199 1. Introduction Summer pruning of apples (Malus x domestica) is a practice used primarily to enhance fruit quality through the manipulation of tree physiology and alteration of the canopy environment, particularly light. The majority of studies of summer pruning in apple have focused on physi- ological impacts such as photosynthate partitioning, win- ter hardiness, return bloom, fruit coloring and post-harvest quality. However, summer pruning can have impacts on apple diseases, because it alters canopy microclimate, can remove diseased tissue, improves deposition of fun- gicides and other chemicals, and in altering tree physiol- ogy may change resistance to disease. Summer pruning may enhance disease management, but in some cases may increase the risk of disease. Of the few studies that have investigated interactions between summer pruning and apple diseases, most were done on semi-dwarf trees, and very few have looked at high-density systems. In semi-dwarf trees, summer pruning offered both hor- ticultural and disease management benefits. This is illus- trated by an example from the mid-1980’s in the northeast- ern US, where summer pruning was used to compensate for the loss of daminozide in commercial apple production (Autio and Greene, 1990). The predominant cultivar pro- duced in the region at that time was ‘McIntosh’, which fre- quently drops fruit to the ground before they are sufficient- ly colored for harvest. Daminozide (Alar®) prevented this premature fruit drop, allowing development of full fruit color. When the manufacturers of daminozide removed the registration for apple use, it created potentially devastat- ing crop loss through premature drop in ‘McIntosh’. As a response, growers were encouraged to summer prune, primarily to accelerate development of fruit color through increased light penetration in the canopy. The practice was successful, to a large extent compensating for daminozide treatments. It also had a side-benefit, in that incidence of the summer disease complex sooty blotch and flyspeck (SBFS) decreased in summer-pruned trees, primarily as the result of reduced humidity and improved fungicide penetration in the canopy (Cooley et al., 1997). At this time, the most recent major review of summer pruning was written 25 years before this review, focusing exclusively on effects on tree growth, yield, flowering, and fruit development (Saure, 1987). Since then, commercial apple production has seen wide-spread adoption of high- density planting systems in which the methods and im- pacts of summer pruning would be expected to differ sub- stantially from those used in semi-dwarf (e.g. M.7, ca. 5 m tall) trees, but few studies have examined the impacts of summer pruning on apple diseases in high-density trees. In larger, semi-dwarf trees, summer pruning does not have an impact on the tree scaffold, but focuses on small branches and is largely intended to increase light penetration and Summer pruning of apple: impacts on disease management D.R. Cooley, W.R. Autio Department of Plant, Soil and Insect Sciences, University of Massachusetts Amherst, Amherst, MA, USA. Key words: apple scab, black rot, canopy management, cultural control, fire blight, Malus x domestica, microclimate, Nectria canker, powdery mildew, sanitation, sooty blotch and flyspeck, white rot. Abstract: Pruning, including summer pruning, of apples can have a positive impact on disease management in two basic ways: through removal of dead tissue and inoculum, and through alteration of the canopy microclimate. Summer prun- ing can also increase diseases if it is done when disease risk is high. However summer pruning is used almost exclusively as a horticultural tool to improve fruit quantity and quality. As orchard planting and training systems have moved from semi-dwarf trees to high-density, fully-dwarf trees, very few summer pruning studies have looked at impacts related to disease, yet summer pruning in high-density systems may have important disease management effects. Growers should avoid summer pruning practices which will increase disease risks, and use those that offer both horticultural and disease management benefits. More research in this area is needed, as cultural components of apple disease management will become increasingly important in sustainable production systems. This review looks at important apple diseases, includ- ing apple scab, fire blight, sooty blotch and flyspeck, black rot, white rot, Nectria canker and powdery mildew, and uses dormant pruning studies plus knowledge of the epidemiology of the diseases to suggest ways that summer pruning would be expected to impact disease management. Adv. Hort. Sci., 2011 25(3): 199-204 Received for publication 20 June 2011 Accepted for publication 27 July 2011 200 air circulation, beneficial to both fruit quality and disease management. However, in modern high-density produc- tion systems a primary goal is light penetration, and overall tree training maintains a relatively small, open canopy. In such trees, summer pruning may not significantly increase air circulation, improve drying in the canopy, or improve pesticide deposition, and it is unclear whether it has bene- fits in terms of disease management. Instead, pruning cuts during the growing season may increase the risk of infec- tion. Alternatively, pruning and removing diseased tissue, sanitation, may reduce disease impacts and future risks, but such cuts may conflict with desired tree architecture in a high-density system. Yet as restrictions on chemical use in plant disease management increase, cultural con- trols such as sanitation and inoculum destruction become more important. Much of this review must extrapolate from studies on semi-dwarf trees, dormant pruning, and the epidemiology of apple diseases to identify potential benefits and risks of summer pruning related to disease. It outlines types of summer pruning used in high-density systems, and then looks at important apple diseases that may be impacted by summer pruning and how pruning for sanitation may be useful. 2. Impacts on tree growth, yield, flowering and fruit development Summer pruning can take on various forms from sim- ple watersprout removal only to significant reductions in canopy density. Much study of summer pruning came from an interest in enhanced light penetration into the summer canopy, thus improving fruit color development. Vincent (1917), Preston and Perring (1974), Stiles (1980), Lord and Greene (1982), Marini and Barden (1982), Morgan et al. (1984), Autio and Greene (1990), Schupp (1992), and Ystaas (1992) all showed increased fruit redness as a result of summer pruning. Decreases in fruit size, however, have also been reported in some studies (Stiles, 1981; Marini and Barden, 1982; Greene and Lord, 1983; Myers and Fer- ree, 1983) but not all and not consistently. Li et al. (2003) modeled tree physiology as a result of summer pruning and found reductions in carbohydrates, potentially lead- ing to a carbohydrate shortage after summer pruning. The potential for shortage was greater as the intensity of sum- mer pruning increased. Fruit size impacts of that shortage can be mediated by improved water status resulting from reduced transpiration. Additionally, varying responses may be partially explained by the location of the summer- pruning treatment. Greene and Lord (1983) suggested that, as the severity of pruning increased or as the distance be- tween the cut and the fruit decreased, the potential for a size reduction is enhanced. Timing of summer pruning also is an important consid- eration. In general, regrowth during the period following summer pruning is greater the earlier the summer pruning is performed. Autio and Greene (1990) showed a linear decrease in the amount of regrowth as the pruning was performed from early (~45 days after full bloom) to late summer (~105 days after full bloom). Zamani et al. (2006) described a similar response from summer pruning from 30 to 90 days after full bloom. Such data indicate that summer pruning acts as a stress on apples. If a stress is severe enough it can predispose woody plants to disease particularly from canker patho- gens, but plants will recover from light to moderate stress (Schoeneweiss, 1981). At the same time, abiotic stresses can induce disease resistance in plants, including apples, though the physiological mechanisms behind induced re- sistance are not well understood (Hammerschmidt, 1999; Poupard et al., 2003). Developing a better understanding of the detrimental and positive impacts of pruning stress at the physiological level is an area in need of more research. 3. Impacts on disease Pruning apple trees, including summer pruning, can impact disease in several ways: by altering microclimate and architecture of the canopy, by removing inoculum and infected tissue, and by creating wounds that pathogens can invade. In their experiment in an organic orchard, Simon et al. (2006) observed that centrifugal training decreased apple scab and key insect pests in an organic orchard, and listed five explanatory hypotheses: 1) removal of inocu- lum and arthropods with the removal of fruiting spurs; 2) change in canopy microclimate, particularly better aera- tion; 3) decreased shoot density and increased distance be- tween growing shoots slowing transmission; 4) changes in tree physiology inducing resistance or otherwise changing tissue susceptibility; 5) decreased canopy density improv- ing pesticide penetration and deposition. Pruning for sanitation is specifically designed to remove inoculum, thereby delaying or slowing epidemics and decreasing disease incidence and severity. For example, pruning removes primary inoculum of apple powdery mil- dew and fire blight, and is routinely recommended as part of the management programs for these diseases (Covey and Fischer, 1990; Xu, 1999; Steiner, 2000; Holb, 2005). However, pruning for sanitation often requires pruning cuts that do not conform to horticultural goals, and in most cases is performed in winter or early spring rather than summer. Summer pruning may remove inoculum, though it is not the primary purpose of the practice. Changing the canopy density alters microclimate thereby impacting infection and disease development. Mi- croclimate factors, particularly those related to moisture, have a major effect on plant diseases (Huber and Gillespie, 1992), and altering canopy density, as summer pruning does, influences canopy drying and disease (Gubler et al., 1987; Cooley et al., 1997; Sentelhas et al., 2005; Batzer et al., 2008). Leaf wetness duration (LWD) is a particularly important factor in plant disease epidemics and is often used in disease forecast models (Gleason et al., 2008). For example, LWD has a major impact on whether or not apple scab (Venturia inaequalis) infections occur (Mills, 1944; 201 MacHardy and Gadoury, 1989; Stensvand et al., 2005; Xu and Robinson, 2005). High humidity and LWD also in- crease disease incidence and severity of SBFS (Cooley et al., 2011), cedar-apple rust (Gymnosporangium juniperi- virginianae) (Aldwinckle et al., 1980), black rot (Botryos- phaeria obtuse) (Arauz and Sutton, 1989), white rot or Bot rot (Botryosphaeria dothidea) (Sutton and Arauz, 1991), Nectria canker (Nectria galigena) (Krahmer, 1981; Xu et al., 1998), and fire blight (Erwinia amylovora) (Steiner, 2000). Of these diseases, apple scab, SBFS, black rot, white rot and bitter rot drive most of the fungicide applica- tions made in the eastern US, and account for substantial fungicide use in many apple production areas around the world (Cooley, 2009). By maintaining an apple canopy that dries relatively quickly, LWD periods are shortened, which may allow decreases in fungicide use. The relationship between plant growth and the rate of an epidemic is complex, depending on tissue susceptibil- ity, existing infections and the density of susceptible tissue, among other factors (Ferrandino, 2008). For apple scab, the relative risk of infection is affected by the amount of leaf tis- sue available for infection interacting with increasing onto- genic resistance and inoculum availability, which all change over time (Ficke et al., 2002). Summer pruning removes target tissue as well as sources of inoculum, and hence should slow development of apple scab epidemics. The tim- ing of tissue removal should affect disease, and in general removal early in the growing season should reduce disease more than mid- or late-season removal. Still the interaction between pruning and the different epidemiological factors is complex. In the scab example, if early pruning stimulates vegetative growth, the rapid development of relatively large amounts of young, susceptible tissue may erase any early- season disease suppression. Holb et al. (2004) observed that heavy winter pruning suppressed foliar scab, but the impact on fruit at harvest was not significant. For fire blight, it is recommended that flower clusters be removed from non-bearing trees before bloom, because the flowers are an important infection court for E. amy- lovora (Steiner, 2000). Pruning relatively non-productive flower clusters, as in centrifugal training, may reduce risk of fire blight. Pruning also usually improves penetration of fungi- cides and other disease controlling chemicals (Sutton and Unrath, 1984; Travis et al., 1987; Cooley et al., 1997; Cross et al., 2003). Both summer (Cooley et al., 1997) and winter pruning (Ocamb-Basu et al., 1988; Holb, 2005) have been shown to improve spray penetration relative to non-pruned trees, though a comparison between two high density pruning methods in which centrifugal training re- duced scab relative to original solaxe pruning did not show a difference in spray deposition (Simon et al., 2006). Apple scab Scab is probably the most important diseases threat- ening apples in humid production regions, but only one published study has been done on the impacts of summer pruning on the disease. Disease incidence in apple scab is strongly related to the duration of wetting periods and the amount of inoculum available in an orchard, with lon- ger wetting periods and more inoculum increasing disease incidence and severity (MacHardy, 1996). Simon et al. (2006) showed a decrease in scab in high-density plant- ings pruned using centrifugal pruning relative to original solaxe pruning. They suggested that centrifugal pruning shortened wetting periods in the canopy thereby reducing the number and/or intensity of infection periods, though they do not present data on canopy microclimate. A study by Holb (2005) looked at different levels of winter pruning on scab in high-density organic orchards, and concluded that heavy pruning significantly reduced the area under the disease progress curve for foliar and fruit scab on susceptible cultivars. They hypothesized that suppression of scab epidemics were caused by a reduction of inoculum overwintering in apple buds, improved fun- gicide deposition in pruned trees, and modification of the in-canopy microclimate, though microclimate factors did not consistently vary among pruning regimens. Fire blight Fire blight is an increasingly serious disease of apples worldwide. The disease affects all apple tissues, but is most damaging when it migrates from primary infections, commonly in blossoms and young shoots, to limbs and trunks. Scaffold limb and trunk infections are particularly damaging, cutting production over several seasons and of- ten killing trees (Van der Zwet and Beer, 1995; Steiner, 2000; Thomson, 2000). Primary infections may also oc- cur when trees are damaged mechanically by hailstones or other means, allowing the bacterial pathogen to enter the plant. In the case of fire blight, pruning for horticulture pur- poses also may provide entry points for the pathogen. An early study of effects of summer pruning on fire blight in apple showed that it markedly increased infections (Lake et al., 1975). Hence pruning when fire blight models (e.g. (Steiner and Lightner, 1996; Smith, 1999) indicate risk of infection is high should be avoided if possible, or a treat- ment of streptomycin or other chemical prior to pruning be made if it is not. For example, mechanical hedging as practiced in fruiting walls would be expected to open multiple sites to fire blight infection for several days, and would be analogous to a hailstorm in terms of generating risk of infection from fire blight. Fire blight epidemics often force growers to prune in an attempt to stop the progress of infections and remove inoculum. Recommendations for such pruning generally suggest cutting back to a healthy branch union approxi- mately 25 cm below visible infections; disinfection of pruning tools with alcohol or bleach between cuts may also be recommended (Van der Zwet and Beer, 1995; Steiner, 2000; Toussaint and Philion, 2008). In apples it has gener- ally been recommended diseased tissue be pruned out as soon as symptoms are observed, and pruning continued at frequent intervals thereafter in order to slow and stop epi- demics (Covey and Fischer, 1990; Steiner, 2000; Toussaint 202 and Philion, 2008). Shtienberg et al. (2003) found that fac- tors related to the host, pathogen and environment should all be taken into account when determining whether and how to prune fire blight in pears, and elements of this ap- proach may be useful in apples. Sooty blotch and flyspeck Summer pruning has been shown to decrease SBFS in apples, primarily because it reduces relative humidity and improves fungicide penetration and coverage in the canopy (Cooley et al., 1997). This study was conducted on free- standing semi-dwarf apple trees approximately 5 m tall by 3 m diameter. It is not known whether similar results would be obtained in systems using fully dwarf trees in dense plant- ings. However a trial in the US showed that it took over 450 hours LWD for SBFS symptoms to develop in fully-dwarf, well-maintained trees while large trees with dense canopies developed signs at 225 hours LWD (Ellis et al., 1999). The extent to which fully-dwarf trees in high-density systems may benefit from summer pruning has not be studied. Mum- mified fruit have been shown to harbor inoculum for SBFS pathogens, and removing these mummies can reduce dis- ease incidence (Gleason et al., 2011). Black rot and white rot Black rot and white rot are fungal diseases that can attack fruit, foliage and woody tissue of apples. Sutton (1981) showed that much of the inoculum for these diseas- es comes from prunings in or near production blocks, and it is recommended that prunings be removed or chopped so that they rapidly disintegrate so as to remove inocu- lum from the orchard. Removing mummified fruit is also recommended as a cultural control. In that rates of these diseases on fruit is related to wetness duration and can be controlled with fungicides, pruning that reduces canopy humidity and improves fungicide coverage would be ex- pected to enhance their management (Sutton, 1981; Arauz and Sutton, 1989; Arauz and Sutton, 1990; Sutton and Arauz, 1991; Parker and Sutton, 1993). Nectria canker Nectria can cause infections on fruit and woody tissue in apple. Pruning wounds are susceptible to the disease, and hence summer pruning can have an impact on canker inci- dence (Krahmer, 1981; Xu et al., 1998). Studies have con- sistently shown that new wounds, including pruning cuts, are readily colonized by N. galigena. While this is another example of a disease that can be exacerbated by summer pruning, unlike fire blight, there are no forecast models to predict when summer pruning is less risky. There are fungi- cidal chemicals that can be very effective in reducing can- ker incidence if applied right after pruning, including the organically accepted slaked lime (Heijne et al., 2005). Powdery mildew Since the early 20th century, dormant pruning has been recommended as a control measure against pow- dery mildew (Fisher, 1920). More recent studies from eastern Europe suggest that summer pruning that targets infected shoots can significantly reduce the disease, and even eliminate the disease (e.g. Berbekov et al., 2006; Holb and Abonyl, 2007). Disease reduction is probably primarily the result of inoculum removal, though reduc- tion in canopy humidity may play some role as well (Xu, 1999). 4. Conclusions While the role of summer pruning in modern high- density apple orchards is not disease management, the practice does alter the canopy architecture in ways that may reduce moisture levels and wetting period duration. For some diseases, notably fire blight and Nectria canker, summer pruning can increase the risk of infection by caus- ing wounds. While some recent studies show that summer pruning can reduce risk for major apple diseases, such as scab and powdery mildew, virtually no studies have been done outside Europe. There is a need to assess the horticul- tural and disease management benefits and costs of sum- mer pruning across a broader range of climates and high- density production systems, in order to determine whether summer pruning can be an element in economically and environmentally sustainable apple production. References ALDWINCKLE H.S., PEARSON R.C., SEEM R.C., 1980 - In- fection periods of Gymnosporangium juniperi-virginianae on apple. - Phytopathology, 70: 1070-1073. ARAUZ L.F., SUTTON T.B., 1989 - Temperature and wetness duration requirements for apple infection by Botryosphaeria obtusa. - Phytopathology, 79: 440-444. ARAUZ L.F., SUTTON T.B., 1990 - Protectant and after-infec- tion activity of fungicides against Botryosphaeria obtusa on apple. - Plant Disease, 74: 1029-1034. AUTIO W.R., GREENE D.W., 1990 - Summer pruning affects yield and improves fruit quality of McIntosh apples. - J. Am. Soc. Hortic. Sci., 115: 356-359. BATZER J.C., GLEASON M.L., TAYLOR S.E., KOEHLER K.J., MONTEIRO J., 2008 - Spatial heterogeneity of leaf wetness duration in apple trees and its influence on perfor- mance of a warning system for sooty blotch and flyspeck. - Plant Disease, 92: 164-170. BERBEKOV V.N., BYASTRAYA G.V., YAGUBYAN S.K., 2006 - Summer apple shaping and pruning as a method for decreas- ing damage done by powdery mildew (Russian). - ANO Reda- ktsiya Zhurnala Sadovodstvo i Vinogradarstvo, pp. 8-10. COOLEY D.R., 2009 - Biorational approaches to disease man- agement in apples, pp. 214-252. - In: LESKEY T.C., M. ALUJAH, and C. VINCENT (eds.) Biorational tree fruit pest management. Commonwealth Agricultural Bureau In- ternational, Oxfordshire, UK. COOLEY D.R., GAMBLE J.W., AUTIO W.R., 1997 - Summer pruning as a method for reducing flyspeck disease on apple fruit. - Plant Disease, 81: 1123-1126. 203 COOLEY D.R., ROSENBERGER D.A., GLEASON M.L., KOEHLER G., COX K., CLEMENTS J.M., SUTTON T.B., MADEIRAS A., HARTMAN J.R., 2011 - Variability among forecast models for the apple sooty botch/flyspeck disease complex. - Plant Disease, 95(9): 1179-1186. COVEY R.H., FISCHER W.R., 1990 - Timely cutting of fire blight infections reduced losses. - Acta Horticulturae, 273: 351-353. CROSS J.V., WALKLATE P.J., MURRAY R.A., RICHARD- SON G.M., 2003 - Spray deposits and losses in different sized apple trees from an axial fan orchard sprayer: 3. Ef- fects of air volumetric flow rate. - Crop Prot., 22: 381-394. ELLIS M.A., MADDEN L.V., WILSON L., 1999 - Evaluation of an empirical model for predicting sooty blotch and fly- speck of apples in Ohio. - Ohio State University Research Bulletin, Research Circular, pp. 1-6. FERRANDINO F.J., 2008 - Effect of crop growth and canopy filtration on the dynamics of plant disease epidemics spread by aerially dispersed spores. - Phytopathology, 98: 492-503. FICKE A., GADOURY D.M., SEEM R.C., 2002 - Ontogenic resistance and plant disease management: A case study of grape powdery mildew. - Phytopathology, 92: 671-675. FISHER D.F., 1920 - Control of apple powdery mildew. - U.S. Department of Agriculture, Farmer’s Bulletin, no. 1120. GLEASON M.L., BATZER J.C., SUN G., ZHANG R., ARIAS M.M.D., SUTTON T.B., CROUS P.W., IVANOVIC M., MC- MANUS P.S., COOLEY D.R., MAYR U., WEBER R.W.S., YODER K.S., DEL PONTE E.M., BIGGS A.R., OERTEL B., 2011 - A new view of sooty blotch and flyspeck. - Plant Disease, 95: 368-383. GLEASON M.L., DUTTWEILER K.B., BATZER J.C., TAY- LOR S.E., SENTELHAS P.C., MONTEIRO J., GILLESPIE T.J., 2008 - Obtaining weather data for input to crop disease warning systems: leaf wetness duration as a case study. - Sci. Agric., 65: 76-87. GREENE D.W., LORD W.J., 1983 - Effects of dormant pruning, summer pruning, scoring, and growth regulators on growth, yield, and fruit quality of ‘Delicious’ and ‘Cortland’ apple trees. - J. Am. Soc. Hortic. Sci., 108: 590-595. GUBLER W.D., MAROIS J.J., BLEDSOE A.M., BETTIGA L.J., 1987 - Control of Botrytis bunch rot of grape with can- opy management. - Plant Disease, 71: 599-601. HAMMERSCHMIDT R., 1999 - Induced disease resistance: how do induced plants stop pathogens? - Physiol. Mol. Plant Pathol., 55: 77-84. HEIJNE B., DE JONG P.F., WENNEKER M., JANSONIUS P.J., 2005 - Slaked lime against European fruit tree canker: efficacy and introduction into practice. - ISOFAR, Prooceed- ings of the Conference “Researching Sustainable Systems”, 21-23 September, Adelaide, South Australia. HOLB I.J., 2005 - Effect of pruning on apple scab in organic apple production. - Plant Disease, 89: 611-618. HOLB I.J., ABONYL F., 2007 - Control of apple powdery mildew in integrated and organic production. (Hungarian - English summary). - Növényvédelem, 43: 247-252. HOLB I.J., HEIJNE B., JEGER M.J., 2004 - Overwintering of conidia of Venturia inaequalis and the contribution to early epidemics of apple scab. - Plant Dis., 88: 751-757. HUBER L., GILLESPIE T.J., 1992 - Modeling leaf wetness in relation to plant disease epidemiology. - Annual Review of Phytopathology, 30: 553-577. KRAHMER H., 1981 - Regeneration of pruning wounds of apple trees and their susceptibility to infections by Nectria galligena. - Angew. Bot., 55: 429-439. LAKE C.F., STUSHNOFF C., KENNEDY W., 1975 - Fire blight infection on summer-pruned apples. - Plant Disease Reporter, 59: 620-622. LI K.T., LAKSO A.N., PICCIONI R., ROBINSON T., 2003 - Summer pruning effects on fruit size, fruit quality, return bloom and fine root survival in apple trees. - J. Hortic. Sci. & Biotechnology, 78: 755-761. LORD W.J., GREENE D.W., 1982 - Effects of summer pruning on the quality of McIntosh apples. - Hortscience, 17: 372-373. MACHARDY W.E., 1996 - Apple scab: biology, epidemiology and management. - APS Press, St. Paul, MN, USA, pp. 545. MACHARDY W.E., GADOURY D.M., 1989 - A revision of Mills criteria for predicting apple scab infection periods. - Phytopathology, 79: 304-310. MARINI R.P., BARDEN J.A., 1982 - Yield, fruit size, and qual- ity of three apple cultivars as influenced by summer or dor- mant pruning. - J. Am. Soc. Hortic. Sci., 107: 474-479. MILLS W.D., 1944 - Efficient use of sulfur dusts and sprays dur- ing rain to control apple scab. - N.Y. Agr. Exp. Sta. Ithaca Ext., Bull. No. 630, pp. 4. MORGAN D.C., STANLEY C.J., VOLZ R., WARRINGTON I.J., 1984 - Summer pruning of ‘Gala’ apple: The relation- ships between pruning time, radiation penetration, and fruit quality. - J. Am. Soc. Hortic. Sci., 109: 637-642. MYERS S.C., FERREE D.C., 1983 - Influence of time of sum- mer pruning and limb orientation on yield, fruit size, and quality of vigorous ‘Delicious’ apple trees. - J. Am. Soc. Hortic. Sci., 108: 630-633. OCAMB-BASU C.M., SUTTON T.B., NELSON L.A., 1988 - The effects of pruning on incidence and severity of Zygophi- ala jamaicensis and Gloedes pomigena infections of apple fruit. - Phytopathology, 78: 1004-1008. PARKER K.C., SUTTON T.B., 1993 - Effect of temperature and wetness duration on apple fruit infection and eradicant ac- tivity of fungicides against Botyosphaeria dothidea. - Plant Disease, 77: 181-185. POUPARD P., PARISI L., CAMPION C., ZIADI S., SIMO- NEAU P., 2003 - A wound- and ethephon-inducible PR-10 gene subclass from apple is differentially expressed during infection with a compatible and an incompatible race of Venturia inaequalis. - Physiol. Mol. Plant Pathol., 62: 3-12. PRESTON A.P., PERRING M.A., 1974 - The effect of summer pruning and nitrogen on growth, cropping and storage qual- ity of Cox’s Orange Pippin apple. - J. Hortic. Sci. & Biotech- nology, 49: 77-83. SAURE M.C., 1987 - Summer pruning effects in apple - a re- view. - Sci. Hortic., 30: 253-282. SCHOENEWEISS D.F., 1981 - The role of environmental stress in diseases of woody plants. - Plant Disease, 65: 308-314. SCHUPP J.R., 1992 - Effect of root pruning and summer prun- ing on growth, yield, quality, and fruit maturity of McIntosh apple trees. - Acta Horticulturae, 322: 173-175. SENTELHAS P.C., GILLESPIE T.J., BATZER J.C., GLEA- SON M.L., MONTEIRO J., PEZZOPANE J.R.M., PEDRO M.J., 2005 - Spatial variability of leaf wetness duration in different crop canopies. - International Journal of Biometeo- rology, 49: 363-370. 204 SHTIENBERG D., ZILBERSTAINE M., OPPENHEIM D., LEVI S., SHWARTZ H., KRITZMAN G., 2003 - New considerations for pruning in management of fire blight in pears. - Plant Disease, 87: 1083-1088. SIMON S., LAURI P.E., BRUN L., DEFRANCE H., SAUPHA- NORE B., 2006 - Does manipulation of fruit-tree architec- ture affect the development of pests and pathogens? A case study in an organic apple orchard. - J. Hortic. Sci. & Bio- technology, 81: 765-773. SMITH T.J., 1999 - Report on the development and use of Cou- garblight 98C - A situation-specific fire blight risk assessment model for apple and pear. - Acta Horticulturae, 489: 429-436. STEINER P.W., 2000 - Integrated orchard and nursery man- agement for control of fire blight, pp. 339-358. - In: VAN- NESTE J.L. (ed.) Fire Blight: The Disease and Its Causative Agent, Erwinia amylovora. - CABI, Oxon, Wallingford, UK, pp. 370 STEINER P.W., LIGHTNER G.W., 1996 - MaryblytTM 4.3. A predictive program for forecasting fire blight disease in ap- ples and pears. - University of Maryland, College Park, MD, USA. STENSVAND A., EIKEMO H., GADOURY D.M., SEEM R.C., 2005 - Use of a rainfall frequency threshold to adjust a degree-day model of ascospore maturity of Venturia inae- qualis. - Plant Disease, 89: 198-202. STILES W.C., 1980 - Pruning, growth regulator, and nutrition studies with apples. - Maine State Pomo. Soc. Ann. Rep., pp. 25-34. STILES W.C., 1981 - Summer pruning and growth regulator effects on ‘McIntosh’ apples. - Maine State Pomo. Soc. Ann. Rep., pp. 26-29. SUTTON T.B., 1981 - Production and dispersal of ascospores and conidia by Physallospora obtusa and Botryosphaeria dothidea in apple orchards. - Phytopathology, 71: 584-589. SUTTON T.B., ARAUZ L.F., 1991 - Influence of temperature and moisture on germination of ascospores and conidia of Botryosphaeria dothidea. - Plant Disease, 75: 1146-1149. SUTTON T.B., UNRATH C.R., 1984 - Evaluation of the tree- row-volume concept with density adjustments in relation to spray deposits in apple orchards. - Plant Disease, 68: 480-484. THOMSON S.V., 2000 - Epidemiology of fire blight, pp. 9-36. - In: VANNESTE J.L. (ed.) Fire blight: The disease and its causative agent, Erwinia amylovora. - CABI, Oxon, Wall- ingford, UK, pp. 370. TOUSSAINT V., PHILION V., 2008 - Natural epidemic of fire blight in a newly planted orchard and effect of pruning on disease development, pp. 313-320. In: JOHNSON K.B., and V.O. STOCKWELL (eds.) Proceedings of the Eleventh In- ternational Workshop on Fire Blight. International Society Horticultural Science, Leuven 1, Belgium. TRAVIS J.W., SKROCH W.A., SUTTON T.B., 1987 - Effect of canopy density on pesticide deposition and distribution in apple trees. - Plant Disease, 71: 613-615. VAN DER ZWET T., BEER S.V., 1995 - Fire blight - its nature, prevention, and control: a practical guide to integrated dis- ease management. - Cornell University, USDA Agricultural Information Bull. no. 631, pp. 91. VINCENT C.C., 1917 - Winter versus summer pruning of ap- ple trees. - Idaho Agric. Expt. Sta. Bul. University of Idaho, USA. XU X.M., 1999 - Modelling and forecasting epidemics of apple powdery mildew (Podosphaera leucotricha). - Plant Pathol- ogy, 48: 462-471. XU X.M., BUTT D.J., RIDOUT M.S., 1998 - The effects of in- oculum dose, duration of wet period, temperature and wound age on infection by Nectria galligena of pruning wounds on apple. - Eur. J. Plant Pathol., 104: 511-519. XU X.M., ROBINSON J., 2005 - Modelling the effects of wet- ness duration and fruit maturity on infection of apple fruits of Cox’s Orange Pippin and two clones of Gala by Venturia inaequalis. - Plant Pathology, 54: 347-356. YSTAAS J., 1992 - Effects of summer pruning on yield, fruit size, and fruit quality of the apple cultivar ‘Summerred’. - Acta Horticulturae, 322: 277-282. ZAMANI Z., SAIE A., TALAIE A., FATAHI, R., 2006 - Effects of summer pruning on growth indices of two important Ira- nian apple cultivars ‘Golab’ and ‘Shafi-Abadi’. - Acta Horti- culturae, 707: 269-274.