Autumn acaricide applications as a new strategy to control the pear leaf blister mite Eriophyes pyri

ARTICLE IN PRESS

Crop Protection 26 (2007) 1532–1537 www.elsevier.com/locate/cropro

Autumn acaricide applications as a new strategy to control the pear leaf blister mite Eriophyes pyri Claudia Daniela,, Christian Linderb, Eric Wyssa a

Research Institute of Organic Agriculture, Ackerstrasse, Postfach, CH-5070 Frick, Switzerland b Agroscope RAC Changins, CP 1012, CH-1260 Nyon 1, Switzerland

Received 14 September 2006; received in revised form 14 December 2006; accepted 29 December 2006

Abstract The pear leaf blister mite Eriophyes pyri (Pagenstecher) causes severe damage to pear leaves and fruits. As mites are well sheltered from exposure to plant protection agents during summer and acaricide efficacy is reduced when temperatures are low in early spring, autumn acaricide applications were evaluated to control mites as they migrate to their hibernation sites. Post-harvest sulphur and mineral oil treatments were applied in September 2003 and mites were monitored in the following spring. Only the sulphur-treated trees were virtually free of blisters. Sulphur treatments showed an efficacy of 95.3% (one application) to 99.6% (three applications), whereas, mineral oil treatments only had an efficacy of 12.8% (one application) to 69.6% (three applications). That post-harvest sulphur applications could decontaminate heavily infested orchards was possible was confirmed by a large-plot trial in two orchards in 2004/ 2005. r 2007 Elsevier Ltd. All rights reserved. Keywords: Acari; Eriophyes pyri; Eriophyidae; Organic pear growing; Mineral oil

1. Introduction The pear leaf blister mite, Eriophyes pyri (Pagenstecher) (Acari: Eriophyidae), is a serious, regionally and temporally occurring pest in Swiss pear orchards. These tiny mites (body length 0.16–0.2 mm) hibernate in colonies of females under the bud scales of pear trees (Jeppson et al., 1975). In spring, they attack still rolled up young leaves and invade the leaf mesophyll causing blisters on both sides of the leaves usually along the midvein (Baillod and Ho¨hn, 1991). First light green, later red, the blisters finally turn necrotic and black, which leads to a reduced photosynthetic efficiency and to partial leaf fall during August (Easterbrook, 1996). Blisters also occur around the fruit calyx causing fruit deformations and premature fruit fall (Easterbrook, 1996). Eggs are laid and the nymphs develop inside the blisters. The young adults emerge and migrate to form new blisters. The mites occur in 2–4 generations each Corresponding author. Tel.: +41 62 865 72 91; fax: +0041 62 865 72 73. E-mail address: claudia.daniel@fibl.org (C. Daniel).

0261-2194/$ - see front matter r 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2006.12.016

year. After mid-summer and during autumn, the young females return to their hibernation sites (Bovey et al., 1979, Alford, 1992, Friedrich and Rode, 1996). The mites cannot survive more than 4 days outside the blisters (Jeppson et al., 1975). By their hidden way of living inside the leaf blisters, the mites are well protected from the impact of plant protection products. Until now the only strategy to control these mites in pear orchards were applications in early spring (BBCH stage 51–53, Meier, 1997), when the mites leave their hibernation sites under the bud scales and colonize the young leaves. The efficacy of the acaricides dicofol, bromopropylate and azocyclotin in early spring during bud burst was evaluated by Laffi and Ermini (1998). The treatments resulted in a considerable decrease of infestation level but did not provide complete control. Mineral oil (3%) was also tested at bud swelling and gave variable efficacies between 34% and 93% (Laffi and Ermini, 1998). Winter oil treatments showed a good efficacy against the pear rust mite Epitremerus pyri (Nalepa) (Acari: Eriophyidae) but did not provide sufficient control of the pear leaf blister mite Eriophyes pyri (Baillod et al., 1991). In a review, Easterbrook (1996)

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mentions an efficacy of sulphur applications in early spring of 72–87% but, the success of this treatment strongly depends on application time. Predation by phytoseiids mites like Typhlodromus pyri Scheuten and other predators is likely to occur during the migration phase in spring and autumn but its real impact on eriophyid populations is not documented (Easterbrook, 1996). Currently, in Swiss organic pear growing a mineral or rape oil treatment at bud burst is used with variable success to reduce the infestation level while conventional production relies on treatments with mineral oil or rape oil and Diazinon (Delabays et al., 2005). Based on the fact that the mites have to leave their sheltering blisters in late summer, post-harvest applications were tested to control them before they get back to the hibernation sites. The simple and well-known acaricide sulphur was expected to solve blister mite problems during this still warm period. The aims of the present study were: (1) to confirm the acaricidal effect of post-harvest treatments with sulphur, (2) to test different application regimes of sulphur and (3) to compare the effectiveness of sulphur with traditional control approaches in order to develop an alternative control strategy against Eriophyes pyri. 2. Materials and methodes 2.1. Small-plot trial in spring 2003 The aim of the first small-plot trial was to evaluate the efficacy of the organic standard spring treatment with mineral oil. The trial was conducted in a heavily infested, 25-yr old, organically managed pear orchard in Aubonne (southwestern Switzerland, region of Lake of Geneva) in spring 2003. The orchard consisted of 11 rows of approximately 3 m high pear trees with 45 trees per row. The trial was arranged according to the EPPO Standards for the Efficacy

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Evaluation of Plant Protection Products (Anonymous, 2004a) in a completely randomized block design with five replicates (three on variety Conference, two on variety Packham’s) per treatment with four trees per replicate. The treatments were applied to runoff using a high-pressure hand-held gun at stage 51 BBCH and at stage 53 BBCH. Untreated trees served as control. Details of the treatments are given in Table 1. The number of damaged young fruits per 100 fruits per replicate was counted on 23 April (BBCH stage 67–69). Climatic conditions during the trial were monitored using a Campbell CR10X meteorological station. Data were tested for normal distribution and compared by a 3-way ANOVA (variety, block, treatment) using JMP (Version 5.0.1.2). The number of damaged fruit was treated as dependent and treatments as the nominal independent variable. Means were compared by Tukey HSD test. 2.2. Small-plot trial in autumn 2003 The aim of the autumn small-plot trial was to evaluate the efficacy of post-harvest mineral oil and sulphur treatments. The trial was conducted in the same orchard as the trial in spring 2003. The experimental design included five replicates (two on variety Confe´rence, three on variety Packham’s) per treatment with three trees per replicate. Details of the treatments are given in Table 1. Bud samples were examined in the laboratory to estimate the density of mites under the bud scales. For each sample, 10 buds (two randomly chosen shoots with five basal buds each) were opened, thoroughly rinsed in water containing 0.05% Tweens80 (Merck-Schuchardt, Hohenbrunn, Germany), and filtered on black filter paper circles (Schleicher & Schu¨ll, No 551, Dassel, Germany). The number of mites was counted under the microscope (magnification 40  ). One sample per plot was taken in late autumn (06 November

Table 1 Treatments applied in field trials in 2003 and 2004 Product

Concentration/ treatment volume (l/ha)

Number of applications (dates of application)

Small-plot trial in spring 2003 — Mineralo¨l Omya (Omya Schweiz AG, Oftringen, Switzerland)

— 2%/2000l/ha

Control Mineral oil

— 2 (26 February, 12 March 2003)

Small-plot trial in autumn 2003 — Mineralo¨l Omya (Omya Schweiz AG, Oftringen, Switzerland) Mineralo¨l Omya (Omya Schweiz AG, Oftringen, Switzerland) Sulphur (Thiovit Jet; Syngenta Agro AG, Dielsdorf) Sulphur (Thiovit Jet; Syngenta Agro AG, Dielsdorf)

— 2%/2000l/ha 2%/2000l/ha 2%/2000l/ha 2%/2000l/ha

Control Mineral Mineral Sulphur Sulphur

— 1 (10 September 2003) 3 (10, 17, 26 September 2003) 1 (10 September 2003) 3 (10, 17, 26 September 2003)

Large-plot trial in autumn 2004 — Sulphur (Thiovit Jet; Syngenta Agro AG, Dielsdorf) Sulphur (Thiovit Jet; Syngenta Agro AG, Dielsdorf)

— 2%/800l/ha 2%/800l/ha

Control Sulphur 1  Sulphur 2 

oil 1  oil 3  1 3

— 1 (17 September 2004) 2 (17 September, 2 October 2004)

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2003) and one in early spring (17 February 2004). On 21 April (BBCH stage 65) the damage caused by the pear leaf blister mite were visually monitored according to the EPPO Standards for the Efficacy Evaluation of Plant Protection Products (Anonymous, 2004a) on 25 blossom clusters and 25 leaf clusters per plot. Since no EPPO standard for Eriophyes pyri is available the methods described for Aceria sheldoni (Acari: Eriophyidae) (Anonymous, 2004b) were adapted to Eriophyes pyri. Damage was classified into categories (see Table 2). Climatic conditions during the trial were monitored using a Campbell CR10X meteorological station. Data from the bud samples were [lg(x+1)] transformed to obtain normal distribution and compared by a 2-way ANOVA (treatment, variety). Means were compared by Tukey HSD test. From the visually monitored damage categories in spring, the average damage per plot was calculated (mean category of damage over 25 blossom clusters and 25 leaf clusters) in order to obtain normal distribution. These data were compared by a 3-way ANOVA (variety, block, treatment). Means were compared by Tukey HSD test. 2.3. Large-plot trials in autumn 2004 The aim of the large-plot trial was to confirm the results obtained in autumn 2003 under large-scale conditions. The trial was conducted in two organically managed pear orchards in Aesch (North–Western Switzerland, region of Basel) in autumn 2004. Orchard 1 consisted of three rows of 8-yr-old pear trees with 80 trees per row (pear varieties: Williams, Confe´rence and Winternellis). Orchard 2 consisted of four rows of 6-yr-old pear trees with 130 trees per row (pear varieties: Concorde and Confe´rence). In both orchards a block design with three or four replicates (rows), respectively, was arranged. Treated plots comprised 20 (orchard 1) or 30 trees (orchard 2) each; control plots comprised 35 (orchard 1) or 55 trees (orchard 2) each. The treatments were applied to runoff using a tractor-mounted air-blast sprayer. Details of the treatments are given in Table 1. To assess the primary infestations, a visual examination of the leaves at the base of young shoots was conducted on 17 September 2004. The level of infestation for each tree as a whole was classified into categories (Table 2) on each of the 240 trees. On 21 April (BBCH stage 61) the damage

caused by the pear leaf blister mite was visually monitored on 10 trees per plot (five randomly selected blossom clusters per tree). Damage was classified into categories (Table 2). To obtain normal distribution, the average damage per plot was calculated (mean category of damage over 50 blossom clusters). Data of primary infestation were compared by a 2-way ANOVA (orchard, variety). The data from the visual control on 21 April were pooled over the two orchards and compared by a 3-way ANOVA (variety, orchard, treatment). Means were compared by Tukey HSD test. 3. Results 3.1. Small-plot trial in spring 2003 The temperature during the experimental period (25 February and 19 March 2003) averaged 5.9 1C (Tmax ¼ 13.3 1C; Tmin ¼ 1.2 1C), and the relative humidity averaged 65.5%. The infestation level was not influenced by pear variety (F1,4 ¼ 2.58, Pvariety ¼ 0.1832) whereas, blocks had a significant effect (F3,4 ¼ 16.93, Pblock ¼ 0.0097). The infestation level in two blocks in the centre of the orchard was significantly lower than in the two blocks at the border. The mineral oil treatment significantly reduced the number of damaged young fruits (F1,4 ¼ 71.87, Ptreatment ¼ 0.0011; Fig. 1) and showed an efficacy of 60.5% (Abbott’s formula, Abbott, 1925). 3.2. Small-plot trial in autumn 2003 The temperature during the experimental period (09 September and 03 October 2003) averaged 14.8 1C (Tmax ¼ 26.5 1C; Tmin ¼ 7.8 1C), and the relative humidity averaged 77.3%. The mites examined from the bud samples were determined to the level of genus (Eriophyes ssp.). No additional mite genera were found. In late autumn (06 November 2003), the mineral oil and sulphur treatments showed significantly lower numbers of Eriophyid mites under the bud scales than the untreated control (F4,19 ¼ 9.22, Ptreatment ¼ 0.0003; Fig. 2). This resulted in an efficacy of 88.0% for ‘‘mineral oil 1  ’’, 96.9% for ‘‘mineral oil 3  ’’, 98.0% for ‘‘sulphur 1  ’’ and 99.8% for ‘‘sulphur 3  ’’ (Abbott’s formula). The pear variety

Table 2 Categories of damage by Eriophyes pyri on pear Category

Symptoms during flowering

Symptoms during autumn

0 1 2 3

Unharmed, no blisters 1–15% of the leaf and calyx surface covered with blisters 15-40% of the leaf and calyx surface covered with blisters 440% of the leaf and calyx surface covered with blisters, leaves developed and unfolded; blossoms opened Youngest leaves completely red, rolled up, stunted; blossoms heavily infested and not opened

Unharmed, no blisters 1–15% of leaf surface covered with blisters 15–40% of the leaf surface covered with blisters 440% of the leaf surface covered with blisters. Separated blisters Merged blisters, leaves completely necrotic and black

4

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had a significant influence on the number of mites (F1,19 ¼ 4.41, Pvariety ¼ 0.05). The variety Confe´rence showed higher mite densities than the variety Packham’s. The bud samples taken in spring (17 February 2004) did not show any influence of pear variety on mite numbers (F1,19 ¼ 0.16, Pvariety ¼ 0.69). Concerning the effect of the treatments, the significant differences found on 06 November 2003 were confirmed on 17 February 2004 (F4,19 ¼ 16.38, Ptreatmento0.0001; Fig. 2). The efficacy was 99.7% for ‘‘mineral oil 1  ’’, 97.5% for ‘‘mineral oil 3  ’’, 100.0% for ‘‘sulphur 1  ’’ and 99.9% for ‘‘sulphur 3  ’’ (Abbott’s formula). At the visual examination on 21 April 2004 pear trees were flowering (BBCH stage 65) and the damage caused by the pear leaf blister mite was clearly visible. Leaf and blossom clusters showed comparable infestation rates (Fig. 3) and were pooled for statistical analysis. Both

On 17 September 2004, the primary infestation was visually monitored. In both orchards more than 96% of the trees showed damage caused by the pear leaf blister mite.

90

3.5 Category of damage

a

70 60 50

b

40 30

2

1

0

20

a

14 12 10 8 b

4

b

b

b

2 0

Control

Control

Mineral oil Mineral oil 1x 3x

Sulphur 1x

Sulphur 3x

Mineral oil 1x

Mineral oil 3x

Sulphur 1x

b

Sulphur 3x

Fig. 3. Effect of post-harvest treatments with mineral oil and sulphur on the damage caused by Eriophyes pyri (+SD) in spring 2004. Statistical analysis: 3-way ANOVA over average damage of leaf and blossom clusters; Tukey HSD test, a ¼ 0.05; different letters show significant differences.

100

16

6

b

Mineral oil

06 November 2003

18

b

1.5

10

Fig. 1. Effect of mineral oil treatment on mean number of damaged young fruits (+SD) in a small-plot trial in Aubonne on 23 April 2003 (BBCH stage 67–69). Statistical analysis: 3-way ANOVA; Tukey HSD test, a ¼ 0.05; different letters show significant differences.

blossomclusters

a

2.5

0.5

Control

leafclusters

a

3

20

Number of Eriophyes ssp. per bud

% damaged fruits

3.3. Large-plot trial in autumn 2004

4

0

Number of Eriophyes ssp. per bud

autumn sulphur treatments (‘‘sulphur 1  ’’, ‘‘sulphur 2  ’’) and the treatment ‘‘mineral oil 3  ’’ significantly reduced the damage in spring (F4,15 ¼ 48.70; Ptreatmento0.0001), whereas the treatment ‘‘mineral oil 1x’’ did not show significant differences compared to the untreated control. The treatments showed efficacies of 12.8% for ‘‘mineral oil 1  ’’, 69.6% for ‘‘mineral oil 3  ’’, 95.3% for ‘‘sulphur 1  ’’ and 99.6% for ‘‘sulphur 3  ’’ (Abbott’s formula). Infestation level was not influenced by pear variety (F1,15 ¼ 4.04, Pvariety ¼ 0.0628) or block (F4,15 ¼ 1.82, Pblock ¼ 0.1773).

100 80

1535

90

17 February 2004

a

80 70 60 50 40 30 b

20

b

b

b

Sulphur 1x

Sulphur 3x

10 0

Control

Mineral oil Mineral oil 1x 3x

Fig. 2. Effect of post-harvest treatments with mineral oil and sulphur on the mean number of Eriophyes ssp. per bud (+SD) in late autumn and early spring. Statistical analysis: Data transformed [lg(x+1)], 2-way ANOVA; Tukey HSD test, a ¼ 0.05; different letters show significant differences.

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4

blossom clusters

Category of damage

3.5 3

a

2.5 2 1.5 1 0.5 0

Control

b

b

Sulphur 1x

Sulphur 2x

Fig. 4. Effect of post-harvest sulphur treatments on the damage caused by Eriophyes pyri (+SD) in spring 2005. Statistical analysis: 3-way ANOVA; Tukey HSD test, a ¼ 0.05; different letters show significant differences.

Concerning the category of damage no significant differences between the two orchards and the plots were observed (2-way-ANOVA, F1,30 ¼ 0.38, Porchard ¼ 0.54; F3,30 ¼ 0.71, Pvariety ¼ 0.55). The visual examination on 21 April 2005 (BBCH stage 61) showed a significant effect of treatment (F2,28 ¼ 80.92; Ptreatmento0.0001; Fig. 4) but no effect of variety (F3,28 ¼ 1.91, Pvariety ¼ 0.15). The infestation level in orchard 2 was higher than in orchard 1 (F1,28 ¼ 4.77, Porchard ¼ 0.04). The treatments showed efficacies of 94.0% for ‘‘sulphur 1  ’’ and 93.3% for ‘‘sulphur 2  ’’ (Abbott’s formula). In the control plots 88.5% of the blossom clusters were damaged by the pear leaf blister mite, whereas in the sulphur treated plots only 7.7% (‘‘sulphur 1  ’’) and 8.3% (‘‘sulphur 2  ’’) of the blossom clusters showed any symptoms of pear leaf blister mite infestation.

4. Discussion The trial in spring 2003 demonstrated that the standard organic strategy, mineral oil applications in early spring, is not sufficiently effective. Although, the treatments significantly reduced the pear leaf blister mite population, still 23.6% of young fruits were damaged (control plots: 59.8%). These results correspond with similar assessments in Italy (Laffi and Ermini, 1998). Therefore, new strategies to control the pear leaf blister mite in organic fruit growing are needed. With this objective, post-harvest sulphur treatments were conducted to protect pear trees against infestations of Eriophyes pyri in the following spring. With an efficacy of up to 100% (Abbots formula) even a decontamination of heavily infested orchards is possible. This type of postharvest treatment is valuable for the control of the pear leaf blister mite in two different climatic regions in Switzerland (region of the lake of Geneva and the region of Basel). No

significant differences were found between the single and repeated sulphur treatments. The acaricidal effect of the different sulphur formulations has been known since 1920 (Yothers, 1915, Goodwin and Martin, 1928) and they are widely used to control different Eriophyid mite pests in tomato (Tuft and Anderson, 1953), mango (Muniappan and Rajendran, 1989), citrus (Yothers, 1915), tea (Rao, 1970) and grapevine (Keiffer, 1946, Paris and Didier, 1963, Goebel et al., 2001, Bernard et al., 2005) production. Likewise, the minimal temperature of 17 1C, which is needed to produce an acaricidal effect of sulphur, has been known for many years (Klett, 1969, Auger et al., 2003). Hence, sulphur treatments in spring were not tested, since the average temperature of 5.9 1C during this period was clearly under the minimal temperature. The climatic conditions during the post-harvest period are much more favourable (average temperature: 14.8 1C). Moreover, humidity in autumn is higher than in spring. As shown in laboratory studies by Auger et al. (2003) a higher humidity intensifies the effect of sulphur against mites (Tetranychus urticae). The bud samples taken from the control plots in late autumn 2003 and early spring 2004 showed high variations in the number of mites per bud. Moreover, the number of mites per bud did not correspond with the infestation level in spring (Daniel et al., 2004): in particular the mineral oil treated trees yielded only a few mites under the bud scales but showed a high infestation level in spring. Since there is a high variability among the buds, we might have overlooked existing differences due to too small sample size. However, increasing the sample size to obtain a reliable estimation would lead to an amount of work which cannot be tackled. Therefore, the examination of bud samples is not a convenient forecasting method. Consequently, an economic threshold level should be established according to leaf damage in the previous year to facilitate the decision for treatments. All trials were conducted in organic orchards with an intense sulphur spraying schedule in summer. The normal spraying schedule against pear scab Venturia pirina (Ascomycotina: Venturiaceae) comprises 8–10 weekly treatments of 3 kg sulphur per hectare between April and July. Since these orchards were heavily infested by Eriophyes pyri, it can be assumed that the mites inside the blisters are well protected from the impact of sulphur during summer. However, a single application at a higher dosage (2%; i.e. 16 kg/ha) during migration in autumn significantly reduced infestation level. In Switzerland sulphur is registered at similar dosages (10–15 kg/ha) for the control of Calepitrimerus vitis Nalepa (Acari: Eriophyidae) in grape and Acalitus essigi (Hassan) (Acari: Eriophyidae) in blackberry during bud burst in spring. The influence of post-harvest sulphur treatments on predatory mites could not be evaluated in these trials. Phytoseiids mites such as T. pyri are much less numerous on pears than on apple which is usually linked with pesticides programs and lack of pilosity of the leaves of

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the main commercial varieties (Baillod et al., 1992, Easterbrook, 1996). Summer sulphur applications are classified as moderately harmful to T. pyri by Delabays et al. (2005) and may have an impact on phytoseiids but, in late September most of the predatory mites have already moved to their overwintering sites (Overmeer, 1985) and negative side effects of post-harvest sulphur treatments are less likely to occur. In conclusion, a post-harvest application of sulphur is a promising and suitable method to control Eriophyes pyri and to decontaminate heavily infested orchards. This strategy is a viable alternative to the strategies commonly used to control E. pyri in organic and conventional pear orchards. Acknowledgements We thank C. Suter and P. Nussbaumer for permitting the trials to be conducted within their orchards, and two anonymous referees for comments on earlier versions of the manuscript. For statistical advice we are grateful to the statistical advisory service of Swiss Federal Institute of Technology Zurich (ETH Zu¨rich). References Abbott, W.S., 1925. A method for computing the effectiveness of an insecticide. J. Econ. Entomol. 18, 265–267. Alford, D.V., 1992. Farbatlas der Obstscha¨dlinge. Enke Verlag, Stuttgart. Anonymous, 2004a. EPPO Standards—Efficacy Evaluation of Plant Protection Products—Volume 1 General Standards. OEPP/EPPO, Paris, France. Anonymous, 2004b, EPPO Standards—Efficacy Evaluation of Plant Protection Products—Volume 3 Insecticides and acaricides, Guideline PP1/87(2): 113–115, OEPP/EPPO Paris, France. Auger, P., Guichou, S., Kreiter, S., 2003. Variations in acaricidal effect of wettable sulphur on Tetranychus urticae (Acari: Tetranychidae): effect of temperature, humidity and life stage. Pest. Manage. Sci. 59, 559–565. Baillod, M., Ho¨hn, H., 1991. Eriophyides des fruits a` pe´pin (pommier, poirier). Rev. Suisse Vitic. Arboric. Hortic. 23, 39–40. Baillod, M., Oppikofer, A., Antonin, P., 1991. Roussissure des poires cause´e par l‘e´riophyide libre du poirier, Epitrimerus pyri (Napalea), en Valais. Rev Suisse Vitic Arboric Hortic. 23, 87–92. Baillod, M., Erard, F., Antonin, P., Sta¨ubli, A., 1992. Distribution, methods de controˆle, estimation du risque´ pour Panonychus ulmi (Koch) et Tetranychus urticae Koch en vergers de poirires et incidence

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