apple leaf shredding as a non-chemical tool to manage apple scab and spotted tentiform leafminer

Agriculture, Ecosystems and Environment 104 (2004) 595–604

Apple leaf shredding as a non-chemical tool to manageapple scab and spotted tentiform leafminer

Charles Vincent∗, Benoit Rancourt, Odile CarisseHorticultural Research and Development Center, Agriculture and Agri-Food Canada, 430 Gouin Blvd.,

Saint-Jean-sur-Richelieu, Que., Canada J3B 3E6

Received 25 March 2003; received in revised form 22 December 2003; accepted 7 January 2004

Abstract

The effect of leaf-shredding onVenturia inaequalis, andPhyllonorycter blancardella and its parasitoids was studied underorchard conditions, respectively, during four and three overwintering periods. Naturally scab-infected leaves were collected inthe fall. Five treatments were compared in 1995 and 1996, i.e. shredded leaves, urea (5%),Microsphaeropsis ochracea, Atheliabombacina and untreated leaves (control). In 1997 and 1998, two more treatments were added, i.e. shredded leaves treated with5% urea and shredded leaves treated withM. ochracea. The ascospore production from a sample corresponding to the averagearea of nine leaves was evaluated for each spore ejection period from late April to early July. All treatments applied in fall1995 and 1996 significantly reduced ascospore production in 1996 and 1997, and there was no significant difference amongtreatments. The most efficient treatment was urea followed by leaf shredding,M. ochracea, andA. bombacina, with reduction inascospore production of 92.1, 85.2, 84.8, and 80.6%, respectively. In 1998 and 1999, highest reduction in ascospore productionwas obtained for combined treatments, i.e. shredding andM. ochracea or shredding and urea, with 93.9 and 90.5% reduction inascospore production, respectively. Apple leaf-shredding in the fall of 1994, 1995 and 1996 significantly reduced emergence ofboth adultP. blancardella and adult parasitoids associated with the leafminer. Leaf-shredding is a sanitation practice that shouldbe systematically done as a long-term tactic as part of a sustainable integrated pest management program in apple orchards.Crown Copyright © 2004 Published by Elsevier B.V. All rights reserved.

Keywords: Physical control; Shredding; Apple scab;Venturia inaequalis; Spotted tentiform leafminer;Phyllonorycter blancardella

1. Introduction

Apple scab,Venturia inaequalis (Cke.) Wint., isa major concern to apple producers (Sivanesan andWaller, 1974). It occurs primarily in temperate zonesof North America, Europe and Asia where springsare cool and humid (Jones and Aldwinckle, 1990).Apple scab is the most important disease of apple(MacHardy, 1996), and it may endanger the entire crop

∗ Corresponding author. Tel.:+1-450-346-4494x202;fax: +1-450-346-7740.E-mail address: [email protected] (C. Vincent).

if appropriate control measures are not applied. Man-agement typically involves 6–14 fungicide treatmentsper season, depending on weather and disease pressure(Köller et al., 1991; Beresford and Manktelow, 1994;MacHardy, 1996; Köller and Wilcox, 1999; Carisseand Dewdney, 2002), which represent up to 10% ofthe apple production costs. In the US, a total of 2 mil-lion kg of fungicides (a.i.) was applied on 140 667 haof apple orchards surveyed in eight states in 2001(U.S.D.A., 2002). In addition, fungicides may haveadverse effects on predacious mites and health con-cerns for both farmers and consumers (Bower et al.,1995; Schneider and Dicker, 1994).

0167-8809/$ – see front matter. Crown Copyright © 2004 Published by Elsevier B.V. All rights reserved.doi:10.1016/j.agee.2004.01.027

596 C. Vincent et al. / Agriculture, Ecosystems and Environment 104 (2004) 595–604

Widely distributed in North America and Europe,the spotted tentiform leafminer (STLM),Phyllono-rycter blancardella (F.) (Lepidoptera: Gracillari-idae), overwinters as a pupa in mined apple leaves(Pottinger and LeRoux, 1971). Synthetic insecticidesused against other pests are the main control tacticsfor STLM (Pree et al., 1994), which has developedresistance to organophosphates and pyrethroids (Pree,1990; Pree et al., 1986, 1994). Many parasitoidsare associated with apple leafminers (Bishop et al.,2001), some of which overwinter with their hostin apple leaves (Pottinger and LeRoux, 1971). Atthe present time, their impact cannot be effectivelymanaged in a commercial context, primarily be-cause of logistic constraints in rearing and releasingthem.

Different strategies of physical control have beenevaluated for apple scab, including pruning to increaseair circulation and to reduce leaf wetness periods,burning leaf litter, and using earthworms to increaseleaf decomposition (Kolbe, 1983). BecauseV. inae-qualis and P. blancardella overwinter mainly in theleaf litter, practices that contribute to destroy fallenleaves should reduce the risks they pose at the set ofa growing season.

When apple leaves are destroyed by shredding,scab-risk may be reduced by 90% in northeasternUSA (Sutton et al., 2000). However, because of op-erational difficulties to shred all the leaves, the actualreduction in scab-risk ranges from 50 to 65%. Themode of action of leaf-shredding is unknown, butconsidering the size of pseudothecia (90–150�), di-rect effect on pseudothecia is unlikely. Combiningleaf-shredding with treatments such as urea or fun-gal antagonists could enhance leaf decomposition,increase microbial competition, or restrain pseudothe-cia maturation (Carisse and Dewdney, 2002; Carisseet al., 2000a). The objective of the present study wasto evaluate the effectiveness of leaf-shredding, ureaand fungal antagonists against apple scab and spottedtentifrom leafminer and its parasitoids.

2. Materials and methods

The experiments were conducted at the experimen-tal farm of Agriculture and Agri-Food, Canada, Fre-lighsburg (45◦03′00′′N–72◦50′00′′W), Que., Canada.

Naturally infected apple (Malus pumila Mill.) leaveswere collected in early October. Cv. ‘McIntosh’was chosen because of its susceptibility to ap-ple scab. Trees had not been sprayed with fungi-cides and all collected leaves showed typical scabsymptoms.

Leaf shredding was done with a commercial shred-der (PolyQuip Turbo Vac, equipped with a 8 hpBriggs and Stratton engine) that produced an averageleaf size of 1.7 cm2 (range: 0.1–6.0 cm2). To esti-mate the size of shredded leaf fragments, a sampleof 500 leaf fragments was collected at random andmeasured using a leaf area meter (Lambda Instru-ments, Li-Cor, Li-3000 and Li-3050A). Urea wasapplied at a rate of about 1 ml per leaf of a 5% so-lution (46% N, 50 g per 1000 ml).Microsphaeropsisochracea Carisse and Bernier was isolated from appleleaf litter in abandoned orchards of Quebec (Bernieret al., 1996; Carisse and Bernier, 2001). A cultureof Athelia bombacina Pers. was obtained from Uni-versity of Wisconsin. Both antagonists were storedin sterilized soil maintained at 2◦C. The fungi werecultured on PDA (Difco Laboratories, Detroit, Michi-gan, USA) at room temperature. Mycelial slurrieswere prepared by homogenizing the fungal culturesin distilled sterile water at a ratio of 60 ml of waterfor each Petri dish with a StomakerTM laboratoryblender (Seward Medical, London, UK). The concen-tration of the inoculum (in cfu) was evaluated from asample of 0.5 ml of inoculum suspension transferredinto 4.5 ml distilled sterile water. The solutions wereplated using serial dilutions on PDA. The final con-centration was (1.8–3.5) × 104 and (1.6–2.87) × 104

colony-forming units (cfu)/ml forM. ochracea andA. bombacina, respectively. For the treatment withM. ochracea andA. bombacina, scabbed leaves wereinoculated with 1 ml of mycelial slurry per leaf. Infall 1995 and 1996 five treatments were compared,i.e. shredded leaves, urea,M. ochracea, A. bombacinaand untreated leaves (control). In fall 1997 and 1998,two treatments were added, i.e. shredded leavestreated with urea and shredded leaves treated withM.ochracea for a total of seven treatments. On 25 Octo-ber 1995, 25 October 1996, 17 October 1997 and 8October 1998, 540 leaves (180 leaves per treatmentper block) were treated and overwintered on the or-chard floor in plastic mesh bags. All treatments wereapplied on the same day in a completely randomized

C. Vincent et al. / Agriculture, Ecosystems and Environment 104 (2004) 595–604 597

block design with three blocks, with five and seventreatments in 1995 and 1996 (ascospore productionmeasured in 1996 and 1997) and in 1997 and 1998(ascospore production measured in 1998 and 1999),respectively.

Ascospore production was evaluated over the entireejection period. In early spring of 1996–1999, nineleaves (or corresponding amount of shredded leaveswhich was calculated as 0.5% of the leaf fragments)were selected at random from each treatment and in-stalled on the wire bottom of a wooden spore trap,ventral face upward. To estimate the amount of as-cospores glass microscope slides coated with a thinlayer of petroleum jelly were placed 0.5 cm above theleaves (Carisse et al., 2000a). The slides were col-lected twice a week and replaced by new ones. Col-lected slides were stored at 10◦C until examination.The number of ascospores was recorded on 40% ofthe trapping surface and reported as the number of as-cospores per slide.

Because the number of treatments differed, datafrom 1996 and 1997 and from 1998 and 1999 were an-alyzed separately. Homogeneity of variance (F-tests)was done to determine if results from the two exper-iments could be pooled and to ensure the underly-ing assumptions of the statistical models. Analysis ofvariance was used to test the effect of fall treatmentson total ascospore production, multiple comparisontests (LSD) were performed to detect significant dif-ferences among means, and orthogonal comparisonswere made to compare different levels of treatmentresults. Because data were collected over time fromthe same leaves and, therefore, were not independent,repeated measures analysis (Manova procedure) wasused to test the effect of fall treatments on ascosporeproduction for each spring sampling date. Statisticalanalyses were conducted using the SAS software (Ver-sion 8, SAS Institute Inc., Cary, NC).

Apple leaves were collected on 31 October and 4November 1994 in a commercial orchard located atDunham (45◦7′59′′N–72◦47′59′′W), Que. The leaveswere randomly assigned to 12 groups (= replicates)of 350 mined leaves each, i.e. six to be shredded andsix to be kept intact (= control). After shredding, eachgroup of leaves was positioned as a complete random-ized block design with six replicates in 45 cm×60 cmquadrats located on the ground underneath a tree ofan orchard composed of ca. 300 ‘Empire’ trees at the

Frelighsburg experimental farm. Within each quadrat,the top 7.5 cm of soil had been removed and sieved(5 mm mesh). The sieved soil was put back over a geo-textile membrane layed in the bottom of the excavatedvolume. On 7 November 1994 each group of leaveswas positioned after treatment on the soil and coveredwith a plastic screen (mesh size= 1.5 mm) to allowSTLM to overwinter and to prevent removal by earth-worms or by the wind. On 10 May 1995, each groupof leaves was transferred to a cardboard box on top ofwhich a funnel with a non-return device allowed thecapture of any adult insect emerging (Bishop et al.,2001). The boxes were placed in an open insectaryand emergence was recorded bi-weekly.

In 1995 and 1996, a third treatment was added totest the effect of decreased leaf surface. All mines weregently cut out with scissors at ca. 2 mm from theiredge. The remaining of the leaf material was shred-ded as in 1994. Both shredded material and cut mineswere mixed and positioned randomly in quadrats foroverwintering studies as previously described.

On 23 and 25 October 1995, leaves were collectedin the same commercial apple orchard. Dissection ofa random sample of 350 leaves showed an average of2.6 mines per leaf. The remaining leaves (i.e. 6300)were randomly assigned to 18 groups (350 per group)that were positioned on 27 October 1995 in the Fre-lighsburg experimental orchard. Three treatments wereconsidered: (1) leaves unshredded (= control); (2)leaves shredded as in 1994; (3) leafminer mines cutout with scissors and mixed with non-mined portionsof shredded leaves. On 26 April 1996, overwinteredleaf material was transferred into emergence boxes asdescribed previously.

On 25 October 1996, leaves were collected in acommercial apple orchard located at St-Jean-Baptiste-de-Rouville (45◦7′52′′N–72◦47′12′′W), Que. Dissec-tion of a random sample of 350 leaves showed anaverage of 3.4 mines per leaf. The remaining leaves(i.e. 6300) were randomly assigned to 18 groups (350per group) that were positioned on 29 October 1996in the Frelighsburg experimental orchard. The treat-ments were as described for fall 1996. On 29 April1997, overwintered leaf material was transferred intoemergence boxes as described previously.

The analysis of variance and Student–Newman–Keuls tests were done with the Software Systat forIBM-Windows computer (Systat, 2002).


3. Results and discussion

A total of 21 647 and 10 751 ascospores weretrapped, respectively, in 1996 and 1997 (Fig. 1). Asthe homogeneity of variance test allowed (P ≥ 0.05),the analysis was conducted on 1996 and 1997 andon pooled data. All treatments significantly reducedascospore production in spring 1996 (P < 0.001)and 1997 (P < 0.0001), respectively, and no signif-icant difference was observed among treatments. In1996, highest reduction in ascospore production wasobtained for apple leaves treated with urea followedby shredding,M. ochracea, and A. bombacina, as-cospores being reduced, respectively, by 96.7, 89.1,84.8, and 82.1%. In 1997, the order of efficacy ofthe fall treatments was different, with ascospores pro-duction reduced by 84.7, 82.8, 77.5, and 77.5% forthe leaves treated withM. ochracea, urea, shreddedand A. bombacina, respectively (Fig. 1). Based on1996–1997 pooled data, the most effective fall leaftreatment was urea followed by leaf shredding,M.ochracea, and A. bombacina, with reduction in as-cospores production of 92.1, 85.2, 84.8, and 80.6%,respectively. The pattern of ascospore ejection overtime was similar on treated and non-treated leaves,

Fig. 1. Total ascospore production during spring 1996 and 1997 from scabbed leaves. Within the same year, bars with the same letters are notsignificantly different according to LSD tests,P < 0.05. ∗Significantly different from control based on orthogonal comparisons (P < 0.05).

with maximum ejection occurring on 17 May 1996and 15 May 1997 (Fig. 2). Repeated measures analy-sis revealed that there was a significant effect of falltreatment (P < 0.0001), time (P < 0.0001), and thatthe effect of fall treatment on ascospore productiondid not vary over time (P ≥ 0.05).

A total of 28 269 and 12 964 ascospores weretrapped in 1998 and 1999, respectively (Fig. 3). Alltreatments significantly reduced ascospore produc-tion in 1998 (P < 0.01) and 1999 (P < 0.0001)(Fig. 3). In 1998 and 1999, highest reduction in as-cospore production was obtained when apple leaveswere shredded and treated withM. ochracea or urea(Fig. 3). In 1999, when leaves were treated with bothA. bombacina and urea, ascospore production wasreduced by less than 80%.

Based on 1998–1999 pooled data, the most effec-tive treatment was shredded leaves treated withM.ochracea or with urea followed byM. ochracea, leafshredding, urea, andA. bombacina: these treatmentscaused reduction in ascospores production of 93.9,90.5, 84.6, 83.0, 73.5, and 70.6%, respectively. For1998–1999, the temporal pattern of ascospore ejec-tion was similar on treated and control leaves, withmaximum ejection on 12 May 1998 and 10 May 1999


Fig. 2. Ascospore production from scabbed leaves treated in the fall. Ascospores measured for each rain, the first sampling dates beingon 8 May 1996 and 31 April 1997.

(Fig. 4). There were significant effects of fall treat-ments (P < 0.0001) and time (P < 0.0001). The ef-fect of fall treatments on ascospore production did notvary over time (P ≥ 0.05).

Overwintering scabbed leaves are known to host theprimary inoculum (Scribner, 1888). A quantitative re-lationship between the amount of scabbed leaves inthe leaf litter and the amount of inoculum was estab-

lished byCurtis (1924). Keitt (1936) suggested thatapple leaves should be destroyed by burning or by disccultivation. Fall application of fungicides such as ben-zimidazole and sterol inhibiting fungicides were alsotested, but are not recommended because of likely de-velopment of resistance inV. inaequalis populations(Keitt and Palmiter, 1937; Keitt et al., 1941; Biggs andWarner, 1990). Sanitation measures disappeared from


Fig. 3. Total ascospore production during spring 1998 and 1999 from scabbed leaves. Within the same year, bars with the same letters arenot significantly different according LSD tests,P < 0.05. ∗Significantly different from control based on orthogonal comparisons (P < 0.05).

the recommendations until 1990 when the effects ofleaf removal were reported byRosenberger (1990).Sutton et al. (2000)calculated that shredding of all ap-ple leaves in November or April resulted in 80–90%reduction of scab risk. However incomplete shreddingreduced scab risk by 50–65% only.

The effect of urea on apple scab was reportedby Ross (1961)who proposed that high amounts ofnitrogen suppressed pseudothecial formation and,consequently, ascospore production.Oland (1963)evaluated post-harvest, pre-leaf fall urea sprays as away to supply nitrogen to the tree and reduce scabrisk. Ross and Burchill (1968), Burchill and Cook(1970), Burchill and Hutton (1965), Gupta and Lele(1980), and Sutton et al. (2000)studied the role ofurea in the inhibition of pseudothecial development,which is not fully understood.Cross et al. (1968)es-tablished that chemical and microbial changes as wellas deterioration of the physical support for pseudothe-cia formation contributed to the loss of ascospores.

Urea enhances microbial populations of appleleaves (Hislop and Cox, 1969). Antagonists were

evaluated on their capacity to reduce the supply of as-cospores when applied in the fall (Carisse et al., 2000a;Heye, 1982; Heye and Andrews, 1983). To reduce as-cospore production withA. bombacina, however, largequantities of inoculum are required, making the treat-ment uneconomical (Miedtke and Kennel, 1990). M.ochracea was evaluated at a rate of 1×1011 spores/haunder large plots or semi-commercial conditions(Carisse et al., 2000a,b) and applications resulted in a71–84% reduction in the production of ascospore thefollowing spring.

Urea and fungal antagonists can be used with othertreatments such as leaf shredding (Gupta and Lele,1980; Ciecierski et al., 1995). Ascospore productionwas reduced by >90% in leaves shredded and treatedwith urea orM. ochracea. Shredding breaks the leavesinto small pieces, which decompose easier and aremore readily eaten by earthworms and small insects.

From an implementation standpoint, shredding ortreatment with urea or fungal antagonists have ad-vantages and disadvantages. Applications of urea orfungal antagonists are easier to make because they


Fig. 4. Ascospore production from scabbed leaves treated in the fall. Ascospores measured for each rain, the first sampling dates beingon 3 May 1998 and 24 April 1999.

can be applied with airblast sprayers. However, thereis no experimental evidence that urea or biofungicideapplications will reduce the inoculum of pathogensother thanV. inaequalis or of insect species other thanleafminers.

From 10 May to 20 June 1995, no adult STLMor parasitoids emerged from the shredded leaves,while an average of 5.8 STLM adults and 16.5 par-asitoids emerged from the control group (Table 1).

Only 0.3 STLM adults emerged in 1996 from shred-ded leaves, while an average of 87.8 emerged fromleaves cut with scissors, a figure not significantly dif-ferent from the control group (108.5 adults) and forparasitoids. The results of 1997 were consistent withthose of 1995 and 1996, except that cut leaves treat-ment resulted in a significant, unexplained, decreasein the number of parasitoids relative to the control(Table 1).


Table 1Average emergence (n = 6 groups of 350 leaves per group) of adult spotted tentiform leafminer and its parasitoids

Year of emergence Treatment Spotted tentiform leafmineradults (average± S.D.)

Adult parasitoids(average± S.D.)

1995 Control 5.83 a± 3.60 16.5 a± 11.95Leaves shredded 0.00 b± 0.00 0.00 b± 0.00

1996 Control 108.5 a± 34.28 9.67 a± 1.03Leaves cut 87.8 a± 13.98 6.67 a± 5.01Leaves shredded 0.3 b± 0.52 0.67 b± 0.52

1997 Control 31.3 a± 9.11 7.7 a± 5.32Leaves cut 24.5 a± 23.61 2.50 b± 2.74Leaves shredded 0.17 b± 0.41 0.00 b± 0.00

Within years and columns, averages flanked by the same letters are not significantly different (Student–Neuman–Keuls test,P < 0.05).

4. Conclusions

Leaf-shredding not only reduces apple scab, butalso affects overwintering STLM populations. This ishinted by the fact that, in apple orchards, there is anegative relationship between earthworm (Lumbricusterrestris L.) populations andP. blancardella and itsparasitoids, notably braconids (Laing et al., 1986). Inexperimental plots, leaf burial by earthworms reducedthe emergence of STLM adults by ca. 95% (Lainget al., 1986). There is no study on non-chemical man-agement tactics for apple leafminers. Leaf-shreddingis non-selective (Vincent et al., 2003), overwinter-ing parasitoid populations and other apple leafminerspecies likeP. crataegella (Clemens) present in NewEngland orchards being also decimated (Maier, 2002).Leaf shredding is likely to be a valuable componentof a sustainable STLM program, and there is potentialfor reducing the inoculum of other diseases, includingAlternaria blotch caused byAlternaria mali Roberts.Nevertheless, depending on the topography of the or-chards and fall weather conditions, it might be difficultto shred enough leaves to have an impact.MacHardy(2004) suggested that after shredding, apple leavesshould be removed from the orchard. However, remov-ing shredded leaves requires additional machinery, andthe benefit of removing leaves may be achieved by ap-plying urea or fungal antagonists such asM. ochracea.Despite the various levels of ascospore inhibition re-ported, urea treatments present several advantages, in-cluding the absence of effects on auxiliary fauna andthe low implementation cost. Furthermore, there is noevidence that the amount of nitrogen applied stimu-

lates and pre-disposes tree growth to winter injury. Theresults were obtained on small plots, but comparableresults are likely be obtained on a larger scale.

Acknowledgements

This study was funded by a Canada Green Planproject 14-066 awarded to C. Vincent and O. Carisse.We thank Chris T. Maier, W.E. MacHardy and DonAylor for commenting an early draft of the manuscript,D. Rolland, S. Bissonnette, N. Larocque, A. Lefeb-vre, and T. Jobin for technical input and J. Andrews(University of Wisconsin) for providing culturesof Athelia bombacina. This is contribution number335/2003.09.02R from the Horticultural Research andDevelopment Centre of Agriculture and Agri-FoodCanada at Saint-Jean-sur-Richelieu.

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