Integrated pest management approach for a new pest, Lacanobia ...

PS912.921/2003 Pest Management Science

Integrated pest management approach for a new pest, Lacanobia subjuncta (Lepidoptera: Noctuidae), in Washington apple orchards Michael D Doerr,∗ Jay F Brunner and Lawrence E Schrader Department of Entomology, Washington State University, Tree Fruit Research and Extension Center, Wenatchee, WA 98801, USA

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

PR

O

O

FS

Abstract: Bioassays of Lacanobia subjuncta (Grote and Robinson) larvae established baseline LC50 values and identified the potential of reduced-risk, organophosphate replacement and naturally derived insecticides (eg chloronicotinyls, spinosyns, oxadiazines, insect growth regulators, microbial insecticides and particle films) to control this pest. The toxicities of these products were compared with those of organophosphate, carbamate, chlorinated cyclodiene and synthetic pyrethroid insecticides used in the management of lepidopteran pests in Washington apple orchards. Field trials were conducted comparing candidate insecticides to conventional alternatives. Several new insecticides (eg spinosad, methoxyfenozide, indoxacarb and an aluminosilicate particle film) proved to be effective for the management of L subjuncta. We summarize the goals and challenges of developing an integrated pest management program for new and resurgent pests as insecticide tools continue to change, and propose a hypothesis for the sudden increase in pest status of L subjuncta based on organophosphate tolerances. The role of novel insecticides with unique modes of action in resistance management and the encouragement of biological control are also discussed.  2004 Society of Chemical Industry

TE

Prior to 1996, Lacanobia subjuncta (Grote and Robinson) (Lepidoptera: Noctuidae) was not recognized as a pest in Washington orchards.7,8 Since then, L subjuncta larvae have become troublesome in apple orchards of central Washington and northeast Oregon.9 Lacanobia subjuncta caused more crop loss in apple orchards in the Columbia basin region of Washington State and northeast Oregon than any other pest in the late 1990s.10 The first line of defense against a new pest usually involves the development of insecticide controls. Initial field trials with registered insecticides showed that chlorpyrifos (organophosphate), methomyl (carbamate) and endosulfan (chlorinated cyclodiene) had the most promise for suppressing L subjuncta.10 However, Smith et al 11 categorized many OP and carbamate insecticides as being highly toxic to several biological control agents important to apple pest management in Washington. Furthermore, these authors categorized novel (eg growth regulators, spinosyn and the chloronicotinyl imidacloprid) and biorational insecticides (eg horticultural mineral oil, fatty acid soaps, azadirachtin and Bacillus thuringiensis) as having low

N

C

O R

R

EC

1 INTRODUCTION To implement the Food Quality Protection Act (FQPA) of 1996, the Environmental Protection Agency (EPA) has prioritized registration of ‘reducedrisk’ insecticides specifically as organophosphate (OP) replacements.1 These new insecticides generally have a reduced spectrum of activity, and thus their fit into specific pest-management programs with changing pest complexes requires a continued evaluation effort. Washington apple growers have been instrumental in adopting new pest management techniques (ie mating disruption for codling moth, Cydia pomonella (L) (Lepidoptera: Tortricidae) that demonstrate a reduced reliance on OP insecticides.2 – 5 A consistent pattern associated with a move away from OP insecticides is a resurgence in secondary pests, especially leafrollers, Pandemis pyrusana Kearfott and Choristoneura rosaceana (Harris) (Lepidopteran: Tortricidae).2,4,6 The emergence of leafrollers as more important pests emphasizes the vulnerability of biointensive pest-management programs to changes in the status of a known pest or emergence of a new pest.

D

Keywords: Lacanobia subjuncta; insecticide; bioassay; toxicity; spinosad; methoxyfenozide; indoxacarb; Surround WP

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Pest Manag Sci 60:000–000 (online: 2004) DOI: 10.1002/ps.912

∗

Correspondence to: Michael D Doerr, Department of Entomology, Washington State University, Tree Fruit Research and Extension Center, 1100 N Western Avenue, Wenatchee, WA 98801, USA E-mail: [email protected] Contract/grant sponsor: Washington Tree Fruit Research Commission (Received 23 June 2003; revised version received 3 February 2004; accepted 6 April 2004)

 2004 Society of Chemical Industry. Pest Manag Sci 1526–498X/2004/$30.00

1

MD Doerr, JF Brunner, LE Schrader

R

O R

C

N

2

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

D

PR

O

O

FS

2.2 Susceptibility of field populations to azinphos-methyl The susceptibility of five field-collected populations to azinphos-methyl was assessed in 2000. Lacanobia subjuncta larvae were collected from orchards actively managed with insecticides but which contained significant populations, making it easy to collect large numbers of larvae. It was assumed that these populations had been exposed to insecticides for many years and were likely to have developed some tolerance or resistance to OP insecticides. Larvae were reared in the laboratory and bioassays were conducted on neonates of the F1 generation using the methods described in Section 2.1. 2.3 Reversion of susceptibility to azinphos-methyl over time The Chelan colony, collected in 2000, was maintained in the laboratory through eight generations (2000–2001). Changes in susceptibility of this colony in the absence of insecticide exposure were monitored in the fifth and eighth generation using the leaf disk bioassay methods described in Section 2.1.

EC

2 EXPERIMENTAL METHODS 2.1 Laboratory bioassays Tolerance levels of L subjuncta larvae were determined for 11 newly registered insecticides, or those expected to be registered soon, and 13 insecticides commonly used in apple in Washington (Table 1). The insecticides were selected for evaluation based on their potential to control lepidopteran pests. Lacanobia subjuncta larvae used in bioassays were originally collected from an apple orchard near Quincy, Washington, in 1999. Larvae were reared in the laboratory on a combination of artificial cutworm diet (Bio-Serv, #F9170, Frenchtown, New Jersey) and untreated apple (Malus domestica Borkhausen, ‘Delicious’) leaves following the methods described by Doerr et al.12 Bioassays were run on the F1 generation of the Quincy colony. In 2000, a second laboratory colony was established from larvae collected in an apple orchard near Chelan, Washington. Bioassays were conducted against the F1 and F3 generations during that year. The Chelan colony, hereafter referred to as ‘Lab Colony’, was maintained through 2002. Bioassays were conducted on neonate larvae unless otherwise denoted. A leaf disk bioassay was used to assess the toxicities of different insecticides to L subjuncta larvae. Treatments were prepared by diluting formulated insecticide in water (0.5 litre). Serial dilutions were made, with four to eight concentrations per insecticide. Latron B-1959 (2 µl; Dow AgroSciences, Indianapolis, Indiana), a wetting agent, was added to each insecticide treatment. A control of water plus the wetting agent was run with each bioassay. Untreated ‘Delicious’ apple leaves were collected from the WSU Tree Fruit Research and Extension Center, Wenatchee, Washington. Leaves were dipped in an insecticide solution three times to insure adequate wetting and then allowed to air dry. A leaf disk (2.3 cm diameter) was taken from each treated leaf, and four

leaf disks of the same treatment (concentration) were placed in a small covered Petri dish (Falcon 1006, 50 × 9 mm, Becton-Dickinson Labware, Franklin Lakes, New Jersey) and coded with a treatment ID. Petri dishes were randomly selected, and five 1- to 2-day-old L subjuncta larvae were placed directly on the leaf disks. Five to ten dishes (25–50 larvae) were prepared at each concentration depending on the supply of larvae from the Lab Colony. Petri dishes were then placed inside a food storage container and kept at 23 (±1)◦ C and 16 : 8 h light : dark photoperiod. Larvae were examined after 7 days and mortality recorded. Mortality was determined by probing larvae with a fine camel’s-hair brush; any controlled movement in response to touch was scored as alive. For our purpose, a ‘controlled movement’ was defined as the larva having the ability to move one body length when probed.

TE

toxicity to the same natural enemies. The registration of novel insecticides, especially those with a narrow spectrum of activity, allows natural controls to combat secondary pests that can be serious problems in disrupted management systems. Here we chronicle the development of an insecticide control program for L subjuncta. Laboratory bioassays established baseline tolerance levels of L subjuncta to several classes of insecticide. Field trials were conducted with insecticides that showed the greatest potential for management of L subjuncta. In addition, dose–mortality data for azinphos-methyl from several field-collected L subjuncta populations are presented as well as the relative change in susceptibility of one population over several generations after being removed from selection pressure. A discussion of why L subjuncta may have emerged as a pest in Washington orchards and the current approach to its management is included.

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

2.4 Stage-specific activity of spinosad and endosulfan The relative susceptibilities of L subjuncta first, third and fifth instars to spinosad and endosulfan were evaluated using the leaf disk bioassay method. Larvae of the F3 generation from the 2000 Chelan colony were segregated by instar using head-capsule measurements.12 Neonate larvae were assayed in 50 × 9 mm Petri dishes as described in Section 2.1, whereas third and fifth instars were assayed in plastic portion cups (0.1 litre, #S-300, Prairie Packaging, Inc, Bedford Park, Illinois). Treated leaf disks were placed inside an arena to which five L subjuncta larvae were added (25 larvae per concentration). Larval mortality was determined as described in Section 2.1. 2.5 Azadirachtin cohort study The effect of azadirachtin on neonate and thirdinstar L subjuncta was evaluated using a modified Pest Manag Sci 60:000–000 (online: 2004)

N

U

Pest Manag Sci 60:000–000 (online: 2004) Asana XL Surround WP Raynox

Azinphos-methyl Chlorpyrifos Phosmet Malathion/methoxychlor Indoxacarb

Esfenvalerate Kaolin

Raynox

Organophosphate

Synthetic pyrethroids Particle film

Oxadiazine

Azadirachtin

Neem seed extract

Avaunt 30 WDG

Guthion 50WP Lorsban 50WP Imidan 70WP

Ecozin

Bt, var aizawai Spinosad

D

Organic

Reduced risk, OP alternative

Organic


OP alternative Reduced risk, OP alternative Not registered Organic

Chitin biosynthesis inhibitor Acetyl choline esterase inhibitor


Voltage-dependent sodium channel blocker Sodium channel modulator Disrupts normal insect behavior

Acetyl choline receptor modulator General insect growth regulator activity Acetyl choline esterase inhibitor

Microbial disrupters of insect midgut membrane

GABA-gate chloride channel antagonist Acetylcholine receptor agonists/antagonist

Chloride channel activator Ecdysone agonists/disrupter

Mode of action

OP alternative Reduced risk, OP alternative

Registration program

FS

O

EI DuPont de Nemours & Co, Inc N/A Engelhard Corp 56 069.0 × 3 applications Washington St Univ N/A

O

N/A 1,682.1 N/A N/A 126.2

N/A

N/A N/A N/A N/A N/A N/A N/A 105.2

N/A 350.5 N/A N/A 1,121.4 N/A 1,513.9 N/A

PR

Bayer Corp Dow AgroSciences Gowan Co Wilbur-Ellis Co EI DuPont de Nemours & Co, Inc

Amvac Chem Corp

TE

Syngenta Crop Protection Cerexagri, Inc Bayer Corp Valent Ag Products Certis USA, LLC Ecogen, Inc Valent Ag Products Dow AgroSciences

Syngenta Crop Protection Dow AgroSciences Dow AgroSciences Makhteshim Agan UAP-Platte Chem Co Aventis CropScience EI DuPont de Nemours & Co, Inc FMC Corp

Registrant

EC

Naturalyte spinosyns

Microbial

R

Actara Assail 70WP Calypso 4F Dipel DF Javelin Crymax Xentari Success 2 SC

O R

Thiamethoxam Acetamiprid Thiacloprid Bacillus thuringiensis, var kurstaki

C

Chloronicotinyl

Trade name Proclaim 5 SG Intrepid 2F Confirm 2F Diamond 7.5 WG Carbaryl 50WP Larvin 3.2EC Lannate LV Thiodan 50WP

Active ingredient

Avermectin Emamectin benzoate Benzoic acid hydrazide Methoxyfenozide Tebufenozide Benzoylphenyl urea Difluorobenzamide Carbamate Carbaryl Thiodicarb Methomyl Chlorinated cyclodiene Endosulfan

Insecticide class

Rate in field trials (g AI ha−1 )

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

Table 1. Insecticides evaluated for activity against Lacanobia subjuncta, 1999–2001

Management of Lacanobia subjuncta

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

3


R

O R

C

N

4

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

D

PR

O

O

FS

2.7 Field trials Candidate insecticides as determined by laboratory screening were evaluated in comparison with an industry standard and an untreated control for their ability to control L subjuncta larvae in a series of field trials conducted in apple orchards from 1998 through 2001. Tests were conducted in seven apple orchards in central Washington. The orchards differed as to apple cultivar but in all cases consisted of mature trees. Treatments were applied to approximately 0.13ha plots, replicated three times in a randomized complete block. All treatments were applied with a Rears Pack-Blast air-blast sprayer calibrated to deliver 950 litre ha−1 at 1378 kPa. The generalized timing of application was one spray targeted at the initial appearance of a fourth instar. Orchard sampling indicated that this event occurred when 75% of eggs had hatched. An exception to this generalized protocol was with the organically registered product Surround WP. This product was applied three times at 7-day intervals initiated at the start of oviposition, three applications at 7-day intervals initiated at egg hatch, and six applications at 7-day intervals covering the majority of the oviposition and hatch periods as determined by orchard monitoring. Since sampling protocols for measuring L subjuncta populations had not been optimized, insecticide efficacy was assessed initially by fruit injury (1998) and then by foliage infestation as measured by recent feeding damage at the end of the larval development period. It appeared that foliage damage was a more discriminating measure of treatment effect, especially when pest densities were low to moderate. Twenty-five fruits or 25 growing shoots were examined on each of 10 trees per replicate (750 fruits and shoots per treatment). The number of shoots or fruits damaged by larval feeding was recorded.

EC

2.6 Particle film choice tests Two insecticides using particle film technology, Surround WP and Raynox , were evaluated in direct choice tests for their ability to deter neonate L subjuncta larvae from colonizing an apple leaf disk. Treatments were prepared by diluting the appropriate amount of product (equivalent to 56.1 kg Surround WP per 1870 litre water or 125 g litre−1 Raynox AI) in water (0.5 litre) in a glass beaker. An untreated control was prepared using water alone. Untreated apple leaves were collected from ‘Delicious’ trees at the WSU Tree Fruit Research and Extension Center, Wenatchee, Washington. Leaves were dipped into the particle film solutions, then allowed to dry. The same leaves were dipped again into the same treatment, providing a coating mimicking two applications which is typical of the use pattern recommended in Washington orchards (Engelhard Corp, pers comm) for each product. One leaf disk (2.3 cm diameter) was taken from each leaf. Two disks were placed in a Petri dish (Falcon 1006, 50 × 9 mm) but did not touch. The bioassay consisted of 50 arenas with a direct choice test (one treated and one untreated leaf disk). Ten positive controls (two treated disks) and ten negative controls (two untreated disks) were also established to evaluate any potential mortality that may have resulted from the particle film treatments. Petri dishes were chosen randomly and two 2- to 5-day-old larvae were placed on the leaf disks. The Petri dish lids were put in place, and dishes were stored inside a food storage container and kept at 23 (±1)◦ C constant temperature and 16:8 h light:dark photoperiod. Choice test arenas were examined after 5 days. The 5-day evaluation period was established because healthy larvae could consume an entire leaf disk in that time, thus effectively eliminating any ‘choice’ thereafter. Larval survival in the positive and negative controls was recorded after 10 days. Mortality

in the control arenas was extended to allow a full expression of particle film treatment effects.

TE

leaf disk bioassay. Our observations of lepidopteran behavior following exposure to azadirachtin residues suggested that delayed mortality was an important factor and the standard leaf disk bioassay would not be sufficient to characterize adequately the efficacy of this product. Three cohorts of 50 neonate larvae each were established for a longer-term analysis of azadirachtin efficacy. The first cohort was exposed as neonates to a concentration equivalent to a dilute field rate (6.2 mg litre−1 ) using the leaf disk technique described in Section 2.1. This larval cohort was reared on treated leaf disks for 14 days, then transferred to untreated leaf disks for the remainder of the test. The second cohort was reared on untreated leaf disks for 14 days before being exposed to treated leaf disks. At 14 days this cohort consisted primarily of third and fourth instars. After a 14-day exposure to treated leaf disks this cohort was transferred back to untreated foliage. The third cohort of larvae was reared solely on untreated leaf disks. Each cohort was replicated three times (150 larvae per treatment). Larvae were checked weekly and mortality noted through 28 days.

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

2.8 Statistical analysis Probit regression lines were estimated using the probit option of POLO.13 The LC50 value alone does not provide much insight into the relative toxicity of an insecticide against a pest; therefore, we calculated a toxicity ratio, the LC50 divided by the dilute field rate concentration. Mean mortality data in the azadirachtin cohort study were corrected by Abbott’s formula.14 Particle film choice tests were analyzed with a chi-square goodness-of-fit test (P = 0.05). To normalize field trial data, the average percentage fruit injury or average percentage shoots with feeding injury was Log(X + 1) transformed.15 Field trial and azadirachtin cohort data were analyzed using a oneway analysis of variance (ANOVA). Mean separations were determined by Student’s paired t test (P = 0.05) using JMP statistical software.16 Pest Manag Sci 60:000–000 (online: 2004)


0.025 suggested that it would be a good candidate for further testing in field trials for control of L subjuncta (Table 2). Endosulfan had an LC50 value higher than emamectin benzoate, 1.8 mg litre−1 versus 0.1 mg litre−1 , but endosulfan is used at a much higher concentration so that the relative toxicity ratio was actually lower, 0.004. Two carbamate insecticides, thiodicarb and methomyl, had similar LC50 values, 12.6 and 12.0 mg litre−1 , respectively, along with similar low relative toxicity ratios, 0.070 and 0.089. The other carbamate evaluated, carbaryl, had a higher LC50 value and a relative toxicity ratio that was three to four times higher than those of thiodicarb and methomyl. All of these carbamate insecticides might be effective as field controls for L subjuncta, but we would expect carbaryl to be the weaker candidate. Three insecticides in the chloronicotinyl class, a group that is relatively new to the apple

Table 2. Probit analysis of various insecticides against neonate Lacanobia subjuncta larvaea using a leaf disk bioassayb , 1999–2001

LC50 (mg litre−1 ) (95% CI)

Chelan-F3

150

3.6 (1.1)

0.1 (0.06–0.13)

2000 2000 2000 2000

Chelan-F3 Chelan-F3 Chelan-F3 Chelan-F3

125 125 125 125

1.8 (0.8) 2.2 (1.8) 25.7 (25.7) 1.1 (0.5)

11.0 kg ha−1 (—)e 17.4 kg ha−1 (—)e 4.5 kg ha−1 (—)e 17.0 kg ha−1 (—)e

Carbamate Carbaryl Thiodicarb Methomyl

2000 2000 2000

Chelan-F3 Chelan-F3 Chelan-F3

150 150 150

2.4 (0.7) 2.8 (0.5) 2.0 (0.3)

Chlorinated cyclodiene Endosulfan

2000

Chelan-F3

150

2.2 (0.5)

Chloronicotinyl Thiamethoxam Acetamiprid Thiacloprid

2000 2000 2000

Chelan-F3 Chelan-F3 Chelan-F3

200 150 175

Growth regulator Tebufenozide Methoxyfenozide Difluorobenzamide

1999 2000 2001

Quincy-F1 Chelan-F1 Lab Colony

Organophosphate Chlorpyrifos Phosmet Azinphos-methyl Malathion

2000 2000 2000 2000

Spinosyn Spinosad

4

Toxicity ratiod 0.025

63.6 (18.9–104.6) 12.6 (9.3–16.9) 12.0 (7.4–20.3)

300 180 135

0.212 0.070 0.089

1.8 (0.9–2.8)

450

0.004

3.8 (0.9) 3.0 (0.6) 3.9 (1.1)

43.4 (30.9–57.2) 71.3 (46.8–100.3) 110.3 (62.5–149.5)

15 45 56

2.893 1.584 1.970

150 150 400

2.5 (0.5) 1.3 (0.3) 1.6 (0.4)

47.8 (33.5–74.6) 6.2 (2.3–14.0) 0.20 (0.04–0.41)

93 75 8

0.514 0.083 0.025

Chelan-F3 Chelan-F3 Chelan-F1 Chelan-F3

200 150 150 150

2.5 (0.4) 2.1 (0.5) 2.6 (0.4) 2.8 (1.2)

1.0 (0.6–1.5) 171.4 (48.0–303.0) 408.3 (301.4–557.3) 9.1 (1.8–13.8)

500 850 300 750

0.002 0.202 1.361 0.012

Quincy-F1

150

2.0 (0.6)

1.9 (0.3–3.4)

30

0.063

2000

Chelan-F3

150

2.4 (0.6)

1.6 (0.9–2.5)

30

0.053

2000

Chelan-F3

150

2.3 (0.9)

0.2 (0.02–0.3)

25

0.008

D

TE

EC

R

O R

PR

10.000 15.818 4.091 15.455

1999

Synthetic pyrethroid Esfenvalerate

Dilute field rate (mg litre−1 )

1.1 kg ha−1 1.1 kg ha−1 1.1 kg ha−1 1.1 kg ha−1

N

Oxadiazine Indoxacarb

2000

C

Avermectin Emamectin benzoate Bacillus thuringiensis Dipel DF Javelin Crymax Xentari

Source

O

Slope (SE)

Year

O

nc

Class chemical

a

Colony source: collected from Chelan, Washington (Naumes, Chelan Ranch) in spring 2000. For those chemicals bioassayed against larvae from the colony, the number of generations past the fiducial generation is indicated by ‘F’. b Mortality assessed after 7 days exposure to treated leaves. c n, number of larvae assayed. d LC50 : dilute field rate; measure of relative toxicity of various products. e Poor data fit, no confidence intervals generated.

Pest Manag Sci 60:000–000 (online: 2004)

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

FS

3 RESULTS 3.1 Laboratory bioassays Table 2 summarizes the probit analysis for all the insecticides evaluated using the leaf disk bioassay method. The test year, source of population, number of larvae used in the probit analysis, slope of the probit line with standard error, LC50 value including 95% confidence limits and dilute concentration of the insecticide based on the manufacturer’s recommendation are given. The toxicity ratio provided some relative means for comparison between candidate insecticides, and a measure to narrow the potential candidates for the field trial program, especially among those within a specific class of insecticide where the mode of action and behavior in the environment are similar. Emamectin benzoate had a low LC50 value, 0.1 mg litre−1 , and though its proposed dilute field rate is low, 4 mg litre−1 , the relative toxicity ratio of

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

5


of other lepidopteran pests. Thus, it was considered unlikely that Bt products would be suitable candidates for L subjuncta management.

TE

D

PR

O

O

3.3 Stage-specific activity of spinosad and endosulfan Spinosad and endosulfan both had low LC50 values and low relative toxicity ratios against neonate L subjuncta (Table 4). However, when third and fifth instars were used in the bioassay the LC50 values for spinosad increased, from 1.6 mg litre−1 to 34.5 mg litre−1 for fifth instars, and relative toxicity ratios decreased, indicating that its efficacy had decreased significantly (Table 4). There was little change in the LC50 value or relative toxicity ratio of endosulfan between neonates and third instars, but there was a significant increase in the LC50 value and relative toxicity ratio against fifth instars (Table 4). The data in this experiment were more variable against fifth instars, thus confidence limits around the LC50 value were not generated for either product against this instar.

R

O R

3.4 Azadirachtin cohort study The L subjuncta larvae exposed to azadirachtin residues as young larvae (Cohort-1) showed increasing

Year

Azinphos-methyl Azinphos-methyl Azinphos-methyl Azinphos-methyl Azinphos-methyl Azinphos-methyl Azinphos-methyl

2000 2000 2000 2000 2000 2001 2001

Source

Azwell-F1 Quincy-F1 Chelan Falls-F1 Royal Slope-F1 Chelan-F1 Chelan-F5 Chelan-F8

N

Chemical

C

Table 3. Susceptibility of field-collected Lacanobia subjuncta populationsab to azinphos-methyl and changes in the susceptibility of one population removed from selection pressure for eight generations

nc

150 150 150 150 150 150 300

Slope (SE)



Toxicity ratiod

4.1 (0.8) 4.7 (1.8) 2.6 (0.4) 4.3 (1.8) 2.6 (0.4) 2.3 (0.8) 3.8 (1.0)

1,112.2 (852.5–1471.5) 725.2 (329.4–928.4) 725.8 (546.4–1010.1) 893.1 9 (—)e 408.3 (301.4–557.3) 241.5 (158.7–534.0) 97.0 (41.2–145.0)

300 300 300 300 300 300 300

3.707 2.417 2.419 2.977 1.361 0.505 0.323

a Colony source: collected from Chelan, Washington (Naumes, Chelan Ranch) in spring 2000. For those chemicals bioassayed against larvae from the colony, the number of generations past the fiducial generation is indicated by ‘F’. b Mortality assessed after 7 days exposure to treated leaves. c n: number of larvae assayed. d LC50 : dilute field rate; measure of relative toxicity of various products. e Poor data fit, no confidence intervals generated.

6

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

FS

3.2 Susceptibility to azinphos-methyl and reversion through time Lacanobia subjuncta larvae from five different orchards had extremely high LC50 values for azinphos-methyl, especially considering that neonates were tested (Table 3). The relative toxicity ratios ranged from 1.36 to 3.71, suggesting that it would be very difficult to control L subjuncta with field applications of azinphos-methyl. One population, Chelan, was removed from any insecticide selection pressure by continuous laboratory rearing and showed increased susceptibility to azinphos-methyl after five generations (Chelan-F5), and this trend continued into the eighth generation (Chelan-F8, Table 3).

EC

industry, had LC50 values that ranged from 43.4 to 110.3 mg litre−1 , all higher values than the dilute field rate concentrations for these insecticides. These data suggest that all three chloronicotinyl insecticides would not be very toxic to L subjuncta and therefore not good candidates for field trials. Two closely related molt accelerating compounds, tebufenozide and methoxyfenozide, showed some significant differences against L subjuncta. The LC50 for tebufenozide was eight times higher than that of methoxyfenozide, 43.3 versus 6.2 mg litre−1 . Since the recommended field rate of the two products is similar, it would be expected that methoxyfenozide would perform better under field conditions. A chitin synthesis inhibitor, difluorobenzamide, had a low LC50 value and a relative toxicity ratio even lower than that of methoxyfenozide, 0.025, and would be expected to be a good candidate for control of L subjuncta in the field (Table 2). The OP insecticide class showed variable results against L subjuncta. The most commonly used OP insecticide in Washington apple production, azinphos-methyl, had a high LC50 (408.3 mg litre−1 ) as well as a high relative toxicity ratio (1.36), suggesting that it would have a low potential to control this pest. Phosmet, a common substitute for azinphos-methyl in Washington apple production, had a lower LC50 (171.4 mg litre−1 ) and a lower relative toxicity ratio (0.202) compared to azinphos-methyl and thus might be expected to provide better control of L subjuncta than azinphos-methyl. Chlorpyrifos and malathion had the lowest LC50 values of the OP insecticides and had very low relative toxicity ratios, 0.002 and 0.012 respectively, suggesting that they would be good candidates for control of this pest. Three unrelated insecticides, indoxacarb, spinosad and esfenvalerate, had both low LC50 values and relative toxicity ratios, suggesting that they would be good candidates for field trials against L subjuncta. Probit analysis for Bt products was based on formulated product, since it was difficult to express concentrations in other units. All of the Bt products had high LC50 values relative to concentrations commonly used in orchards for control

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60


Management of Lacanobia subjuncta Table 4. The effect of spinosad and endosulfan against different stages of Lacanobia subjuncta larvaea using a leaf disk bioassay.b

Chemical

Year

Source

nc

Spinosad Spinosad Spinosad Endosulfan Endosulfan Endosulfan

2000 2000 2000 2000 2000 2000

Chelan-F3 neonates Chelan-F3 3rd instar Chelan-F3 5th instar Chelan-F3 neonates Chelan-F3 3rd instar Chelan-F3 5th instar

150 150 150 150 150 150

Slope (SE)



Toxicity ratiod

2.4 (0.6) 1.8 (0.5) 1.7 (1.3) 2.2 (0.5) 1.4 (0.4) 0.9 (0.4)

1.6 (0.9–2.5) 13.9 (3.5–28.2) 34.5 (—)e 1.8 (0.9–2.8) 2.0 (0.2–5.3) 95.7 (—)e

30 30 30 450 450 450

0.053 0.463 1.150 0.004 0.004 0.213

a Colony source: collected from Chelan, Washington (Naumes, Chelan Ranch) in spring 2000. For those chemicals bioassayed against larvae from the colony, the number of generations past the fiducial generation is indicated by ‘F’. b Mortality assessed after 7 days exposure to treated leaves. c n, number of larvae assayed. d LC : dilute field rate; measure of relative toxicity of various products. 50 e Poor data fit, no confidence intervals generated.

0.0 a 0.0 a 20.9 b 63.5 b

a

Means in the same row followed by the same letter not significantly different (P = 0.05, Student’s paired t test). Means followed by the letter ‘a’ not significantly different from the untreated control.

R

EC

mortality through 14 days, but little mortality once removed from residues, days 15 through 28 (Table 5). Larvae in the second azadirachtin-treated cohort (Cohort-2) showed no mortality relative to the untreated control (Cohort-3) until larvae were exposed to azadirachtin residues, days 15 through 28. The final corrected percentage mortalities of Cohort-1 and Cohort-2 after 28 days were essentially the same (Table 5).

N

C

O R

3.5 Particle film choice tests Both particle film products deterred L subjuncta feeding activity on leaf disks in choice tests at equivalent levels. After 5 days in the choice-test arenas, a small proportion of L subjuncta larvae, 0.063 (chisquare 38.118, P < 0.0001) and 0.173 (chi-square 43.226, P < 0.0001), were found on the Surroundor Raynox- treated leaf disks, respectively. In arenas where there was no choice, mortality of L subjuncta larvae was high, 100%, in the Surround treatment compared with only 10% in the untreated control. In arenas with only Raynox treated disks larval mortality was the same as arenas with untreated leaf disks, 37%. 3.6 Field trials Field trials were conducted over a period of 4 years in seven different orchards throughout central Washington. Carbaryl, an insecticide commonly used Pest Manag Sci 60:000–000 (online: 2004)

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

FS

13.0 a 51.8 b 62.0 c 67.0 b

O

Cohort-2

O

Day 7 Day 14 Day 21 Day 28

Cohort-1

PR

Days after test started

D

Avg corrected mortality (%)a

in Washington orchards during late spring and early summer, and methomyl, an insecticide known to be highly toxic to lepidopteran pests, were applied after the first appearance of fourth instars (Quincy, Washington, 1998). Carbaryl was unable to protect the fruit from injury, while methomyl prevented fruit injury from occurring (F = 9.57, df = 2; P = 0.014) (Table 6). Spinosad was evaluated at different rates along with chlorpyrifos, the industry standard for L subjuncta control at the time (Othello, Washington, 1998). All treatments were applied at the same timing and significantly reduced fruit injury relative to the untreated control with no significant difference noted among the treatments (F = 3.54; df = 4; P = 0.048) (Table 6). Chlorpyrifos reduced fruit injury by 88% compared to the untreated control, but spinosad still appeared to be a suitable substitute even at reduced rates. The particle film Surround WP was evaluated for its ability to deter oviposition and larval feeding (Quincy, Washington, 1999). All Surround WP treatments significantly reduced the percentage of shoots with larval feeding damage relative to the untreated control (F = 16.87; df 3; P < 0.001) (Table 6). Surround WP applied at oviposition or egg hatch resulted in 70 and 89% reduction in shoots with larval feeding damage, respectively, but with no statistical difference between the treatments. When Surround WP was applied at both oviposition and egg hatch (six applications total) there was a 93% reduction in shoots with larval feeding damage, and this was significantly less shoot feeding than with the Surround WP treatment applied only at oviposition. Surround WP residues persisted on the trees, and thus the options of reducing the rate or number of applications are plausible. A trial (Royal Slope, Washington, 2000) was conducted to optimize the rate and timing of indoxacarb. Applications of indoxacarb were timed at initial egg hatch or at the first appearance of fourth instars and compared with a chlorpyrifos treatment applied at egg hatch. All indoxacarb treatments significantly suppressed the percentage

TE

Table 5. Corrected percentage mortality of different age cohorts of Lacanobia subjuncta larvae exposed to azadirachtin residues using a leaf disk bioassay, 2000

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

7

MD Doerr, JF Brunner, LE Schrader Table 6. Control of Lacanobia subjuncta larvae in the apple orchards using candidate insecticides, 1998–2001

Rate (g AI ha−1 )

Insecticide

Fruit injury (%)a

Timing

1998 Quincy, 1st generation Carbaryl Methomyl Untreated

1121.4 1513.9

4th instar larva 4th instar larva

0.4 b 0.0 a 0.5 b

1998 Othello, 1st generation Spinosad Spinosad Spinosad Chlorpyrifos Untreated

70.1 105.2 140.3 1682.1

4th instar larva 4th instar larva 4th instar larva 4th instar larva

0.2 0.3 0.3 0.1 0.8

Rate (g AI ha−1 )

1999 Quincy, 1st generation Surround Surround Surround

Shoots with feeding injury (%)a

Timing Oviposition, +7 days, +7 days Hatch, +7 days, +7 days Oviposition, +7 days, +7 days, +7 days, +7 days, +7 days

56 069.0 56 069.0 56 069.0

a a a a b

30.0 b 11.3 ab 6.7 a

99.7 c

4th instar larva 4th instar larva 4th instar larva 4th instar larva 4th instar larva 4th instar larva

2001 Brewster, 1st generation Indoxacarb Indoxacarb Indoxacarb Indoxacarb Spinosad Methoxyfenozide Untreated

63.0 84.0 105.0 126.2 105.0 280.3

O

63.0 84.0 105.0 126.2 105.0 280.3

PR

2001 Orondo, 1st generation Indoxacarb Indoxacarb Indoxacarb Indoxacarb Spinosad Methoxyfenozide Untreated

D

Initial egg hatch Initial egg hatch 4th instar larva 4th instar larva Initial egg hatch

O R

R

EC

TE

124.0 100.8 124.0 100.8 1682.1

O

Untreated 2000 Royal Slope, 1st generation Indoxacarb Indoxacarb Indoxacarb Indoxacarb Chlorpyrifos Untreated

4th instar larva 4th instar larva 4th instar larva 4th instar larva 4th instar larva 4th instar larva

0.3 1.6 1.5 1.6 19.3 32.1

a a a a b c

3.6 1.4 1.6 1.4 7.4 2.8 39.2

a a a a a a b

2.4 1.4 2.0 1.4 2.0 1.2 11.6

a a a a a a b

C

a Means in the same column of a particular test followed by the same letter not significantly different (P = 0.05, Student’s paired t test). Statistics were performed on transformed data, Log(X + 1).

N

of shoot feeding (95–99%) with no significant rate or timing effects noted (F = 41.50; df = 5; P < 0.001) (Table 6), and all indoxacarb treatments had lower percentage shoot feeding than chlorpyrifos. Chlorpyrifos reduced shoot feeding by only 40%, suggesting that the timing used was too early for this product. These data indicate that indoxacarb could be a suitable replacement for chlorpyrifos and that different timing options of indoxacarb against L subjuncta are possible. Based on data from the previous test (Royal Slope, Washington, 2000) two indoxacarb rate trials were conducted to evaluate lower rates compared to label 8

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

FS

Insecticide

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

rates of spinosad and methoxyfenozide (Orondo, Washington, 2001; Brewster, Washington, 2001). All treatments were applied at the first appearance of fourth instars. All treatments significantly reduced percentage shoot feeding relative to the untreated control at both locations (83–90% in Orondo, 91–97% in Brewster), and there was no statistical difference among the treatments in either test (Orondo F = 72.4; df = 6; P < 0.001; Brewster F = 17.52; df = 6; P < 0.001) (Table 6). These data suggest that spinosad, methoxyfenozide, and reduced rates of indoxacarb were all suitable candidates for control of L subjuncta. Pest Manag Sci 60:000–000 (online: 2004)


R

O R

C

N


61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

PR

O

O

FS

To optimize the use of insecticides with a narrow spectrum of activity, it was important to direct insecticide applications at the most susceptible life stages. While chlorpyrifos and endosulfan controlled all L subjuncta instars, selective or ‘softer’ products (eg spinosad) were more effective against early instars. Optimizing the application timing of softer insecticides will be critical to maintaining control of L subjuncta while promoting integrated pest management. Doerr et al 12 described the response of L subjuncta to temperature. The use of these data to develop a predictive degree-day model would allow a pestmanagement practitioner to target applications when the majority of eggs had hatched but while larvae were still in a stage susceptible to soft products. EPA programs such as Reduced Risk and OP Replacement have provided for the registration of new viable alternatives for control of L subjuncta. Based on this study, Washington apple producers can now choose from three insecticides, methoxyfenozide, spinosad and indoxacarb, that are effective against L subjuncta.27 These insecticides have further advantages over the OP insecticides that they are replacing. First, their unique modes of action allow for practical resistance management through product rotation; second, their short re-entry intervals (4–12 h) make managing the orchard labor force easier; and finally, they selectively conserve natural enemies.28

TE

D

ACKNOWLEDGEMENTS This research was in part funded by a grant from the Washington Tree Fruit Research Commission, and we are grateful to the Commission and the fruit growers of Washington for their support. We are grateful for the assistance of Heath Ohler, Amy Blankenship and Julie Nichols for their quality work in the laboratory and field and Kathleen Pierre for providing a constant supply of laboratory-reared larvae. We would also like to thank Christian Krupke for a critical review of this manuscript.

EC

4 DISCUSSION The sudden increase in pest status of L subjuncta in the late 1990s is not well understood, but different hypotheses have been proposed. Landolt17 suggested that mild winters might allow L subjuncta to survive in larger numbers. The dry summer would then drive L subjuncta from its preferred weed hosts to irrigated orchards. Furthermore, he theorized that genetic adaptations could have altered the insect’s host range or preference. While these explanations remain possibilities, our data suggest that L subjuncta became resistant to OP insecticides, especially azinphosmethyl, the most common OP used in Washington apple orchards. Azinphos-methyl has been used at least one time per year in the majority, 58–98%, of apple orchards over the last decade.18 Landolt19 showed that L subjuncta was able to develop on a wide variety of weeds and crop plants common to eastern Washington, and it is therefore very likely that they were exposed to residues of azinphos-methyl and other OP insecticides. Several authors have speculated that surges in secondary pests such as C rosaceana in Quebec, Canada,20 tufted apple bud moth, Platynota idaeusalis Walker (Lepidoptera: Tortricidae) in Pennsylvania,21 – 23 light brown apple moth, Epiphyas postvittana (Walker) (Lepidoptera: Tortricidae) in New Zealand,24 and spotted tentiform leafminer, Phyllonorycter blancardella (F) (Lepidoptera: Gracillariidae) in North Carolina25 were attributed to the development of resistance to azinphos-methyl. The high level of tolerance to azinphos-methyl in five geographically separated populations of L subjuncta supports our hypothesis that this pest escaped suppression by normal insecticide control programs, leading to increased densities in apple orchards. While we have not been able to locate a field population of L subjuncta that is susceptible to azinphos-methyl, the reversion of susceptibility in the laboratory once a population was removed from selection pressure suggests resistance as a reasonable explanation for the increase in its pest status. The evident susceptibility of L subjuncta larvae to chlorpyrifos but not to phosmet or azinphos-methyl resembles the pattern of resistance and negatively correlated cross-resistance reported by Dunley and Welter26 in codling moth. While this does not prove that L subjuncta developed resistance to azinphos-methyl, it is interesting that two insects, each exposed to azinphos-methyl for many years, showed similar patterns of susceptibility to the same insecticides. The establishment of baseline tolerances for L subjuncta to new insecticides, as well as those used in apple orchards for decades, provides a database to evaluate future reports of control failures. The toxicity ratio provided a good indication of an insecticide’s potential for inclusion in a field trial program. However, the toxicity ratio should not be viewed as a direct predictor of field efficacy, since it does not address the issues of residual activity, delayed mortality, or sub-lethal effects.

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60

REFERENCES 1 Pesticide Registration Notice 98–7, Office of Pesticide Programs, United States Environmental Protection Agency (1998). 2 Brunner JF, Dunley JE, Doerr MD and Beers EH, Effect of pesticides on Colpoclypeus florus (Walker) (Hymenoptera: Eulophidae) and Trichogramma platnera (Nagarkatti) (Hymenoptera: Trichogrammatidae), parasitoids of leafrollers in Washington. J Econ Entomol 94:1075–1084 (2002). 3 Calkins CO, Review of the codling moth areawide suppression program in the western United States. J Agric Entomol 15:327–333 (1998). 4 Gut LJ, Brunner JF, Thayer G and Brown JJ, SARE Project: production of apples without the input of broad-spectrum insecticides. Proc Wash State Hort Assoc (Washington State Horticultural Association, Wenatchee, Washington) 92:239–241 (1996). 5 Thomson DJ, Brunner JF, Gut LJ, Judd G and Knight AL, Ten years implementing codling moth mating disruption in the 9


12

13 14 15 16 17

N

C

O R

R

EC

18

10

61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120

FS

11

O

10

O

9

PR

8

D

7

19 Landolt PJ, Survival and development of Lacanobia subjuncta (Grote and Robinson) (Lepidoptera: Noctuidae) larvae on common weeds and crop plants of eastern Washington. PanPac Entomol 78:1–6 (2002). 20 Smirle MJ, Vincent C, Zurowski CL and Rancourt B, Azinphosmethyl resistance in the obliquebanded leafroller, Choristoneura rosaceana: Reversion in the absence of selection and relationship to detoxication enzyme activity. Pestic Biochem Physiol 61:183–189 (1998). 21 Knight AL, Hull LA, Rajotte E, Hogmire H, Horton D, Polk D, Walgenbach J, Weires R and Whalon J, Monitoring azinphosmethyl resistance in adult male Platynota idaeusalis (Lepidoptera: Tortricidae) in apple from Georgia to New York. J Econ Entomol 83:329–334 (1990). 22 Biddinger DJ, Hull LA and McPheron BA, Cross-resistance and synergism in azinphos-methyl resistant and susceptible strains of tufted apple bud moth (Lepidoptera: Tortricidae) to various insect growth regulators and abamectin. J Econ Entomol 89:274–287 (1996). 23 Bush MR, Abdel-Aal YAI, Saito K and Rock GC, Azinphosmethyl resistance in the tufted apple bud moth (Lepidoptera: Tortricidae): reversion, diagnostic concentrations, associated esterases, and glutathione transferases. J Econ Entomol 86:213–225 (1993). 24 Suckling DM, Rogers DJ, Shaw PW, Wearing CH, Penman DR and Chapman RB, Monitoring azinphos-methyl resistance in the light brown apple moth (Lepidoptera: Tortricidae) in New Zealand. J Econ Entomol 80:733–738 (1987). 25 Walgenbach JF, Gorsuch CS and Horton DL, Adult phenology and management of spotted tentiform leafminer (Lepidoptera: Gracillariidae) in North Carolina, South Carolina, and Georgia. J Econ Entomol 83:985–994 (1990). 26 Dunley JE and Welter SC, Correlated insecticide crossresistance in azinphos-methyl resistant codling moth (Lepidoptera: Tortricidae). J Econ Entomol 93:955–962 (2000). 27 Smith TJ, Dunley JE, Beers EH, Brunner JF, Grove GG, Xiao CL, Elfving D, Peryea FJ, Parker R, Bush M, Daniels C, Maxwell T, Foss S and Roberts S, 2003 Crop protection guide for tree fruits in Washington, Washington State Univ Coop Ext, EB 0419 (2003). 28 Brunner, JF, Dunley JE, Doerr MD and Beers EH, Effect of pesticides on Colpoclypeus florus (Walker) (Hymenoptera: Eulophidae) and Trichogramma platneri (Nagarkatti), parasitoids of leafrollers in Washington. J Econ Entomol 94:1075–1084 (2001).

TE

6

orchards of Washington and British Columbia: starting right and managing for success. IOBC wprs Bulletin (Montfavet, France) 24:23–30 (2001). Knight AL, The impact of codling moth (Lepidoptera: Tortricidae) mating disruption on apple pest management in Yakima Valley, Washington. J Entomol Soc Br Col 92:29–38 (1996). Beers EH, Brunner JF, Willett M and Warner G, Orchard Pest Management: a resource book for the Pacific Northwest, Good Fruit Grower, Yakima, Washington, pp 20–21 (1993). Beers EH, Dunley JE, Brunner JF, Grove GG, Williams KM, Peryea FJ, Smith TJ, Parker R, Mayer DF, Bush M, Daniels C, Maxwell T and Roberts S, 1996 Crop protection guide for tree fruits in Washington, Washington State Univ Coop Ext, EB 0419 (1996). Landolt PJ, Cutworm on organic apples is identified as new, The Good Fruit Grower (Good Fruit Grower, Yakima, Washington) 48:28–29 (1997). Brunner JF and Doerr MD, Timing and products for the control of lacanobia fruitworm, in Proc Wash State Hort Assoc, Washington State Horticultural Association, Wenatchee, Washington, pp 144–147 (2000). Smith TJ, Dunley JE, Beers EH, Brunner JF, Grove GG, Willemsen KM, Peryea FJ, Parker R, Mayer DF, Bush M, Daniels C, Maxwell T and Roberts S, 2001 Crop protection guide for tree fruits in Washington, Washington State Univ Coop Ext, EB 0419 (2001). Doerr MD, Brunner JF and Jones VP, Temperature-dependent development of Lacanobia subjuncta (Lepidoptera: Noctuidae). Environ Entomol 31:995–999 (2002). POLO-PC, a user’s guide to Probit or Logit analysis, LeOra Software, Berkeley, California (1987). Abbott WS, A method of computing the effectiveness of an insecticide. J Econ Entomol 18:265–267 (1925). Bartlett MS, The use of transformations. Biometrics 3:39–52 (1947). JMP statistics and graphics guide, version 3.2.6, SAS Institute, Cary, North Carolina (1995). Landolt PJ, Lacanobia subjuncta (Lepidoptera: Noctuidae) on tree fruits in the Pacific Northwest. Pan-Pac Entomol 74:32–38 (1998). Brunner JF, Jones W, Beers EH, Tangren GV, Dunley JE, Xiao CL and Grove GG, A decade of pesticide use and IPM practices in Washington apple orchards. Agric Environ News 205:1–16 (2003).

U

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60
