wetting periods, temperature and infection risk followed a similar pattern to that described by Mills, South African infections occurred after shorter leaf-wetting periods.

South African data showed that, in susceptible leaves on actively growing trees, high spore numbers caused light infections after infection indices of 100–149, moderate infections after indices of 150–224, and heavy infections after indices greater than 225. Low spore numbers required longer wetting periods to produce significant disease.

In fruit at harvest maturity, high spore numbers caused light infections after infection indices of 440–599, moderate infections after indices of 600–999, and heavy infections after indices greater than 1000.

Intermittent wetting had less impact on spore survival than one might expect. Ascospores continued to cause infections after dry periods of up to 16 hours, and conidia after dry periods of up to 32 hours. Temperatures above 30 °C for 6 or more hours reduced scab infections.

Wetting periods and weather

Schwabe was interested in establishing the relationship between weather conditions and infection risk under South African conditions. He collected data on precipitation, temperature, humidity, and leaf wetness at sites in the Elgin-Grabouw-Vyeboom-Villiersdorp area, the Koue Bokkeveld, and the Langkloof.

The results showed that weather conditions were conducive to scab at all sites during all seasons. Most wetting periods had an infection index greater than 100 — the minimum for leaf infection. But continuous wetting periods with infection indices greater than 600 — high enough to cause moderate to severe fruit infection — rarely occurred in the second half of the growing season.

Schwabe cautioned that weather conditions are not the sole determinant of scab risk. He reported that severe scab occurred early in the season at one site even though the weather at the time was not particularly favourable for scab. He believed the reason lay in high levels of spores carried over from the previous season as heavy scab infections had occurred in autumn, and winter weather had promoted ascospore development.

Due to the importance of spore numbers at the start of the growing season, Schwabe recommended that growers survey their orchards at the end of each season to determine the infection potential for the following season. Infection potential should be assessed together with winter conditions, as these affect the development and release of ascospores.

He also advocated for regular orchard monitoring throughout the season, writing that the scab status of each orchard should always be known. This informs decisions about control.

Overwintering conidia

The apple-scab fungus has adapted to the deciduous nature of apple trees by overwintering in fallen leaves. During winter, the fungus reproduces sexually, producing ascospores that are the primary source of new infections in spring.

However, crop-protection consultants in both the Elgin-Grabouw-Villiersdorp-Vyeboom and Koue Bokkeveld regions have noted that apple-scab infection sometimes occurs before ascospores are around in spring.

Research in the 1950s by Prof. Adriaan Louw of the then Department of Plant Disease Studies at Stellenbosch University did not find viable conidia on twigs or bud scales, and he concluded that overwintering conidia were not a potential source of spring infections.

Dr Saskia von Diest relooked at this question as part of the apple-scab research completed for her doctorate, funded by Hortgro, and conducted under the supervision of Dr Cheryl Lennox of the Department of Plant Pathology at Stellenbosch University, and Prof. William MacHardy of the College of Life Sciences and Agriculture at the University of New Hampshire.

Von Diest tested both the inside and outside of buds, as well as pygmy apples for the presence and number of viable conidia.

Pygmy apples are small fruit that stay on the tree during winter, especially in regions with warmer winters. Von Diest reported that the numbers of conidia on pygmy apples were too great to be counted. About a third were viable in both years that she conducted her research.

Von Diest concluded that pygmy apples may represent a significant source of infection in spring, especially following heavy infections in the previous season. Removing these fruit, even if they have fallen to the ground, can help prevent apple scab from gaining the upper hand in the next season.

Orchard sanitation and leaf shredding

Many apple-scab researchers have highlighted the importance of removing overwintering fungus from orchards to reduce infections by ascospores in spring. Scientists have also reported that urea applications can suppress the production of ascospores. Preventing sexual reproduction by overwintering fungus has the added advantage of slowing the development of resistant apple-scab strains.

Von Diest conducted trials to assess the impact of different orchard-sanitation practices in commercial orchards in the Koue Bokkeveld and Elgin. In the first year of her trials, Von Diest compared three interventions — leaf removal, leaf shredding, and urea sprays — to a negative — no interventions — and a positive — normal fungicide spray programme — control.

In the following three years, Von Diest only looked at leaf shredding compared to a negative and a positive control.

Leaf shredding did not significantly reduce the occurrence of apple scab on leaves compared to no interventions in the first year. But leaf shredding did significantly reduce the occurrence of apple scab on fruit. However, 85% of fruit in the leaf-shredding intervention still developed at least one scab lesion, compared to 5% of fruit in a normal spray programme.

Scab occurrence on fruit and leaves was similar for leaf-shredding and leaf-removal interventions. Urea sprays proved ineffective.

The results for the following three years showed a similar pattern. Leaf shredding did not significantly reduce the number of leaves affected by apple scab, although leaves were less severely infected compared to leaves that had no interventions.

There were significantly fewer infected fruit and infections were less severe in the leaf-shredding treatment compared to no intervention. However, apple-scab occurrence was significantly worse compared to a normal spray programme. Whereas approximately 2% of fruit were affected by scab in the normal spray programme, 15% were affected in the leaf-shredding treatment.

Von Diest speculated that delayed leaf drop, especially in warm-winter areas, reduces the impact of leaf shredding, as fungal sexual reproduction will already have started. Furthermore, effective leaf shredding is hampered by pruning material and tall vegetation in the work row, and by wet winter conditions.

Apple-scab adaptation

Lastly, Von Diest looked into the ascospore production of apple-scab fungus from Grabouw and the Koue Bokkeveld. She collected infected leaves from orchards in both regions in two years, and overwintered some from each region in Elgin and some in the Koue Bokkeveld.

Fungus from the Koue Bokkeveld had a higher potential ascospore production when overwintered in the Koue Bokkeveld than when overwintered in Grabouw. Potential ascospore production by fungus from Grabouw was the same regardless of where it overwintered.

These results suggest that apple-scab populations from the two different regions have adapted to winter conditions in their area. Von Diest concludes that higher potential ascospore production in the Koue Bokkeveld implies that orchard sanitation measures such as leaf shredding will have a greater impact in this region compared to Grabouw.