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Effect of botanically derived pesticides on mirid pests and beneficials in apple
Crop Protection 28 (2009) 309–313
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Effect of botanically derived pesticides on mirid pests and beneficials in apple Gunnhild Jaastad a, *, Nina Trandem b, Berit Hovland a, Sigrid Mogan c a
Norwegian Institute for Agricultural and Environmental Research – Bioforsk Horticulture and Greening Division, Ullensvang, 5781 Lofthus, Norway Norwegian Institute for Agricultural and Environmental Research – Bioforsk Plant Health and Plant Protection Division, Høgskoleveien 7, 1432 Ås, Norway c The Norwegian Agricultural Extension Service, Foss gård, Stokkeveien 4, 3400 Lier, Norway b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 February 2008 Received in revised form 11 November 2008 Accepted 12 November 2008
Mirid bugs (Hemiptera: Miridae) are important pests in apple and pear production in both Europe and the United States. Mirids feed on sap in shoot tips, flower buds and fruitlets, resulting in deformation and stony pits in the fruit. Due to withdrawal of pesticides and concern about the environment alternative control methods against capsids are needed. In this study the effect of neem extract (NeemAzal), garlic extract (Ecoguard), vegetable oil (soybean or rapeseed) and kaolin (Surround) were evaluated for their effect on populations and damage of mirids in apples. Results show that neem extract is a promising alternative, giving as good control of mirid damage as several synthetic pesticides. Kaolin, garlic extract and vegetable oil did not significantly reduce damage. Many omnivorous species were present in the experimental orchards, and a positive correlation between the numbers sampled and fruit damage indicated that several of them could be pests. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Miridae Garlic extract Neem extract Vegetable oil Kaolin Apple
1. Introduction Mirid bugs (Hemiptera: Miridae) are important pests in apple and pear production in both Europe and the United States (Wheeler, 2001; Alford, 2007). In organic production the degree of fruit damage might exceed 40% (Røen et al., 2003). Mirid bugs feed on sap in shoot tips, flower buds and fruitlets, resulting in deformation and stony pits in the fruit (Wheeler, 2001). Mirids damaging fruit are usually both polyphagous and omnivorous, and it can be difficult to assess whether a species should be considered as pest or beneficial. Two species unanimously regarded as apple pests in Northern Europe are Lygocoris pabulinus (Linnaeus) and Lygocoris rugicollis (Falle´n) (Schøyen and Jørstad, 1956; Alford, 2007; Wheeler, 2001). Among species considered beneficial due to their predation of pest insects and mites are Phytocoris longipennis Flor and Blepharidopterus angulatus (Falle´n) (Sørum, 1977a; Edland, 2004; Wheeler, 2001). A third category is species which are mainly predacious, but occasionally cause damage because they are able to feed on plants, e.g. Orthotylus marginalis Reuter, Plagiognathus arbustorum (Fabricius), Psallus ambiguus (Falle´n) and Atractotomus mali (Meyer-Du¨r) (Taksdal, 1983; Jonsson, 1987; Wheeler, 2001; Edland, 2004).
* Corresponding author. Tel.: þ47 95902678. E-mail address: [email protected] (G. Jaastad). 0261-2194/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2008.11.006
Most mirids that cause fruit damage overwinter as eggs and hatch before blossom. The damage is mainly done by nymphs feeding on fruitlets (Jonsson, 1985; Weeler, 2001). Due to withdrawal of synthetic insecticides, concern about the environment, increased organic production and development of insecticide resistance, alternative control methods are needed (Isman, 2006). Several botanically derived pesticides give effective control of insect pests, but few have been systematically tested on heteropterans. Azadirachtin, neem extract, is a botanical pesticide with several modes of action. It has an antifeedant/repellent effect, it disrupts moulting by inhibiting ecdysone production, and it may disrupt normal mating behaviour (Schmutterer, 1990; Copping, 2004; Isman, 2006). Mineral or vegetable oil has been used in decades against dormant insect and mite pests (Chapman et al., 1941; Chapman and Pearce, 1949; Schøyen and Jørstad, 1956; Chapman, 1967). Oils work through a mechanical interference with the gaseous exchange in eggs (Smith and Pearce, 1948) and probably also by blocking spiracles in young and adult arthropods (Cranshaw and Baxendale, 2005). In addition, vegetable oil sprays are often emulsified by soft soaps containing oleic acid that destroy cell membranes (Copping, 2004). Garlic extract has been shown to both cause mortality and to repel insects (Copping, 2004; Prowse et al., 2006). Kaolin is not a botanical extract, but a natural clay mineral (aluminosilicate), creating a physical barrier to infestation by impeding movement, feeding and egglaying (Cottrell et al., 2002). Several fruit tree pests have shown to be suppressed by kaolin (Glenn et al., 1999; Mazor and Erez, 2004; Bu¨rgel et al., 2005; Puterka et al., 2005; Marko´ et al., 2008).
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The main objective of this study was to evaluate the effect of azadirachtin (NeemAzal), vegetable oil, garlic extract (ECOguardÒ) and kaolin (SurroundÒ) on the mirid fauna in apple trees. 2. Materials and methods Experiments were conducted in two apple orchards, one integrated orchard in Ullensvang, Western Norway, and one organic orchard in Lier, South-Eastern Norway. The experiments were set up as randomized block designs with four or five replications. In each plot there were 3 trees of Aroma, and a minimum of 2 border trees between each plot. Pesticides were applied till run-off with a hand-held lance connected to a wheelbarrow or tractor boom sprayer (spray volume approximately 1000–2000 l/ha). Spray volume and dose applied per treatment and trial was measured, and g.a.i. per ha calculated. Treatments, dosages and application times per trial are given in Table 1. The integrated orchard trials were conducted in 2004 and 2005. The orchard (0.4 ha) was planted in 1994 with tree spacing 4.5 1.5 m. Azadirachtin (NeemAzal TS, active ingredient 10 g/l, Trifolio-M GmbH, Germany) was compared to an untreated control and three synthetic pesticides: fenthion (Lebaycid, a.i. 535 g/l, Bayer AG, Germany), phosalone (Zolone Flo, a.i. 500 g/l, Cheminova AS, Denmark) and diflubenzuron (Dimilin SC-48, a.i. 480 g/l, Crompton Europe B.V., Netherlands). The organic orchard trials were conducted in 2004, 2005 and 2006. Planting year was 1988, and tree spacing 4.5 1.5 m. The orchard was 0.5 ha in area. An untreated control was compared to several concentrations and applications of azadirachtin, vegetable oil (soybean oil, Mills, in 2004, and rapeseed oil, Askim, Norway, in 2005) mixed with soft soap (grønnsåpe, Lilleborg, Norway), garlic extract (ECOguardÒ, 99.9% active ingredient, ECOspray Ltd, Northfolk, England) and kaolin (SurroundÒCF, 95% active ingredient; Engelhard Corporations, Iselin, NJ). The mirid fauna was sampled by beating three random branches on every tree in each plot with a stiff rubber hose one week after
the last spray application. Each branch received three quick beats, and dislodged insects were collected by a beating tray (Sutherland, 1996). All insects were identified and counted, but only mirids and anthocorids are shown here. All mirids collected were 3rd to 5th instar nymphs while the majority of anthocorids were adults. Fruit damage was evaluated by randomly picking 100 apples from each plot. Fruit damage was classified according to Rein (1996). Data were analysed by analysis of variance (ANOVA) with treatment and block as explanatory variables (SAS Institute, 1990, 2003). Number of mirids was square-root transformed (O(x þ 0.5)) prior to analysis because standard deviations were proportional to the means (Zar, 1984). Proportion of damaged apples was arcsin transformed prior to analysis (Zar, 1984). For variables that explained a significant part of the variance, Tukey’s test was used to analyse differences between means (Zar, 1984). A Pearson correlation analysis between damage and the number of individuals of each species was performed to get an indication of which species were most harmful to apples. 3. Results Azadirachtin had an effect on both mirid numbers and damage (Tables 2–4). Compared to the untreated control, the numbers of L. pabulinus, O. marginalis, A. mali and P. ambiguus were significantly reduced by azadirachtin treatment in several trials (Tables 2 and 3). Furthermore, application of azadirachtin significantly reduced damage in both years of trials in the integrated field, and in the first year of trials in the organic field (Table 4). Also in the two following years, there was a tendency of less damage in the azadirachtin treated plots of the organic field, although this was not significant. In the trials including one and two applications, different concentrations, or different application times with azadirachtin, no significant differences in damage between these were found (Table 4). When azadirachtin was compared to synthetic pesticides, no statistical difference in either number of mirids or damage was
Table 1 Treatments, doses and application times in the five trials. Spray volume was 1000–2000 l/ha. Field
Year
Treatment (Ô)
Dose/100 l
g.a.i/ha 1st application
g.a.i/ha 2nd application
Application date
Application time BBCHa
Integrated
2004
Fenthion (Lebaycid) Phosalon (Zolone Flo) Diflubenzuron (Dimilin) Azadirachtin (NeemAzal) 2 Control Fenthion (Lebaycid) Phosalon (Zolone Flo) Diflubenzuron (Dimilin) Azadiracthin (NeemAzal) 2 Control
10 ml 100 ml 30 ml 500 ml – 10 ml 125 ml 30 ml 500 ml –
200 1850 640 170 – 130 2720 540 210
– – – 150 – – – – 120 –
1.06 1.06 22.05 22.05 þ 1.06 – 13.06 19.05 31.05 31.05 þ 13.06 –
67 67 65 65 þ 67 – 67 60 65 65 þ 67 –
Vegetable oil (Soybean oil)b Azadiracthin (NeemAzal) Azadiracthin (NeemAzal) 2 Control Vegetable oil (Rapeseed oil)b Azadiracthin (NeemAzal) Azadiracthin (NeemAzal) 2 Azadiracthin (NeemAzal) 2 Garlic extract (Ecoguard) Control Azadiracthin (NeemAzal) Azadiracthin (NeemAzal) 2 Garlic extract (Ecoguard) Garlic extract (Ecoguard) Kaolin (Surround) 2 Control
4000 ml 500 ml 500 ml – 3000 ml 500 ml 500 ml 300 ml 2000 ml – 250 ml 250 ml 2000 ml 2000 ml 3000 mg –
67 l oil 80 80 – 33 l oil 60 60 40 28,440 – 30 30 32,000 40,280 35,625 –
– – 80 – – – 50 40 – – – 40 – – 44,333 –
2.05 19.05 19.05 þ 27.05 – 19.05 27.05 27.05 þ 7.06 27.05 þ 7.06 15.06 – 3.06 3.06 þ 9.06 24.05 3.06 24.05 þ 3.06 –
54 65 65 þ 67 – 57 65 65 þ 67 65 þ 67 69 – 65 65 þ 67 57 65 57 þ 65 –
2005
Organic
2004
2005
2006
a Developmental stage according to Meier et al. (1994), BBCH 54 ¼ tight cluster, BBCH 57 ¼ white tip, BBCH 59 ¼ balloon, BBCH 61 ¼ first blossom, BBCH 65 ¼ full blossom, BBCH ¼ start petal fall, BBCH 69 ¼ petal fall. b Soft soap (ca 1000 ml/100 l) added as emulsifier.
G. Jaastad et al. / Crop Protection 28 (2009) 309–313
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Table 2 Mean std number (untransformed data) of mirids and Anthocoris nemorum per plot recorded by beating tray samples in different treatments in the organic orchard in 2004–2006. Treatment
2004 (n ¼ 5) Controlb Azadirachtin Azadirachtin Soybean oil Correlationc 2005 (n ¼ 4) Control Azadirachtin Azadirachtin Azadirachtin Rapeseed oil Garlic extract Correlation 2006 (n ¼ 4) Control Azadirachtin Azadirachtin Garlic extractd Garlic extracte Kaolin Correlationc
Dosea
– 500 ml 500 ml 2 4000 ml
500 ml 500 ml 2 300 ml 2 3000 ml 2000 ml
250 ml 250 ml 2 2000 ml 2000 ml 3000 mg 2
Mean std number per plot Lygocoris pabulinus
Lygocoris rugicollis
Orthotylus marginalis
Plagiognathus arbustorum
Psallus ambiguus
Atractotomus mali
Anthocoris nemorum
Mean
std
Mean
std
Mean
Mean
Mean
std
Mean
Mean
4.8 1.0 0.8 3.8 0.14 ns
5.7 1.7 1.3 1.6
0.8 0.6 0.0 0.2 0.08 ns
1.5 1.3 0.0 0.4
0.3 0.2 0.0 0.8 0.26 ns
0.5 0.4 0.0 0.4
2.8 2.3 0.8 2.3 2.3 4.3 0.22 ns
2.2 3.9 1.0 1.0 1.7 4.7
a a a a a a
0.8 0.3 0.0 0.3 1.3 0.3 0.43 p ¼ 0.03
1.0 0.5 0.0 0.5 0.5 0.5
9.0 2.8 4.0 3.5 3.3 3.5 0.27 ns
6.4 1.5 2.2 1.9 2.1 3.7
a a a a a a
16.3 2.5 1.3 2.8 6.5 6.0 0.27 ns
4.9 2.4 1.0 1.9 4.2 6.7
a a a a
16.3 5.9 1.5 0.6 0.5 0.6 1.0 0.8 7.5 6.5 5.0 2.4 0.54 p ¼ 0.006
a bc c c ab bc
2.0 1.8 0.0 0.0 0.8 1.0 0.8 1.0 2.0 0.8 1.3 1.5 0.77 p < 0.0001
4.5 1.5 0.5 4.8 13.8 8.8 0.46 p ¼ 0.02
ab b b ab a ab
0 0 0 0 0 0 –
3.9 2.4 1.0 5.6 8.2 5.6
a a a a
a a a a a a
std
7.0 1.2 1.4 8.0 0.51 p ¼ 0.03
4.5 1.6 0.5 6.3
3.3 0.0 0.0 0.0 0.8 3.8 0.16 ns
3.3 0.0 0.0 0.0 1.5 4.3
14.3 1.0 0.0 0.5 0.5 1.0 0.39 ns
10.4 2.0 0.0 1.0 1.0 2.0
a b b a
std
0.3 0.6 0.4 0.6 0.19 ns
0.5 0.9 0.9 1.3
a a a a a a
0.5 0.0 0.0 0.0 1.3 0.3 0.14 ns
1.0 0.0 0.0 0.0 2.5 0.5
a b b b b b
0 0 0 0 0 0 –
a a a a
a a a a a a
ab ab a b
std 0 0 0 0
std
2.2 1.0 1.4 1.2 0.10 ns
2.0 1.0 1.1 1.1
a a a a
ab ab b ab a ab
0.0 0.0 0.3 0.0 0.3 0.0 0.21 ns
0.0 0.0 0.5 0.0 0.5 0.0
a a a a a a
a b b b b b
1.5 0.8 1.0 0.3 0.5 0.8 0.37 ns
3.0 1.0 2.0 0.5 0.6 1.5
a a a a a a
–
Different letters within columns and year indicate significantly different means (square-root transformed data) (Tukey’s test, p < 0.05). a Dose of product/100 l. b n ¼ 4. c Pearson correlation coefficient between number of capsids and damage. d Application time BBCH 57 (Meier et al., 1994). e Application time BBCH 65 (Meier et al., 1994).
found between azadirachtin treated trees and trees treated with fenthion (Tables 3 and 4). However, azadirachtin was more effective than phosalon and diflubenzuron in 2004 (Table 4). In 2005, only azadirachtin and diflubenzuron treated plots had significantly fewer damaged apples than control plots. No mirid species was significantly suppressed by vegetable oil (Table 2) and neither treatment with soybean oil nor rapeseed oil had any effect on damage (Table 4). Neither an early nor a late application of garlic extract significantly reduced fruit damage compared to the untreated control (Table 4). Garlic extract did, however, significantly reduce the number of L. pabulinus in 2005 and the number of O. marginalis and A. mali in 2006 (Table 2). Kaolin treatment significantly reduced the number of O. marginalis and A. mali, however no effect on damage was found. In the correlation analysis between number of individuals and damage in every plot (regardless of treatment) a significant positive relationship was found for the following species (Tables 2 and 3): L. pabulinus (in three of the five trials in total); L. rugicollis, O. marginalis and P. ambiguus (in two trials); P. arbustorum and A. mali (in one trial). In contrast, numbers of the well-known predators Anthocoris nemorum (Linnaeus) and P. longipennis were not correlated with damage in any of the trials (Tables 2 and 3). 4. Discussion Of the botanical pesticides we tested, azadirachtin was clearly the most efficient. The effect was also similar or better compared to the synthetic pesticides included in the experiments. Similar results have been obtained by others. Palm and Hauschildt (2003)
compared azadirachtin to several synthetic pesticides over 4 years, and the results showed an efficiency of 4–90% regarding mirid damage to apples. However, mirid species and number of replicates were not given in their report. Furthermore, Dorn et al. (1986) demonstrated that azadirachtin prevented moulting and increased the percentage of nymphs that died without moulting in the milkweed bug (Oncopeltus fasciatus (Dallas)). Tedeschi et al. (2001) found that neem formulations increased mortality in the predatory mirid Macrolophus caliginosus Wagner. In our study azadirachtin did not significantly affect the most important predatory hemipterans, A. nemorum and P. longipennis, while the omnivorius P. ambiguus and A. mali, mainly regarded as beneficials, were negatively affected by azadirachtin treatment. However, our findings indicate that both P. ambiguus and A. mali are causing damage to apples as the number of both species was positively correlated to damage. This is supported by Taksdal (1983), who showed that P. ambiguus can cause stony pits in pears. Based on our results, one treatment with azadirachtin at a concentration of 250–300 ml/100 l gives the same control as higher doses and two treatments. The lack of effect by vegetable oil treatment might be due to only the operculum of capsid eggs being visible on the plant, i.e. little of the total egg surface being exposed. Oil treatment is effective against over wintering eggs of other pest species such as aphids and spider mites (Pless et al., 1995; Jaastad, 2007). However, these eggs are fully exposed on the plant surface. Rapeseed oil was applied later in the season than soybean oil, however no clear differences between these two application times were found. Different timings of vegetable oil treatment were, however, not compared within trials.
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Table 3 Mean std number (untransformed data) of mirids and Anthocoris nemorum per plot recorded by beating tray samples in different treatments in the integrated orchard in 2004–2005. Treatment
Dosea
Mean std number per plot (n ¼ 5) Lygocoris pabulinus
Lygocoris rugicollis
Mean
std
–
3.2
1.3
Fenthion
10 ml
0.0
Phosalone Diflubenzuron Azadirachtin Correlationb
100 ml 30 ml 500 ml 2
0.6 1.6 0.0 0.55 p ¼ 0.005
2004 Control
2005 Control Fenthion Phosalone Diflubenzuron Azadirachtin Correlationb
– 10 ml 125 ml 30 ml 500 ml 2
0.6 0.0 0.4 0.4 0.2 0.02 ns
Orthotylus marginalis
Plagiognathus arbustorum
Psallus ambiguus
Phytocoris longipennis
Anthocoris nemorum
Mean
std
Mean
std
Mean
std
Mean
std
Mean
std
11.9
ab
3.8
1.6
a
1.1
b
3.2
2.0
a
Mean
std
a
0.8
1.3
a
2.2
1.9
ab
3.4
2.4
a
3.6
1.9
a
12.6
0.0
b
0.2
0.4
a
0.2
0.4
b
0.4
0.5
a
0.6
0.5
a
1.2
0.9 1.8 0.0
b ab b
0.2 0.0 0.0 0.08 ns
0.4 0.0 0.0
a a a
3.4 2.3 1.4 1.5 0.2 0.4 0.56 p ¼ 0.004
a ab b
4.0 4.2 1.8 1.8 1.2 1.6 0.45 p ¼ 0.02
a a a
1.2 1.6 5.0 4.5 1.2 1.3 0.50 p ¼ 0.01
a a a
7.6 21.2 7.6 0.26 ns
8.4 10.6 5.1
ab a ab
4.6 3.4 2.8 0.15 ns
3.2 3.2 0.8
a a a
0.5 0.0 0.5 0.5 0.4
a a a a a
0 0 0 0 0 –
1.0 0.0 0.8 0.8 0.0 0.36 ns
a a a a a
0 0 0 0 0 –
5.8 3.8 1.6 1.3 3.2 2.6 3.4 1.9 0.0 0.0 0.53 p ¼ 0.006
a ab ab a b
1.6 0.4 1.4 1.0 0.4 0.30 ns
2.3 0.5 1.4 1.0 0.9
a a a a a
0.6 0.6 0.6 1.2 0.0 0.11 ns
0.9 0.5 0.5 0.8 0.0
a a a a a
1.7 0.0 0.8 0.8 0.0
Different letters within columns and year indicate significantly different means (square-root transformed data) (Tukey’s test, p < 0.05). a Dose of product/100 l. b Pearson correlation coefficient between number of capsids and damage.
Garlic extract has previously been shown to cause mortality in insect pests. Prowse et al. (2006) found that garlic application increased the mortality of eggs, larvae and adults of two dipteran species (Delia radicum (L.) and Musca domestica L.). Even if garlic extract reduced number of L. pabulinus and O. marginalis in one trial each, we did not find any effect of garlic extract on damage. Similar results were obtained by Singh (2006). He compared garlic extract
to several other plant products against the rice gundhi bug Leptocorisa sp. (Alydidae: Hemiptera), and found no effect of garlic extract. Copping (2004) writes that garlic extract is mainly a repellent and should be applied to the host plant before insects settle. Mirid nymphs hatch from eggs laid in the host plant the previous autumn. They have limited opportunities to change host plant before they become adults. Autumn application shortly
Table 4 Mean % apples (untransformed data) per plot damaged by mirids in different treatments in the integrated and the organic orchards 2004–2006. Field
Year
Treatment
Product/100 l
% Damage
Integrated n¼5
Variable
df
F
p
2004
Control Fenthion Phosalon Diflubenzuron Azadirachtin 2
– 10 ml 100 ml 30 ml 500 ml 2
23.0 2.8 19.8 18.4 0.8
a b a a b
Treatment Block
4,16 4,16
16.82 1.30
<0.0001 0.31
n¼5
2005
Control Fenthion Phosalon Diflubenzuron Azadirachtin 2
– 10 ml 125 ml 30 ml 500 ml 2
16.8 7.4 8.6 5.2 2.4
a ab ab b b
Treatment Block
4,16 4,16
8.14 1.48
0.0009 0.25
Organic n¼5
2004
Control Azadirachtin Azadirachtin 2 Soybean oil
– 500 ml 500 ml 2 4000 ml
33.2 3.6 3.8 35.2
a b b a
Treatment Block
3,11 4,11
18.32 1.64
0.0001 0.23
n¼4
2005
Control Azadirachtin Azadirachtin 2 Azadirachtin 2 Garlic extract Rapeseed oil
– 500 ml 500 ml 2 300 ml 2 2000 ml 3000 ml
10.3 0.3 0 0.8 5.8 8.8
a a a a a a
Treatment Block
5,15 3,15
1.94 0.46
0.15 0.71
n¼4
2006
Control Azadirachtin Azadirachtin 2 Garlic extracta Garlic extractb Kaolin 2
– 250 ml 250 ml 2 2000 ml 2000 ml 3000 mg
11.0 1.8 0 7.0 8.3 1.8
a a a a a a
Treatment Block
5,15 3,15
1.50 1.44
0.25 0.27
Data analysis on arcsin-transformed percentages, means with different letters within years are significantly different (p < 0.05, Tukey’s test). a Developmental stage BBCH 57 according to Meier et al. (1994). b Developmental stage BBCH 65 according to Meier et al. (1994).
G. Jaastad et al. / Crop Protection 28 (2009) 309–313
before egglaying starts, might be better timing for garlic extract to achieve a repellent effect against mirids on apple. Knight et al. (2001) investigated the effect of kaolin on several apple pests. They found some effect on the mullein bug (Campylomma verbasci) (Meyer-Du¨r). However, in a one year study by Beers and Himmel (2002) no effect of kaolin on number or damage by C. verbasci was found. Lalancette et al. (2005) evaluated kaolin on both arthropods and diseases on peach. Based on damage at harvest, they concluded that kaolin had little effect on the tarnished plant bug (Lygus lineolaris (Palisot de Beuvois)). Results from our study confirm these results, as a small but variable effect of kaolin was found. However, kaolin was only tested in one trial. Baumler and Potter (2007) compared azadirachtin, kaolin, garlic extract and some other biopesticides to several synthetic pesticides against the Japanese beetle (Popillia japonica Newman). They also concluded that azadirachtin was the only biopesticide that had any effect against this pest. Even though the mean differences in damage between treatments were large, for instance in 2005 and 2006 in the organic field, no statistically significant differences were found. A clumped distribution of mirids, leading to a large variation in mirid numbers among plots receiving the same treatment, might explain this. A significant block effect on the number of L. pabulinus in 2004 (df ¼ 4,11, F ¼ 6.65, p ¼ 0.006) and on O. marginalis in 2005 (df ¼ 3,15, F ¼ 3.66, p ¼ 0.04), shows that the distribution of mirids was clumped. The variation in numbers of each species between fields and years also shows that the spatial distributions were highly variable. No bioassay or controlled experiment was performed to investigate the ability of different species to cause damage to apples in this study. Field trials with mirids in isolation bags to investigate the damage potential on selected host plants have been done by others (Sørum, 1977b; Taksdal, 1983). However, as mirids are forced to feed on the given food in such trials, we would argue that a correlation analysis between numbers present and damage might give just as good indication of whether a given species tend to damage the fruit. In our study, the numbers of L. pabulinus, L. rugicollis, O. marginalis, P. ambiguus, P. arbustorum and A. mali correlated positively with the apple damage. As expected, the nonphytophageous species A. nemorum and P. longipennis did not correlate with damage. Field trials with mirids are difficult as their distribution may be clumped and the variation in numbers between years is large. However, these trials are still needed to evaluate the effect of different control methods. Thus, in conclusion, the botanical pesticide azadirachtin is a promising control method against mirid pests of apples, whereas garlic extract, vegetable oils and kaolin will probably not control these pests. Acknowledgements We thank Marius Egge and Sjur K. Jaastad for allowing these experiments to be conducted in their orchard and Jostein Ulgenes, Andrew Leese and Sjur K. Jaastad for valuable assistance during field work. This work was financially supported by the Norwegian Research Council. References Alford, D.V., 2007. Pests of Fruit Crops. Academic Press, Burlington, MA, USA. Baumler, R.E., Potter, D.A., 2007. Knockdown, residual, and antifeedant activity of pyrethroids and home landscape bioinsecticides against Japanese beetles (Coleoptera: Scarabidae) on Linden foliage. J. Econ. Entomol. 100, 451–458. Beers, E.H., Himmel, P.D., 2002. Control of Campylomma verbasci with registrated and unregistrated pesticides. In: Proceedings of the 76th Annual Western Orchard Pest and Disease Management Conference. Portland, OR, USA. Bu¨rgel, K., Daniel, C., Wyss, E., 2005. Effects of autumn kaolin treatments on the rosy apple aphid, Dysaphis plantaginea (Pass.) and possible modes of action. J. Appl. Entomol. 129, 311–314.
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Chapman, P.C., 1967. Petroleum oils for the control of orchard pests. N.Y. State Agricultural Experimental Station Bulletin 814, 1–22. Chapman, P.C., Pearce, G.W., 1949. Susceptibility of winter eggs of the European red mite to petroleum oils and dinitro compounds. J. Econ. Entomol. 42, 44–47. Chapman, P.C., Pearce, G.W., Avens, A.W., 1941. The use of petroleum oils as insecticides, part III oil deposit and the control of fruit tree rollers and other apple pests. J. Econ. Entomol. 34, 639–647. Copping, L.G., 2004. The Manual of Biocontrol Agents, third ed. BCPC, Hampshire, England. Cottrell, T.E., Wood, B.W., Reilly, C.C., 2002. Particle film affects black pecan aphid (Homoptera: Aphididae) on pecan. J. Econ. Entomol. 95, 782–788. Cranshaw, W.S., Baxendale, B., 2005. Insect Control: Horticultural Oils. Available from: (www document). Dorn, A., Rademacher, J.M., Sehn, E., 1986. Effect of azadirachtin on the moulting cycle, endocrine system, and ovaries in last-instar larvae of the milkweed bug, Oncopeltus fasciatus. J. Insect Physiol. 32, 231–238. Edland, T., 2004. Sugande skade- og nyttedyr i frukthagar (in Norwegian). Grønn kunnskap 8 (4), 175. Glenn, D.M., Puterka, G.J., Vanderzwet, T., Byers, R.E., Feldhake, C., 1999. Hydrophobic particle films: a new paradigm for suppression of arthropod pests and plant diseases. J. Econ. Entomol. 92, 759–771. Isman, M.B., 2006. Botanical insecticides, deterrents, and repellents in modern agriculture and an increasingly regulated world. Annu. Rev. Entomol. 51, 45–66. Jaastad, G., 2007. Late dormant rapeseed oil treatment against black cherry aphid and cherry fruit moth in sweet cherries. J. Appl. Entomol. 131, 284–288. Jonsson, N., 1985. Ecological segregation of sympatric heteropterans on apple trees. Fauna Norv. Ser. B 32, 7–11. Jonsson, N., 1987. Nymphal development and food consumption of Atractotomus mali (Meyer-Du¨r) (Hemiptera: Miridae), reared on Aphis pomi (DeGeer) and Psylla mali Schmidberger. Fauna Norv. Ser. B 34, 22–28. Knight, A.L., Christianson, B.A., Unruh, T.R., 2001. Impact of seasonal kaolin particle films on apple pest management. Can. Entomol. 133, 413–428. Lalancette, N., Belding, R.D., Shearer, P.W., Frecon, J.L., Tietjen, W.H., 2005. Evaluation of hydrophobic and hydrophilic kaolin particle films for peach crop, arthropod and disease management. Pest Manag. Sci. 61, 25–39. Marko´, V., Blommers, L.H.M., Bogya, S., Helsen, H., 2008. Kaolin particle films suppress many apple pests, disrupt natural enemies and promote wooly apple aphid. J. Appl. Entomol. 132, 26–35. Mazor, M., Erez, A., 2004. Processed kaolin protects fruits from Mediterranean fruit fly infestations. Crop Prot. 23, 47–51. Meier, V.U., Graf, H., Hack, H., Hess, M., Kennel, W., Klose, R., Mappes, D., Seipp, D., Stauss, R., Sterif, J., Van den Boom, T., 1994. Pha¨nologische Entwicklungsstadien des Kernobstes (Malus domestica Borkh. and Pyrus communis L.), des Steinobstes (Prunus-Arten), der Johannisbeere (Ribes-Arten) und der Erdbeere (Fragaria x ananassa Duch.). Nachrichtenbl. Deut. Pflanzenschutzd. 46, 141–153 (in German). Palm, G., Hauschildt, H., 2003. Beka¨mpfung der Problemscha¨dlinge Fruchtscha¨digende Wanzen und Apfelschalenwickler. Mitt. OVR 58, 113–122 (in German). Pless, C.D., Deyton, D.E., Sams, C.E., 1995. Control of San Jose scale, Terrapin scale and European red mite on dormant fruit trees with soybean oil. HortScience 30, 94–97. Prowse, G.M., Galloway, T.S., Foggo, A., 2006. Insecticidal activity of garlic juice in two dipteran pests. Agric. For. Entomol. 8, 1–6. Puterka, G.J., Glenn, D.M., Pluta, R.C., 2005. Action of particle films on the biology and behavior of pear psylla (Homoptera: Psyllidae). J. Econ. Entomol. 98, 2079–2088. Rein, A., 1996. Damage on Apples Before Storage. Agro Inform as, N-3810 Gvarv, Norway. 27pp. Røen, D., Nornes, L., Jaastad, G., 2003. Årsaker til fråsortering i økologisk dyrka frukt. Norsk. Frukt og Bær 6, 28–30 (in Norwegian). SAS Institute, 1990. SAS/STAT User’s Guide, Version 6, fourth ed. SAS Institute Inc., Cary, NC, USA. SAS Institute, 2003. Version 9.1. SAS Institute Inc., Cary, NC, USA. Schmutterer, H., 1990. Properties and potentials of natural pesticides from the neem tree, Azadirachta indica. Annu. Rev. Entomol. 35, 271–297. Schøyen, T.H., Jørstad, I., 1956. Skadedyr og sykdommer i frukt- og bærhagen. H. Aschehoug & Co., Oslo, Norway (in Norwegian). Singh, P.K., 2006. Efficiency of some species and plant products on incidence of rice gundhi bug, Leptocorisa spp. (Alydidae: Hemiptera). J. Plant Prot. Environ. 3, 32–35. Smith, E.H., Pearce, G.W., 1948. The mode of action of petroleum oils as ovicides. J. Econ. Entomol. 41, 173–180. Sutherland, W.J., 1996. Ecological Census Techniques: A Handbook. Cambridge University Press, Cambridge, United Kingdom. Sørum, O., 1977a. Bugs (Heteroptera) as predators in apple and pear orchards. Gartneryrket 67, 726–728 (in Norwegian). Sørum, O., 1977b. Noxious bugs in Norwegian apple and pear orchards. Gartneryrket 67, 436–444 (in Norwegian). Taksdal, G., 1983. Orthotylus marginalis Reuter and Psallus ambiguus (Falle´n) (Heteroptera, Miridae) causing stony pits in pears. Acta Agric. Scand. 33, 205–208. Tedeschi, R., Alma, A., Tavella, L., 2001. Side-effects of three neem (Azadirachta indica A. Juss) products on the predator Macrolophus caliginosus Wagner (Het., Miridae). J. Appl. Entomol. 125, 397–402. Wheeler, A.G., 2001. Biology of the Plant Bugs. Cornell University Press, New York, USA. Zar, J.H., 1984. Biostatistical Analysis. Prentice-Hall International, Inc., NJ, USA.
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Effect of botanically derived pesticides on mirid pests and beneficials in apple Gunnhild Jaastad a, *, Nina Trandem b, Berit Hovland a, Sigrid Mogan c a
Norwegian Institute for Agricultural and Environmental Research – Bioforsk Horticulture and Greening Division, Ullensvang, 5781 Lofthus, Norway Norwegian Institute for Agricultural and Environmental Research – Bioforsk Plant Health and Plant Protection Division, Høgskoleveien 7, 1432 Ås, Norway c The Norwegian Agricultural Extension Service, Foss gård, Stokkeveien 4, 3400 Lier, Norway b
a r t i c l e i n f o
a b s t r a c t
Article history: Received 28 February 2008 Received in revised form 11 November 2008 Accepted 12 November 2008
Mirid bugs (Hemiptera: Miridae) are important pests in apple and pear production in both Europe and the United States. Mirids feed on sap in shoot tips, flower buds and fruitlets, resulting in deformation and stony pits in the fruit. Due to withdrawal of pesticides and concern about the environment alternative control methods against capsids are needed. In this study the effect of neem extract (NeemAzal), garlic extract (Ecoguard), vegetable oil (soybean or rapeseed) and kaolin (Surround) were evaluated for their effect on populations and damage of mirids in apples. Results show that neem extract is a promising alternative, giving as good control of mirid damage as several synthetic pesticides. Kaolin, garlic extract and vegetable oil did not significantly reduce damage. Many omnivorous species were present in the experimental orchards, and a positive correlation between the numbers sampled and fruit damage indicated that several of them could be pests. Ó 2008 Elsevier Ltd. All rights reserved.
Keywords: Miridae Garlic extract Neem extract Vegetable oil Kaolin Apple
1. Introduction Mirid bugs (Hemiptera: Miridae) are important pests in apple and pear production in both Europe and the United States (Wheeler, 2001; Alford, 2007). In organic production the degree of fruit damage might exceed 40% (Røen et al., 2003). Mirid bugs feed on sap in shoot tips, flower buds and fruitlets, resulting in deformation and stony pits in the fruit (Wheeler, 2001). Mirids damaging fruit are usually both polyphagous and omnivorous, and it can be difficult to assess whether a species should be considered as pest or beneficial. Two species unanimously regarded as apple pests in Northern Europe are Lygocoris pabulinus (Linnaeus) and Lygocoris rugicollis (Falle´n) (Schøyen and Jørstad, 1956; Alford, 2007; Wheeler, 2001). Among species considered beneficial due to their predation of pest insects and mites are Phytocoris longipennis Flor and Blepharidopterus angulatus (Falle´n) (Sørum, 1977a; Edland, 2004; Wheeler, 2001). A third category is species which are mainly predacious, but occasionally cause damage because they are able to feed on plants, e.g. Orthotylus marginalis Reuter, Plagiognathus arbustorum (Fabricius), Psallus ambiguus (Falle´n) and Atractotomus mali (Meyer-Du¨r) (Taksdal, 1983; Jonsson, 1987; Wheeler, 2001; Edland, 2004).
* Corresponding author. Tel.: þ47 95902678. E-mail address: [email protected] (G. Jaastad). 0261-2194/$ – see front matter Ó 2008 Elsevier Ltd. All rights reserved. doi:10.1016/j.cropro.2008.11.006
Most mirids that cause fruit damage overwinter as eggs and hatch before blossom. The damage is mainly done by nymphs feeding on fruitlets (Jonsson, 1985; Weeler, 2001). Due to withdrawal of synthetic insecticides, concern about the environment, increased organic production and development of insecticide resistance, alternative control methods are needed (Isman, 2006). Several botanically derived pesticides give effective control of insect pests, but few have been systematically tested on heteropterans. Azadirachtin, neem extract, is a botanical pesticide with several modes of action. It has an antifeedant/repellent effect, it disrupts moulting by inhibiting ecdysone production, and it may disrupt normal mating behaviour (Schmutterer, 1990; Copping, 2004; Isman, 2006). Mineral or vegetable oil has been used in decades against dormant insect and mite pests (Chapman et al., 1941; Chapman and Pearce, 1949; Schøyen and Jørstad, 1956; Chapman, 1967). Oils work through a mechanical interference with the gaseous exchange in eggs (Smith and Pearce, 1948) and probably also by blocking spiracles in young and adult arthropods (Cranshaw and Baxendale, 2005). In addition, vegetable oil sprays are often emulsified by soft soaps containing oleic acid that destroy cell membranes (Copping, 2004). Garlic extract has been shown to both cause mortality and to repel insects (Copping, 2004; Prowse et al., 2006). Kaolin is not a botanical extract, but a natural clay mineral (aluminosilicate), creating a physical barrier to infestation by impeding movement, feeding and egglaying (Cottrell et al., 2002). Several fruit tree pests have shown to be suppressed by kaolin (Glenn et al., 1999; Mazor and Erez, 2004; Bu¨rgel et al., 2005; Puterka et al., 2005; Marko´ et al., 2008).
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G. Jaastad et al. / Crop Protection 28 (2009) 309–313
The main objective of this study was to evaluate the effect of azadirachtin (NeemAzal), vegetable oil, garlic extract (ECOguardÒ) and kaolin (SurroundÒ) on the mirid fauna in apple trees. 2. Materials and methods Experiments were conducted in two apple orchards, one integrated orchard in Ullensvang, Western Norway, and one organic orchard in Lier, South-Eastern Norway. The experiments were set up as randomized block designs with four or five replications. In each plot there were 3 trees of Aroma, and a minimum of 2 border trees between each plot. Pesticides were applied till run-off with a hand-held lance connected to a wheelbarrow or tractor boom sprayer (spray volume approximately 1000–2000 l/ha). Spray volume and dose applied per treatment and trial was measured, and g.a.i. per ha calculated. Treatments, dosages and application times per trial are given in Table 1. The integrated orchard trials were conducted in 2004 and 2005. The orchard (0.4 ha) was planted in 1994 with tree spacing 4.5 1.5 m. Azadirachtin (NeemAzal TS, active ingredient 10 g/l, Trifolio-M GmbH, Germany) was compared to an untreated control and three synthetic pesticides: fenthion (Lebaycid, a.i. 535 g/l, Bayer AG, Germany), phosalone (Zolone Flo, a.i. 500 g/l, Cheminova AS, Denmark) and diflubenzuron (Dimilin SC-48, a.i. 480 g/l, Crompton Europe B.V., Netherlands). The organic orchard trials were conducted in 2004, 2005 and 2006. Planting year was 1988, and tree spacing 4.5 1.5 m. The orchard was 0.5 ha in area. An untreated control was compared to several concentrations and applications of azadirachtin, vegetable oil (soybean oil, Mills, in 2004, and rapeseed oil, Askim, Norway, in 2005) mixed with soft soap (grønnsåpe, Lilleborg, Norway), garlic extract (ECOguardÒ, 99.9% active ingredient, ECOspray Ltd, Northfolk, England) and kaolin (SurroundÒCF, 95% active ingredient; Engelhard Corporations, Iselin, NJ). The mirid fauna was sampled by beating three random branches on every tree in each plot with a stiff rubber hose one week after
the last spray application. Each branch received three quick beats, and dislodged insects were collected by a beating tray (Sutherland, 1996). All insects were identified and counted, but only mirids and anthocorids are shown here. All mirids collected were 3rd to 5th instar nymphs while the majority of anthocorids were adults. Fruit damage was evaluated by randomly picking 100 apples from each plot. Fruit damage was classified according to Rein (1996). Data were analysed by analysis of variance (ANOVA) with treatment and block as explanatory variables (SAS Institute, 1990, 2003). Number of mirids was square-root transformed (O(x þ 0.5)) prior to analysis because standard deviations were proportional to the means (Zar, 1984). Proportion of damaged apples was arcsin transformed prior to analysis (Zar, 1984). For variables that explained a significant part of the variance, Tukey’s test was used to analyse differences between means (Zar, 1984). A Pearson correlation analysis between damage and the number of individuals of each species was performed to get an indication of which species were most harmful to apples. 3. Results Azadirachtin had an effect on both mirid numbers and damage (Tables 2–4). Compared to the untreated control, the numbers of L. pabulinus, O. marginalis, A. mali and P. ambiguus were significantly reduced by azadirachtin treatment in several trials (Tables 2 and 3). Furthermore, application of azadirachtin significantly reduced damage in both years of trials in the integrated field, and in the first year of trials in the organic field (Table 4). Also in the two following years, there was a tendency of less damage in the azadirachtin treated plots of the organic field, although this was not significant. In the trials including one and two applications, different concentrations, or different application times with azadirachtin, no significant differences in damage between these were found (Table 4). When azadirachtin was compared to synthetic pesticides, no statistical difference in either number of mirids or damage was
Table 1 Treatments, doses and application times in the five trials. Spray volume was 1000–2000 l/ha. Field
Year
Treatment (Ô)
Dose/100 l
g.a.i/ha 1st application
g.a.i/ha 2nd application
Application date
Application time BBCHa
Integrated
2004
Fenthion (Lebaycid) Phosalon (Zolone Flo) Diflubenzuron (Dimilin) Azadirachtin (NeemAzal) 2 Control Fenthion (Lebaycid) Phosalon (Zolone Flo) Diflubenzuron (Dimilin) Azadiracthin (NeemAzal) 2 Control
10 ml 100 ml 30 ml 500 ml – 10 ml 125 ml 30 ml 500 ml –
200 1850 640 170 – 130 2720 540 210
– – – 150 – – – – 120 –
1.06 1.06 22.05 22.05 þ 1.06 – 13.06 19.05 31.05 31.05 þ 13.06 –
67 67 65 65 þ 67 – 67 60 65 65 þ 67 –
Vegetable oil (Soybean oil)b Azadiracthin (NeemAzal) Azadiracthin (NeemAzal) 2 Control Vegetable oil (Rapeseed oil)b Azadiracthin (NeemAzal) Azadiracthin (NeemAzal) 2 Azadiracthin (NeemAzal) 2 Garlic extract (Ecoguard) Control Azadiracthin (NeemAzal) Azadiracthin (NeemAzal) 2 Garlic extract (Ecoguard) Garlic extract (Ecoguard) Kaolin (Surround) 2 Control
4000 ml 500 ml 500 ml – 3000 ml 500 ml 500 ml 300 ml 2000 ml – 250 ml 250 ml 2000 ml 2000 ml 3000 mg –
67 l oil 80 80 – 33 l oil 60 60 40 28,440 – 30 30 32,000 40,280 35,625 –
– – 80 – – – 50 40 – – – 40 – – 44,333 –
2.05 19.05 19.05 þ 27.05 – 19.05 27.05 27.05 þ 7.06 27.05 þ 7.06 15.06 – 3.06 3.06 þ 9.06 24.05 3.06 24.05 þ 3.06 –
54 65 65 þ 67 – 57 65 65 þ 67 65 þ 67 69 – 65 65 þ 67 57 65 57 þ 65 –
2005
Organic
2004
2005
2006
a Developmental stage according to Meier et al. (1994), BBCH 54 ¼ tight cluster, BBCH 57 ¼ white tip, BBCH 59 ¼ balloon, BBCH 61 ¼ first blossom, BBCH 65 ¼ full blossom, BBCH ¼ start petal fall, BBCH 69 ¼ petal fall. b Soft soap (ca 1000 ml/100 l) added as emulsifier.
G. Jaastad et al. / Crop Protection 28 (2009) 309–313
311
Table 2 Mean std number (untransformed data) of mirids and Anthocoris nemorum per plot recorded by beating tray samples in different treatments in the organic orchard in 2004–2006. Treatment
2004 (n ¼ 5) Controlb Azadirachtin Azadirachtin Soybean oil Correlationc 2005 (n ¼ 4) Control Azadirachtin Azadirachtin Azadirachtin Rapeseed oil Garlic extract Correlation 2006 (n ¼ 4) Control Azadirachtin Azadirachtin Garlic extractd Garlic extracte Kaolin Correlationc
Dosea
– 500 ml 500 ml 2 4000 ml
500 ml 500 ml 2 300 ml 2 3000 ml 2000 ml
250 ml 250 ml 2 2000 ml 2000 ml 3000 mg 2
Mean std number per plot Lygocoris pabulinus
Lygocoris rugicollis
Orthotylus marginalis
Plagiognathus arbustorum
Psallus ambiguus
Atractotomus mali
Anthocoris nemorum
Mean
std
Mean
std
Mean
Mean
Mean
std
Mean
Mean
4.8 1.0 0.8 3.8 0.14 ns
5.7 1.7 1.3 1.6
0.8 0.6 0.0 0.2 0.08 ns
1.5 1.3 0.0 0.4
0.3 0.2 0.0 0.8 0.26 ns
0.5 0.4 0.0 0.4
2.8 2.3 0.8 2.3 2.3 4.3 0.22 ns
2.2 3.9 1.0 1.0 1.7 4.7
a a a a a a
0.8 0.3 0.0 0.3 1.3 0.3 0.43 p ¼ 0.03
1.0 0.5 0.0 0.5 0.5 0.5
9.0 2.8 4.0 3.5 3.3 3.5 0.27 ns
6.4 1.5 2.2 1.9 2.1 3.7
a a a a a a
16.3 2.5 1.3 2.8 6.5 6.0 0.27 ns
4.9 2.4 1.0 1.9 4.2 6.7
a a a a
16.3 5.9 1.5 0.6 0.5 0.6 1.0 0.8 7.5 6.5 5.0 2.4 0.54 p ¼ 0.006
a bc c c ab bc
2.0 1.8 0.0 0.0 0.8 1.0 0.8 1.0 2.0 0.8 1.3 1.5 0.77 p < 0.0001
4.5 1.5 0.5 4.8 13.8 8.8 0.46 p ¼ 0.02
ab b b ab a ab
0 0 0 0 0 0 –
3.9 2.4 1.0 5.6 8.2 5.6
a a a a
a a a a a a
std
7.0 1.2 1.4 8.0 0.51 p ¼ 0.03
4.5 1.6 0.5 6.3
3.3 0.0 0.0 0.0 0.8 3.8 0.16 ns
3.3 0.0 0.0 0.0 1.5 4.3
14.3 1.0 0.0 0.5 0.5 1.0 0.39 ns
10.4 2.0 0.0 1.0 1.0 2.0
a b b a
std
0.3 0.6 0.4 0.6 0.19 ns
0.5 0.9 0.9 1.3
a a a a a a
0.5 0.0 0.0 0.0 1.3 0.3 0.14 ns
1.0 0.0 0.0 0.0 2.5 0.5
a b b b b b
0 0 0 0 0 0 –
a a a a
a a a a a a
ab ab a b
std 0 0 0 0
std
2.2 1.0 1.4 1.2 0.10 ns
2.0 1.0 1.1 1.1
a a a a
ab ab b ab a ab
0.0 0.0 0.3 0.0 0.3 0.0 0.21 ns
0.0 0.0 0.5 0.0 0.5 0.0
a a a a a a
a b b b b b
1.5 0.8 1.0 0.3 0.5 0.8 0.37 ns
3.0 1.0 2.0 0.5 0.6 1.5
a a a a a a
–
Different letters within columns and year indicate significantly different means (square-root transformed data) (Tukey’s test, p < 0.05). a Dose of product/100 l. b n ¼ 4. c Pearson correlation coefficient between number of capsids and damage. d Application time BBCH 57 (Meier et al., 1994). e Application time BBCH 65 (Meier et al., 1994).
found between azadirachtin treated trees and trees treated with fenthion (Tables 3 and 4). However, azadirachtin was more effective than phosalon and diflubenzuron in 2004 (Table 4). In 2005, only azadirachtin and diflubenzuron treated plots had significantly fewer damaged apples than control plots. No mirid species was significantly suppressed by vegetable oil (Table 2) and neither treatment with soybean oil nor rapeseed oil had any effect on damage (Table 4). Neither an early nor a late application of garlic extract significantly reduced fruit damage compared to the untreated control (Table 4). Garlic extract did, however, significantly reduce the number of L. pabulinus in 2005 and the number of O. marginalis and A. mali in 2006 (Table 2). Kaolin treatment significantly reduced the number of O. marginalis and A. mali, however no effect on damage was found. In the correlation analysis between number of individuals and damage in every plot (regardless of treatment) a significant positive relationship was found for the following species (Tables 2 and 3): L. pabulinus (in three of the five trials in total); L. rugicollis, O. marginalis and P. ambiguus (in two trials); P. arbustorum and A. mali (in one trial). In contrast, numbers of the well-known predators Anthocoris nemorum (Linnaeus) and P. longipennis were not correlated with damage in any of the trials (Tables 2 and 3). 4. Discussion Of the botanical pesticides we tested, azadirachtin was clearly the most efficient. The effect was also similar or better compared to the synthetic pesticides included in the experiments. Similar results have been obtained by others. Palm and Hauschildt (2003)
compared azadirachtin to several synthetic pesticides over 4 years, and the results showed an efficiency of 4–90% regarding mirid damage to apples. However, mirid species and number of replicates were not given in their report. Furthermore, Dorn et al. (1986) demonstrated that azadirachtin prevented moulting and increased the percentage of nymphs that died without moulting in the milkweed bug (Oncopeltus fasciatus (Dallas)). Tedeschi et al. (2001) found that neem formulations increased mortality in the predatory mirid Macrolophus caliginosus Wagner. In our study azadirachtin did not significantly affect the most important predatory hemipterans, A. nemorum and P. longipennis, while the omnivorius P. ambiguus and A. mali, mainly regarded as beneficials, were negatively affected by azadirachtin treatment. However, our findings indicate that both P. ambiguus and A. mali are causing damage to apples as the number of both species was positively correlated to damage. This is supported by Taksdal (1983), who showed that P. ambiguus can cause stony pits in pears. Based on our results, one treatment with azadirachtin at a concentration of 250–300 ml/100 l gives the same control as higher doses and two treatments. The lack of effect by vegetable oil treatment might be due to only the operculum of capsid eggs being visible on the plant, i.e. little of the total egg surface being exposed. Oil treatment is effective against over wintering eggs of other pest species such as aphids and spider mites (Pless et al., 1995; Jaastad, 2007). However, these eggs are fully exposed on the plant surface. Rapeseed oil was applied later in the season than soybean oil, however no clear differences between these two application times were found. Different timings of vegetable oil treatment were, however, not compared within trials.
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G. Jaastad et al. / Crop Protection 28 (2009) 309–313
Table 3 Mean std number (untransformed data) of mirids and Anthocoris nemorum per plot recorded by beating tray samples in different treatments in the integrated orchard in 2004–2005. Treatment
Dosea
Mean std number per plot (n ¼ 5) Lygocoris pabulinus
Lygocoris rugicollis
Mean
std
–
3.2
1.3
Fenthion
10 ml
0.0
Phosalone Diflubenzuron Azadirachtin Correlationb
100 ml 30 ml 500 ml 2
0.6 1.6 0.0 0.55 p ¼ 0.005
2004 Control
2005 Control Fenthion Phosalone Diflubenzuron Azadirachtin Correlationb
– 10 ml 125 ml 30 ml 500 ml 2
0.6 0.0 0.4 0.4 0.2 0.02 ns
Orthotylus marginalis
Plagiognathus arbustorum
Psallus ambiguus
Phytocoris longipennis
Anthocoris nemorum
Mean
std
Mean
std
Mean
std
Mean
std
Mean
std
11.9
ab
3.8
1.6
a
1.1
b
3.2
2.0
a
Mean
std
a
0.8
1.3
a
2.2
1.9
ab
3.4
2.4
a
3.6
1.9
a
12.6
0.0
b
0.2
0.4
a
0.2
0.4
b
0.4
0.5
a
0.6
0.5
a
1.2
0.9 1.8 0.0
b ab b
0.2 0.0 0.0 0.08 ns
0.4 0.0 0.0
a a a
3.4 2.3 1.4 1.5 0.2 0.4 0.56 p ¼ 0.004
a ab b
4.0 4.2 1.8 1.8 1.2 1.6 0.45 p ¼ 0.02
a a a
1.2 1.6 5.0 4.5 1.2 1.3 0.50 p ¼ 0.01
a a a
7.6 21.2 7.6 0.26 ns
8.4 10.6 5.1
ab a ab
4.6 3.4 2.8 0.15 ns
3.2 3.2 0.8
a a a
0.5 0.0 0.5 0.5 0.4
a a a a a
0 0 0 0 0 –
1.0 0.0 0.8 0.8 0.0 0.36 ns
a a a a a
0 0 0 0 0 –
5.8 3.8 1.6 1.3 3.2 2.6 3.4 1.9 0.0 0.0 0.53 p ¼ 0.006
a ab ab a b
1.6 0.4 1.4 1.0 0.4 0.30 ns
2.3 0.5 1.4 1.0 0.9
a a a a a
0.6 0.6 0.6 1.2 0.0 0.11 ns
0.9 0.5 0.5 0.8 0.0
a a a a a
1.7 0.0 0.8 0.8 0.0
Different letters within columns and year indicate significantly different means (square-root transformed data) (Tukey’s test, p < 0.05). a Dose of product/100 l. b Pearson correlation coefficient between number of capsids and damage.
Garlic extract has previously been shown to cause mortality in insect pests. Prowse et al. (2006) found that garlic application increased the mortality of eggs, larvae and adults of two dipteran species (Delia radicum (L.) and Musca domestica L.). Even if garlic extract reduced number of L. pabulinus and O. marginalis in one trial each, we did not find any effect of garlic extract on damage. Similar results were obtained by Singh (2006). He compared garlic extract
to several other plant products against the rice gundhi bug Leptocorisa sp. (Alydidae: Hemiptera), and found no effect of garlic extract. Copping (2004) writes that garlic extract is mainly a repellent and should be applied to the host plant before insects settle. Mirid nymphs hatch from eggs laid in the host plant the previous autumn. They have limited opportunities to change host plant before they become adults. Autumn application shortly
Table 4 Mean % apples (untransformed data) per plot damaged by mirids in different treatments in the integrated and the organic orchards 2004–2006. Field
Year
Treatment
Product/100 l
% Damage
Integrated n¼5
Variable
df
F
p
2004
Control Fenthion Phosalon Diflubenzuron Azadirachtin 2
– 10 ml 100 ml 30 ml 500 ml 2
23.0 2.8 19.8 18.4 0.8
a b a a b
Treatment Block
4,16 4,16
16.82 1.30
<0.0001 0.31
n¼5
2005
Control Fenthion Phosalon Diflubenzuron Azadirachtin 2
– 10 ml 125 ml 30 ml 500 ml 2
16.8 7.4 8.6 5.2 2.4
a ab ab b b
Treatment Block
4,16 4,16
8.14 1.48
0.0009 0.25
Organic n¼5
2004
Control Azadirachtin Azadirachtin 2 Soybean oil
– 500 ml 500 ml 2 4000 ml
33.2 3.6 3.8 35.2
a b b a
Treatment Block
3,11 4,11
18.32 1.64
0.0001 0.23
n¼4
2005
Control Azadirachtin Azadirachtin 2 Azadirachtin 2 Garlic extract Rapeseed oil
– 500 ml 500 ml 2 300 ml 2 2000 ml 3000 ml
10.3 0.3 0 0.8 5.8 8.8
a a a a a a
Treatment Block
5,15 3,15
1.94 0.46
0.15 0.71
n¼4
2006
Control Azadirachtin Azadirachtin 2 Garlic extracta Garlic extractb Kaolin 2
– 250 ml 250 ml 2 2000 ml 2000 ml 3000 mg
11.0 1.8 0 7.0 8.3 1.8
a a a a a a
Treatment Block
5,15 3,15
1.50 1.44
0.25 0.27
Data analysis on arcsin-transformed percentages, means with different letters within years are significantly different (p < 0.05, Tukey’s test). a Developmental stage BBCH 57 according to Meier et al. (1994). b Developmental stage BBCH 65 according to Meier et al. (1994).
G. Jaastad et al. / Crop Protection 28 (2009) 309–313
before egglaying starts, might be better timing for garlic extract to achieve a repellent effect against mirids on apple. Knight et al. (2001) investigated the effect of kaolin on several apple pests. They found some effect on the mullein bug (Campylomma verbasci) (Meyer-Du¨r). However, in a one year study by Beers and Himmel (2002) no effect of kaolin on number or damage by C. verbasci was found. Lalancette et al. (2005) evaluated kaolin on both arthropods and diseases on peach. Based on damage at harvest, they concluded that kaolin had little effect on the tarnished plant bug (Lygus lineolaris (Palisot de Beuvois)). Results from our study confirm these results, as a small but variable effect of kaolin was found. However, kaolin was only tested in one trial. Baumler and Potter (2007) compared azadirachtin, kaolin, garlic extract and some other biopesticides to several synthetic pesticides against the Japanese beetle (Popillia japonica Newman). They also concluded that azadirachtin was the only biopesticide that had any effect against this pest. Even though the mean differences in damage between treatments were large, for instance in 2005 and 2006 in the organic field, no statistically significant differences were found. A clumped distribution of mirids, leading to a large variation in mirid numbers among plots receiving the same treatment, might explain this. A significant block effect on the number of L. pabulinus in 2004 (df ¼ 4,11, F ¼ 6.65, p ¼ 0.006) and on O. marginalis in 2005 (df ¼ 3,15, F ¼ 3.66, p ¼ 0.04), shows that the distribution of mirids was clumped. The variation in numbers of each species between fields and years also shows that the spatial distributions were highly variable. No bioassay or controlled experiment was performed to investigate the ability of different species to cause damage to apples in this study. Field trials with mirids in isolation bags to investigate the damage potential on selected host plants have been done by others (Sørum, 1977b; Taksdal, 1983). However, as mirids are forced to feed on the given food in such trials, we would argue that a correlation analysis between numbers present and damage might give just as good indication of whether a given species tend to damage the fruit. In our study, the numbers of L. pabulinus, L. rugicollis, O. marginalis, P. ambiguus, P. arbustorum and A. mali correlated positively with the apple damage. As expected, the nonphytophageous species A. nemorum and P. longipennis did not correlate with damage. Field trials with mirids are difficult as their distribution may be clumped and the variation in numbers between years is large. However, these trials are still needed to evaluate the effect of different control methods. Thus, in conclusion, the botanical pesticide azadirachtin is a promising control method against mirid pests of apples, whereas garlic extract, vegetable oils and kaolin will probably not control these pests. Acknowledgements We thank Marius Egge and Sjur K. Jaastad for allowing these experiments to be conducted in their orchard and Jostein Ulgenes, Andrew Leese and Sjur K. Jaastad for valuable assistance during field work. This work was financially supported by the Norwegian Research Council. References Alford, D.V., 2007. Pests of Fruit Crops. Academic Press, Burlington, MA, USA. Baumler, R.E., Potter, D.A., 2007. Knockdown, residual, and antifeedant activity of pyrethroids and home landscape bioinsecticides against Japanese beetles (Coleoptera: Scarabidae) on Linden foliage. J. Econ. Entomol. 100, 451–458. Beers, E.H., Himmel, P.D., 2002. Control of Campylomma verbasci with registrated and unregistrated pesticides. In: Proceedings of the 76th Annual Western Orchard Pest and Disease Management Conference. Portland, OR, USA. Bu¨rgel, K., Daniel, C., Wyss, E., 2005. Effects of autumn kaolin treatments on the rosy apple aphid, Dysaphis plantaginea (Pass.) and possible modes of action. J. Appl. Entomol. 129, 311–314.
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Chapman, P.C., 1967. Petroleum oils for the control of orchard pests. N.Y. State Agricultural Experimental Station Bulletin 814, 1–22. Chapman, P.C., Pearce, G.W., 1949. Susceptibility of winter eggs of the European red mite to petroleum oils and dinitro compounds. J. Econ. Entomol. 42, 44–47. Chapman, P.C., Pearce, G.W., Avens, A.W., 1941. The use of petroleum oils as insecticides, part III oil deposit and the control of fruit tree rollers and other apple pests. J. Econ. Entomol. 34, 639–647. Copping, L.G., 2004. The Manual of Biocontrol Agents, third ed. BCPC, Hampshire, England. Cottrell, T.E., Wood, B.W., Reilly, C.C., 2002. Particle film affects black pecan aphid (Homoptera: Aphididae) on pecan. J. Econ. Entomol. 95, 782–788. Cranshaw, W.S., Baxendale, B., 2005. Insect Control: Horticultural Oils. Available from: