J Appl Entomol. 2020;144:109–122. wileyonlinelibrary.com/journal/jen  | 109© 2019 Blackwell Verlag GmbH

1  | INTRODUC TION

With the successful implementation of mating disruption for cod‐ling moth (Cydia pomonella), pear psylla, Cacopsylla pyricola (Förster) (Homoptera: Psyllidae) and two‐spotted spider mites, (Tetranychus urticae) are considered the most difficult to manage pests by Washington pear growers managing almost half of the nation's pear acreage (DuPont, 2016; Murray & DeFrancesco, 2014; NASS, 2017). Psylla produces honeydew which causes russet and black sooty mould on fruit resulting in downgraded and rejected fruit.

Natural enemies are a potentially important component of suc‐cessful integrated pest management (IPM) in Pacific Northwest pear orchards. Predaceous true bugs, lady beetles, lacewings, ear‐wigs and parasitic wasps can suppress psylla populations (Horton, 2004; Horton et al., 2002; Horton & Lewis, 2000; Horton, Lewis, & Broers, 2004; Murray & DeFrancesco, 2014). The obligate par‐asitoid Trechnites insidiosus (Crawford) (Hymenoptera: Encyrtidae) can have parasitism rates as high as 50% in organic systems (Beers, Brunner, Willett, & Warner, 1993). Several true bug predators are

common in pears, especially Deraeocoris brevis (Knight) (Hemiptera: Miridae) and Campylomma verbasci (Meyer). Deraeocoris brevis enters orchards early in the spring having overwintered as an adult and the first nymphal generation follows. Late instar nymph and adult D. bre‐vis are capable of destroying 175–226 eggs per day (Booth, 1992; Brunner, 1975). Campylomma verbasci overwinters as an egg within and outside orchards, and emerges just after bloom. Both adults and nymphs of C. verbasci feed on psylla. Also capable of feeding on plant tissue, C. verbasci can maintain high numbers in an orchard, one bug destroying more than 600 psylla eggs during its development (Zwick & Fields, 1977). Lacewings, including Chrysoperla plorabunda (Fitch) (Neuroptera: Chrysopidae), Chrysopa nigricornis (Burmeister) and brown lacewings (Hemerobiidae), have predaceous larvae which commonly feed on soft‐bodied pest insects such as pear psylla. Omnivorous earwigs, especially the European earwig Forficula auric‐ularia L. (Dermaptera: Forficulidae) are also known to be effective in biological control (Carroll & Hoyt, 1984).

Many of the pesticides used against pear psylla are toxic to natural enemies, resulting in orchards with few predators, and

Received:29April2019  |  Revised:14August2019  |  Accepted:17August2019DOI: 10.1111/jen.12694

O R I G I N A L C O N T R I B U T I O N

Integrated pest management programmes increase natural enemies of pear psylla in Central Washington pear orchards

Sara Tianna DuPont  | Christopher John Strohm

Agriculture and Natural Resources, Tree Fruit Research and Extension Center, Washington State University, Wenatchee, Washington

CorrespondenceSara Tianna DuPont, Agriculture and Natural Resources, Washington State University, Tree Fruit Research and Extension Center, 1100 N Western Ave, Wenatchee, WA.Email: tianna.dupont@wsu.edu

Funding informationWashington Specialty Crop Block Grant, Grant/Award Number: #K1986

AbstractNatural enemies are a potentially important component of successful integrated pest management in Pacific Northwest pear orchards. Producers in Washington have dealt with difficult pear psylla, Cacopsylla pyricola (Förster) (Homoptera: Psyllidae), pres‐sure and waning product effectiveness for decades. This study finds that integrated pest management (IPM) programmes can sustain high levels of natural enemies com‐parable to organic management. True bugs Deraeocoris brevis (Knight) (Hemiptera: Miridae) and Campylomma verbasci (Meyer), lacewings Chrysoperla plorabunda (Fitch) (Neuroptera: Chrysopidae) and Chrysopa nigricornis and the parasitic wasp Trechnites insidiosus (Crawford) (Hymenoptera: Encyrtidae) increased in abundance under IPM management. Biological‐based IPM programmes have the potential to conserve nat‐ural enemies providing biological control in late summer when conventional sprays often fail due to pesticide resistance and inability to penetrate dense canopies.

K E Y W O R D S

Deraeocoris, IPM, lacewings, natural enemies, pears, psylla, Trechnites

110  |     DuPONT aND JOHN STROHM

unsuppressed mite and psylla populations. For example, lambda‐cy‐halothrin (Warrior), spinetoram (Delegate) and novaluron (Rimon) cause more than 80% acute mortality of at least one life stage of at least one natural enemy species (Mills, Beers, Shearer, Unruh, & Amarasekare, 2016). Additionally, pesticides previously thought safe for predators have indirect effects including reduced fecundity. For example, spinetoram (Delegate) reduced fertility in Deraeocoris and Galendromus predatory mites (Mills et al., 2016) and spirotetramat (Ultor) reduced the next generation to zero even though it has a low acute toxicity (Beers, 2015).

In order to develop integrated pest management systems for pears which more fully integrate biological control, it is critical to characterize the natural enemy populations in orchards and identify management systems where biological control is optimized. Our study is designed to evaluate the ability of pest management pro‐grammes to sustain high levels of natural enemies and characterize the natural enemy population in these orchards.

2  | MATERIAL S AND METHODS

2.1 | Field sites and experimental treatments

Study sites were located in the Wenatchee River Valley, Washington USA in orchards planted primarily with D’Anjou and Bartlett varieties. Six locations were designated throughout the production zone where each location had similar growing conditions and elevations. Each treatment was applied to five‐acre study plots in each location where plots within a location were within close proximity (within one mile).

Treatments consisted of three management systems: organic, conventional and bio‐based integrated pest management (bIPM). While growers were not restricted to specific spray schedules, growers used a defined set of tools in each system. Organic manage‐ment followed the USDA‐certified organic standards (Organic Food Production Act §205) which prohibits the use of synthetic products. Conventional management was grower standard practice. bIPM used a toolbox of cultural controls and pesticides which were de‐signed to contain selective products with less documented negative impact on natural enemies (Table 1).

2.2 | Natural enemy monitoring methods

Plots were scouted once per week from early April to late September in 2017 and 2018 using beat trays and sticky traps with volatile lures.

2.2.1 | Beat trays

Within each plot, thirty branches (three to six above ground, 3/4 to 1‐1/2 inches in diameter and near‐to‐horizontal) were sampled with a beat tray. An 18 by 18‐inch white beat tray sheet was held 12–18 inches underneath each branch. Branches were tapped three times with a rubber hose. The number of natural enemies per beat tray was counted. Natural enemies included adult T. insidiosus and adult and immature stages of Araneae (spiders), Anthocoridae (minute pirate

bugs), C. verbasci (common mullein bugs), Chrysopidae (green lace‐wings), Coccinellidae (ladybeetles), D. brevis, Dermaptera (earwigs), Geocoridae (big‐eyed bugs), Hemerobiidae (brown lacewings) and Nabidae (damsel bugs).

2.2.2 | Traps

The diversity of the predator and parasitoid community present in pear orchards was examined using sticky card traps baited with lures containing plant volatiles attractive to predacious and parasitoid in‐sects. Each trap lure combination was placed in each of four repli‐cated transects in each orchard plot at a distance of at least 30 m apart and four to six feet above the ground. Each tree with a sticky card trap also contained one earwig trap. All lures were replaced at 6‐week intervals. All traps were checked once per week, and the number of insects was counted.

TA B L E 1   Bio‐based Integrated Pest Management Toolbox. Growers using this system of management selected tools from within this toolbox

Cultural controls

Season long Good coverage

Moderate fertility

Remove water sprouts

Mating disruption for codling moth

Weed management timing (with respect to mites)

Preferred chemical controlsa

Pre‐bloom Petroleum oil Lime sulphur

sulphur Buprofezin

kaolin Pyriproxyfen

Diflubenzuron Isaria fumosorosea apopka strain 97

Petal fall Petroleum oil Azadirachtin

Pyriproxyfen Buprofezin

Rosemary oil Fenbutatin oxide

Isaria fumosorosea apopka strain 97

Cover sprays Rosemary oil Spinosad

Diflubenzuron Azadirachtin

Bacillus thuringiensis subsp. kurstaki

Codling moth granulosis virus

Chlorantraniliprole Methoxyfenozide

Petroleum oil Cyantraniliprole

Cinnamon oil

Summer miticides Spirodiclofen Bifenazate

Fenbutatin oxide Clofentezine

Petroleum oil Hexythiazox

aGrowers were asked to avoid products with high negative impact on natural enemies or low efficacy including: lambda‐cyhalothrin, novalu‐ron, chlorpyrifos, thiamethoxam, malathion, esfenvalerate, acetamiprid, abamectin, pyridaben, imidacloprid and spirotetramat.

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Traps were baited with one of three lure combinations. A yel‐low sticky card (9 × 5.5 inches) with AMP lure (acetic acid 3 ml per lure + methylsalicylate 3.3 ml per lure + 2 phenylethanol 1 ml per lure) was used to collect adult green lacewings (C. plorabunda). A white sticky card (7 × 7 inches) combined with a squalene lure (0.5 ml squalene per lure) was used to collect adult green lacewing (C. nigricornis) (Jones et al., 2011). A yellow sticky card combined with a C. verbasci synthetic sex pheromone spiral (gel matrix releasing butyl butyrate compounds; Scentry biologicals) was used to collect male C. verbasci adults. Both types of yellow sticky card traps were used to collect adult T. insidiosus wasps. Additionally, adults of D. brevis, brown lacewings and ladybee‐tles were collected on all of these traps. Sections (3 × 14 inches) of sin‐gle side corrugated cardboard (3.2 corrugations per inch) were rolled into a cylindrical shape and placed in the canopies of 12 trees within each plot to sample earwigs (Helsen, Vaal, & Blommers, 1998).

2.3 | Natural enemy impact scores

The potential impacts of products on natural enemies were calcu‐lated for each spray used during the season in each plot. Individual product ratings for western predatory mites, mite predators, coc‐cinellids, lacewings and predatory true bugs were converted to nu‐merical ratings from low (1), low to medium (2), medium (3), medium to high (4) and high (5) given in the Washington State University Crop Protection Guide (DuPont, Beers, Amiri, Grove, & Nottingham, 2018). These ratings are based on literature review of multiple sources. An individual product's score is the average of the rating for each of the five natural enemy types. A plot's score is the sum of the score for each spray used during the season where higher scores equal higher natural enemy impact.

2.4 | Statistical analysis

Mean counts of each natural enemy species (C. verbasci adults and nymphs, D. brevis adults and nymphs, earwigs, lacewing adults and nymphs and T. insidiosus adults) in beat trays and traps were log‐transformed and tested for normality using the Shapiro–Wilk test. Normalized data were analysed using the mixed procedure analysis of variance (ANOVA) (SAS 9.4, 2016). A repeated measures ANOVA was performed for each of four periods containing two to ten weeks for each insect species and life stage (pre‐bloom: April 3 to 20 2017, April 3 to 12 2018; bloom: April 24 to May 11 2017, April 16 to May 3 2018; early summer: May 15 to June 29 2017, May 7 to June 28 2018 and late summer: July 3 to September 14 2017, July 2 to September 13 2018) with week (defined as weeks before and after bloom) as a repeated measure and location (block) as a random effect. Two to four plots of different treatments in close geographic proximity (<1 mile) were considered to be within one location. Two locations included only conventional and organic plots and no bIPM plot. One location had two bIPM plots. Treatment differences were discerned using Tukey's honest significant difference test (α = .05). Natural enemy impact scores were analysed using a generalized linear model ANOVA with treatment, location and year as independent variables (SAS 9.4, 2016).

To discern similarity and differences between natural enemy assemblages based on species, we used a non‐metric multidimen‐sional scaling (NMS) ordination, with Sorenson distance measure (PC‐ORD version 4.0 software, McCune and Mefford 1999). NMS is an effective method for multivariate data reduction and analysis of ecological community data sets (McCune & Grace, 2002) partic‐ularly appropriate for extracting important gradients in community

F I G U R E 1   Mean relative abundance of natural enemies in pear orchards collected per tray in 2017 (a) and 2018 (b). Immature insects (grey), adult insects (black). Larger bubbles indicate higher counts. Bubble sizes range from 0 to 1 and are relative to highest weekly mean abundance of any one insect across both years (0.4 Trechnites wasps per tray—August 2018)

112  |     DuPONT aND JOHN STROHM

composition, which can then be related to desired environmental responses. NMS is well‐suited to data that are non‐normal or dis‐continuous. Multiple‐response Permutations Procedures (MRPP) were also employed to test significance among the experimental factors within the datasets (McCune & Grace, 2002; Mielke, 1984). This procedure creates p‐values to determine statistical significance between groups in a system.

3  | RESULTS

3.1 | Seasonal distribution

3.1.1 | Beat trays

Trechnites insidiosus adults were first detected in late April (2018) or mid‐May (2017) with peak abundance of 0.4 per tray in late August (Figure 1). Adults of D. brevis were first detected in early April and first nymphs in late May to early June. Peak nymph abundance of 0.2 per tray was in August, and peak adult abundance of 0.09 per tray was in September 2017. In 2017, C. verbasci nymphs were first detected in late May and adults were seen one week later. In 2018, C. verbasci nymphs were detected as early as late April. Campylomma verbasci peak abundance of 0.28 per tray occurred in early May in 2018 and early August (0.26 nymphs per tray) and September (0.14

adults per tray) in 2017. In both years, earwigs were not seen until mid‐June and occurrence in beat trays was low (highest catch 0.02 per tray). In 2017, lacewing larvae were seen in late May and adults were detected three weeks later in June. Peak abundance occurred during early September for both larvae and adults. In 2018, lacewing adults were first detected in early May and larvae were seen one week later. Peak abundance of 0.05 per tray occurred in late August for adults and in early September for larvae.

3.1.2 | Traps

Trechnites insidiosus were first detected in traps in early April in 2017 and 2018 (Figure 2). Large peaks in abundance (11 and 17 mean per trap) occurred in early May in both years with a second smaller peak in late July in 2018. Adult D. brevis were first detected in traps the first week of April in 2017 and in mid‐April in 2018. Adults of D. brevis were detected all summer with a large peak in abundance in mid‐August in 2018 (0.8 mean per trap). Campylomma verbasci were collected in late May (2018) and the first week of June (2017). In 2017, a major peak in abundance occurred in mid‐June and a second, larger peak occurred in mid‐September (22.4 per trap). In 2018, C. verbasci trap lures were faulty and abundance is not reported here. Earwigs first appeared in traps in mid‐June, and abundance peaked in late July to early August. Adult C. plorabunda were first collected in traps in early April (2017)

F I G U R E 2   Mean total abundance per week of natural enemies collected in traps in pear orchards in 2017 (a) and 2018 (b). Bubble sizes are scaled for each insect. The largest bubble size for Trechnites equals 17 per trap; C. plorabunda 3.7, C. nigricornis 4.2, Earwigs 1.1, D. brevis 0.8 and C. verbasci 22.4

     |  113DuPONT aND JOHN STROHM

and mid‐April (2018). Peak abundance occurred in early July (2017) and late May (2018) with up to 3.8 per trap. Adults of C. nigricornis were col‐lected in early April (2017) and mid‐May (2018) with peak abundance in late August with up to 4.1 per trap.

3.2 | Pest management programme impacts

3.2.1 | Natural enemy counts

An analysis of variance for individual natural enemy species (adults and immatures) was performed with repeated measures for week and locationasablocking factor (Tables2‒5).Due to interactionsbetween treatment, year and week, the information presented here

is for individual years and four growing periods: pre‐bloom, bloom, early summer and summer. Species are discussed for growing peri‐ods for which no treatment by date interactions was significant.

Natural enemies were barely detectable in the pre‐bloom pe‐riod of 2017 and 2018 (Table 2 and 4). During the 2017 bloom pe‐riod, natural enemies were also barely detectable (Table 2). During the 2018 bloom, T. insidiosus wasps, D. brevis adults and C. verbasci nymphs begin to appear in organic and bIPM plots, but varied widely in abundance (Table 4). No significant treatment differences were measurable during pre‐bloom or bloom of either year (Table 2 and 4). During early summer (2018), significantly greater numbers of D. brevis adults and nymphs were found in bIPM plots relative to organic and conventional plots (Table 5; F2,10 = 4.71, p < .05). In late

TA B L E 2   Mean number of insects per tray in pear orchards during pre‐bloom and bloom periods of 2017

Pre‐Bloom April 3 to 20, 2017 Bloom April 24 to May 11, 2017

Organic bIPM Conventional Organic bIPM Conventional

T. insidiosus 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

D. brevis 0.005 ± 0 0.002 ± 0.00 0.002 ± 0.00 0.005 ± 0.00 0.002 ± 0.00 0.002 ± 0.00

Adults 0.005 ± 0 0.002 ± 0.00 0.002 ± 0.00 0.005 ± 0.00 0.002 ± 0.00 0.002 ± 0.00

Nymphs 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

C. verbasci 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Adults 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Nymphs 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Lacewing larvae 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Lacewing adults 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Earwigs 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Total natural enemies

0.008 ± 0.00 0.004 ± 0.00 0.002 ± 0.00 0.008 ± 0.00 0.004 ± 0.00 0.002 ± 0.00

Note: Species numbers include adult and nymph values.Abbreviation: bIPM, biologically based integrated pest management.

TA B L E 3   Mean number of insects per tray in pear orchards during early and late summer periods of 2017

Early summer May 15 to June 29, 2017 Late summer July 3 to September 14, 2017

Organic bIPM Conventional Organic bIPM Conventional

T. insidiosus 0.03 ± 0.02 0.02 ± 0.01 0.01 ± 0.00 0.15 ± 0.03 0.37 ± 0.09 0.01 ± 0.00

D. brevis 0.02 ± 0.01 0.02 ± 0.01 0 ± 0 0.20 ± 0.04 0.17 ± 0.04 0 ± 0

Adults 0.01 ± 0.00ab 0.02 ± 0.01a 0 ± 0b 0.03 ± 0.01 0.05 ± 0.01 0 ± 0

Nymphs 0.02 ± 0.01 0.01 ± 0.01 0 ± 0 0.17 ± 0.03 0.12 ± 0.03 0 ± 0

C. verbasci 0.04 ± 0.02 0.02 ± 0.01 0 ± 0 0.18 ± 0.04 0.42 ± 0.10 0.01 ± 0.00

Adults 0.01 ± 0.01 0.01 ± 0.01 0 ± 0 0.06 ± 0.02 0.18 ± 0.04 0 ± 0

Nymphs 0.02 ± 0.02 0 ± 0 0 ± 0 0.11 ± 0.03 0.25 ± 0.08 0 ± 0

Lacewing larvae 0 ± 0 0 ± 0 0 ± 0 0.04 ± 0.01 0.03 ± 0.01 0 ± 0

Lacewing adults 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0.01 ± 0.00 0 ± 0

Earwigs 0 ± 0 0 ± 0 0 ± 0 0.02 ± 0.00 0 ± 0 0 ± 0

Natural enemies 0.20 ± 0.03a 0.14 ± 0.03ab 0.04 ± 0.01b 0.77 ± 0.10 1.10 ± 0.21 0.05 ± 0.01

Note: Species numbers include adult and nymph values. Values within the same row labelled with different letters are significantly different according to Tukey's honest significant difference test (α = .05).Abbreviation: bIPM, biologically based integrated pest management.

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summer, higher numbers of T. insidiosus and D. brevis were found in organic and bIPM plots compared with conventional plots (Table 5; F2,10 = 4.04, p < .06, F2,10 = 6.02, p < .05). In addition, greater num‐bers of lacewing larvae were collected in organic plots relative to others in late summer (Table 5; F2,10 = 5.01, p < .05). Overall, greater numbers of natural enemies occurred in organic and bIPM plots rel‐ative to conventional plots in both early and late summer (Table 5; F2,10 = 8.19, p < .05). In 2017, trends were similar but only signifi‐cant in early summer (Table 3; F2,10 = 6.64, p < .05). Natural enemy communities were larger in organic and bio‐based IPM manage‐ment compared with very small numbers in conventional systems (Figure 3). The maximum mean per tray for treatments in 2017 was 0.1, 1.3, and 2 for conventional, organic and bIPM, respectively. In

2018, the highest means were 0.2, 0.9 and 1.5, for conventional, or‐ganic and bIPM, respectively. The maximum mean per tray occurred in late August or early September in bIPM and organic plots in 2017 and 2018. In conventional plots, it occurred in mid‐June 2017 and late July 2018 (Figure 3).

3.2.2 | Natural enemy impact score

Spray scores ranged from 27.7 to 91.7. In both 2017 and 2018, treat‐ment was a significant variable in explaining differences in spray score (F2,11 = 17.6, p < .0001). Conventional plots had higher scores with an average of 76.6 than bIPM (47.0) or Organic (45.5) plots. Scores in bIPM and organic plots were not significantly different.

TA B L E 4   Mean number of insects per tray in pear orchards during pre‐bloom and bloom periods of 2018

Pre‐bloom April 3 to 12, 2018 Bloom April 16 to May 3, 2018

Organic bIPM Conventional Organic bIPM Conventional

T. insidiosus 0 ± 0 0 ± 0 0 ± 0 0.16 ± 0.13 0.25 ± 0.17 0.01 ± 0

D. brevis 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Adults 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0.01 ± 0 0 ± 0

Nymphs 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

C. verbasci 0 ± 0 0 ± 0 0 ± 0 0.04 ± 0.03 0.05 ± 0.05 0 ± 0

Adults 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Nymphs 0 ± 0 0 ± 0 0 ± 0 0.04 ± 0.03 0.05 ± 0.05 0 ± 0

Lacewing larvae 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Lacewing adults 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Earwigs 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0 0 ± 0

Total natural enemies 0 ± 0 0 ± 0 0 ± 0 0.21 ± 0.13 0.31 ± 0.18 0.01 ± 0

Note: Species numbers include adult and nymph values.Abbreviation: bIPM, biologically based integrated pest management.

TA B L E 5   Mean number of insects per tray in pear orchards during early and late summer periods of 2018

Early summer May 7 to June 28, 2018 Late summer July 2 to September 13, 2018

Organic bIPM Conventional Organic bIPM Conventional

T. insidiosus 0.09 ± 0.03 0.12 ± 0.03 0.01 ± 0 0.07 ± 0.02a 0.38 ± 0.09b 0.01 ± 0a

D. brevis 0.03 ± 0.01ab 0.05 ± 0.01b 0 ± 0a 0.15 ± 0.03ab 0.2 ± 0.02b 0.01 ± 0.01a

Adults 0 ± 0ab 0.01 ± 0a 0 ± 0b 0.03 ± 0.01 0.04 ± 0.01 0 ± 0

Nymphs 0.03 ± 0.01ab 0.04 ± 0.01a 0 ± 0b 0.12 ± 0.02 0.16 ± 0.02 0.01 ± 0.01

C. verbasci 0.24 ± 0.08 0.14 ± 0.06 0 ± 0 0.1 ± 0.02 0.05 ± 0.01 0 ± 0

Adults 0.06 ± 0.02 0.03 ± 0.02 0 ± 0 0.02 ± 0.01 0.02 ± 0 0 ± 0

Nymphs 0.18 ± 0.08 0.11 ± 0.06 0 ± 0 0.07 ± 0.02 0.03 ± 0.01 0 ± 0

Lacewing larvae 0.01 ± 0 0 ± 0 0 ± 0 0.03 ± 0.01a 0.01 ± 0b 0 ± 0b

Lacewing adults 0 ± 0 0 ± 0 0 ± 0 0.01 ± 0 0.01 ± 0 0 ± 0

Earwigs 0.02 ± 0.01 0 ± 0 0 ± 0 0.02 ± 0.01 0 ± 0 0 ± 0

Natural enemies 0.5 ± 0.09a 0.4 ± 0.07a 0.07 ± 0.01b 0.53 ± 0.06a 0.75 ± 0.09a 0.06 ± 0.01b

Note: Species numbers include adult and nymph values. Values within the same row labelled with different letters are significantly different according to Tukey's honest significant difference test (α = .05).Abbreviation: bIPM, biologically based integrated pest management.

     |  115DuPONT aND JOHN STROHM

Negative impacts to natural enemies in conventional plots are pre‐dicted to be higher than in bIPM or Organic plots.

3.2.3 | Natural enemy community structure

An analysis of natural enemy communities collected in beat trays was conducted using non‐metric multidimensional scaling (NMS) with a user‐supplied seed of 5,002 (2017) and 2,003 (2018) (Figure 4). For 2017, NMS analysis found a successful two‐dimensional solu‐tion with final stress of 11.91 and instability of 0.0000 (Figure 4).

MRPP analysis showed that natural enemy communities in organic were significantly different than conventional (p = .021). For 2018, a successful two‐dimensional analysis had a final stress of 11.8 and instability of 0.00041. MRPP analysis showed that natural enemy communities in organic and bIPM systems were significantly differ‐ent than that of conventional (p = .00013). Vectors represent cor‐relation with the main matrix of predictive variables with R2 > .4. The greater the length of the vector the higher the R2. Score was highly correlated with conventional plot natural enemy insect communities (Figure 4).

4  | DISCUSSION

The phenology of natural enemy communities in this study closely mirrored that of past research with some interesting distinctions. Campylomma verbasci overwinter as an egg in woody host tissue with spring nymph hatch from pink to petal fall and adults appear‐ing in mid to late May (Beers et al., 1993; Horton, Miliczky, Jones, Baker, & Unruh, 2012). In our study, adults appeared generally a lit‐tle later, in early June. Low numbers of C. verbasci nymphs reported in early 2017 are most likely due to human error where scouts were not yet trained to spot tiny insects <2 mm on a beat tray. Deraeocoris brevis overwinter as adults generally laying eggs in April or May with first generation nymphs hatching 2–3 weeks later (Beers et al., 1993; Horton et al., 2012). Here, occurrence of adult D. brevis in early April with first nymphs in late May to early June and peak abundance of adults in August and September was similar to that previously reported in apple orchards in South Central Washington (Horton et al., 2012). Large populations of adult T. insidiosus found in traps during bloom (early May) and a second smaller population peak in mid‐July mirror the life history described in the literature (Beers et al., 1993; Herard, 1985). Smaller numbers during bloom on beat trays in 2017 sampling are likely a misrepresentation, also due to human error where scouts were not yet trained to spot tiny insects on a beat tray. Earwig adults lay eggs in the fall in cells in the soil. Nymphs emerge in the spring and mature in mid‐sum‐mer. In our study, older nymphs and adult earwigs were found in the tree canopy in early to mid‐June consistent with the literature (Helsen et al., 1998).

F I G U R E 3   Natural enemy abundance per beat tray in pear orchards in (a) 2017 and (b) 2018. Conventional (black), bIPM (grey), organic (white). Larger bubbles indicate higher counts. Bubble sizes are scaled based on highest weekly mean abundance from any treatment (2 natural enemies per tray—bIPM, August 2017)

F I G U R E 4   Non‐metric multidimensional scaling analysis of natural enemy community 2017 (a) and 2018 (b). Conventional (black); Organic (white); pIPM (grey). Vectors represent correlation with the main matrix of predictive variables with R2 greater than 0.4. The greater the length of the vector the higher the R2

(a) (b)

116  |     DuPONT aND JOHN STROHM

In this study, we hypothesized that pear pest management pro‐grammes with fewer broad‐spectrum materials (Organic and bIPM) would conserve natural enemies in pear orchards. Two‐year re‐sults reported here support this hypothesis, where natural enemy communities in organic and bIPM orchards generally conserved natural enemies. The 2017 community analysis found natural

enemy communities in organic significantly different than conven‐tional with some bIPM plots more similar to organic and some to conventional (Figure 4). In 2018, bIPM as well as organic natural enemy communities was significantly different than conventional (Figure 4). The total number of natural enemies was larger in organic and bIPM treatments than conventional. High natural enemy impact

TA B L E 6   p‐values of treatment, week and interaction effects 2017

Pre‐blooma Blooma Early summerb Late summerc

T W T × W T W T × W T W T × W T W T × W

T. insidiosus – – – – – – .170 .134 .915 .122 <.001 .007

D. brevis .333 .774 .512 .501 .445 .921 .052 .001 .010 .182 <.001 .227

Adults .333 .774 .512 .501 .445 .921 .046 .015 .405 .164 <.001 .047

Nymphs – – – – – – .042 <.001 .001 .177 <.001 .315

C. verbasci – – – – – – .362 .254 .379 .137 <.001 .097

Adults – – – – – – .315 .015 .142 .126 <.001 .030

Nymphs – – – – – – .408 .425 .468 .151 .002 .157

Lacewing larvae

– – – – – – .384 .049 .825 .163 .051 .263

Lacewing adults

– – – – – – .963 .008 1.000 .278 .044 .061

Earwigs – – – – – – .223 .757 .832 .081 .668 .721

Total natural enemies

.348 .290 .294 .237 .085 .943 .015 .001 .734 .077 <.001 .018

Note: T = treatment, W = week, T × W = treatment x week. Significance marked with boldface.aTreatment (T) df = 2, 10; week (W) df = 2, 32; treatment × week (T × W) df = 4, 32. bTreatment (T) df = 2, 10; week (W) df = 6, 96; treatment × week (T × W) df = 12, 96. cTreatment (T) df = 2, 10; week (W) df = 10, 160; treatment × week (T × W) df = 20, 160.

TA B L E 7   p‐values of treatment, week, and interaction effects 2018

Pre‐blooma Bloomb Early summerc Late summerd

T W T × W T W T × W T × W T W T × W T W T × W

T. insidiosus – – – .352 .093 .622 .105 .001 .016 .019 .353 .505

D. brevis .512 .420 .480 .260 .701 .493 .036 .001 .316 .052 .018 .148

adults .512 .420 .480 .260 .701 .493 .030 .372 .442 .072 .010 .740

nymphs – – – – – – .048 .001 .387 .056 .035 .092

C. verbasci – – – .512 .191 .724 .313 .031 .825 .043 .002 <.001

adults – – – – – – .264 .003 .369 .080 .045 .014

nymphs – – – .512 .191 .724 .328 .022 .766 .042 <.001 <.001

Lacewing larvae

– – – – – – .226 .110 .272 .031 .036 .476

Lacewing adults

– – – – – – .442 .784 .476 .179 .018 .030

Earwigs – – – – – – .305 .051 .114 .253 .060 .086

Total natural enemies

.512 .420 .480 .197 .028 .400 .058 .431 .782 .008 .092 .058

Note: T = treatment, W = week, T × W = treatment x week. Significance marked with boldface.aTreatment (T) df = 2, 10; Week (W) df = 1, 18; Treatment × Week (T × W) df = 2, 18. bTreatment (T) df = 2, 10; Week (W) df = 2, 35; Treatment × Week (T × W) df = 4, 35. cTreatment (T) df = 2, 10; Week (W) df = 7, 120; Treatment × Week (T × W) df = 14, 120. dTreatment (T) df = 2, 10; Week (W) df = 10, 171; Treatment × Week (T × W) df = 20, 171.

     |  117DuPONT aND JOHN STROHM

TA B L E 8   Pesticide Programmes and Natural Enemy Impact Scores 2017a

Plot Treatment Pre‐bloom spraysb Post‐bloom spraysb,c Score

7 CONV Kaolin + kaolin/sulphur/malathion/chlorpyrifos + novaluron/lambda‐cyhalothrin

Novaluron/thiamethoxam/abamectin + novaluron/spiro‐tetramat + spinetoram +thiamethoxam/Fujimite + imi‐dacloprid/spirotetramat/spirodiclofen + spinetoram/azadirachtin/cyflumetofen

85.4

14 CONV Kaolin + kaolin/chlorpyrifos/malathion/sulphur + novaluron/lambda‐cyhalothrin

Novaluron/thiamethoxam/abamectin + novaluron/spirotetramat + spinetoram +thiamethoxam/fenpyroxi‐mate + Monta/spirotetramat/spirodiclofen + spinetoram/cyflumetofen/azadirachtin

85.4

17 CONV Kaolin/sulphur/chlorpyrifos/lambda‐cyhalo‐thrin + abamectin/lambda‐cyhalothrin/novaluron

Novaluron/spirotetramat/abamectin + spirotetra‐mat/novaluron + spinetoram/etoxazole + thiameth‐oxam/fenpyroximate + spinetoram/imidacloprid/spirodiclofen + spinetoram/imidacloprid/cyflumetofen

90.9

18 CONV Novaluron/abamectin Novaluron/abamectin + novaluron/spirotetramat/etoxazole/CM granulosis virus + spinetoram/spirote‐tramat/spirodiclofen + azadirachtin +thiamethoxam/fenpyroximate + acetamiprid/imidacloprid + bifenazate +spinetoram/acetamiprid/cyflumetofen

69.9

23 CONV Kaolin + kaolin/chlorpyrifos/malathion + cal‐cium carbonate/novaluron

Calcium carbonate/novaluron/abamectin/spirotetra‐mat + calcium carbonate/novaluron/spirodiclofen/spirotetramat/clofentezine + azadirachtin/rose‐mary oil + spinetoram/thiamethoxam/hexythiazox/azadirachtin + azadirachtin/rosemary oil + imidacloprid/fenbutatin oxide/azadirachtin/rosemary oil + spinetoram/acetamiprid/cyflumetofen

85.2

26 CONV Kaolin + kaolin/chlorpyrifos + novaluron/abamectin

Calcium carbonate/novaluron/abamectin/spirote‐tramat + calcium carbonate/buprofezin/spirotetra‐mat + spinetoram/hexythiazox + thiamethoxam/acequinocyl/azadirachtin + acetamiprid/cyflumetofen

58.8

11 CONV Kaolin/chlorpyrifos/malathion + novaluron/lambda‐cyhalothrin/abamectin + novaluron/thiamethoxam/abamectin

Novaluron/spirotetramat + spinetoram +thiamethoxam/fenpyroximate + spinetoram/cyflumetofen + imidacloprid

76

12 bIPM Kaolin + pyriproxyfen/cyantraniliprole/sulphur + pyriproxyfen/cyantraniliprole

Calcium carbonate/cyantraniliprole/fenbutatin oxide + cal‐cium carbonate/cyantraniliprole + azadirachtin

34.8

20 bIPM Novaluron/abamectin Buprofezin/abamectin + buprofezin/spirotetramat/CM granulosis virus + spinetoram/spirotetramat/spi‐rodiclofen + azadirachtin +thiamethoxam/fenpyroxi‐mate + acetamiprid/imidacloprid/bifenazate + spinetoram/acetamiprid/cyflumetofen

61.9

21 bIPM Kaolin/chlorpyrifos/malathion + calcium carbonate/novaluron

Calcium carbonate/novaluron/abamectin/spirotetra‐mat + calcium carbonate/novaluron/spirodiclofen/spirotetramat/clofentezine + azadirachtin/rose‐mary oil + spinetoram/thiamethoxam/hexythiazox/azadirachtin + azadirachtin

62.5

24 bIPM Kaolin/chlorpyrifos + novaluron/abamectin Calcium carbonate/novaluron/abamectin/spirote‐tramat + calcium carbonate/buprofezin/spirote‐tramat + spinetoram/hexythiazox + acequinocyl +acetamiprid/cyflumetofen

52.7

27 bIPM Kaolin/sulphur + kaolin/sulphur Azadirachtin/Bacillus thuringiensis subsp. kurstaki + azadirachtin/CM granulosis virus + azadirachtin

31.4

8 ORG Kaolin/sulphur + kaolin/sulphur/azadirachtin Azadirachtin/Bacillus thuringiensis subsp. kurstaki + azadirachtin/CM granulosis virus + azadirachtin

33.4

10 ORG Kaolin/sulphur x2d + kaolin/calcium carbon‐ate + calcium carbonate/azadirachtin

Spinosad/azadirachtin/CM granulosis virus x3 + azadirachtin/CM granulosis virus x4 + lime sulphur

62.5

(Continues)

118  |     DuPONT aND JOHN STROHM

scores were correlated with conventionally managed natural enemy communities indicating that spray programmes were a driving factor differentiating organic and bIPM communities from conventional.

Univariate analysis also demonstrated the ability of bIPM as well as organic management to conserve natural enemies. In 2018, the total number of natural enemies was significantly greater in bIPM than conventional with numbers similar to organic in mid‐late summer (Figure 3; Table 5). In 2017, the significant differences in total natural enemy numbers were in early summer (Table 3) with organic larger than conventional and bIPM intermediate (greater than conventional at p = .065). These differences in the total natu‐ral enemy community were driven by significantly larger numbers of D. brevis and T. insidiosus in early and mid‐summer (Table 5). The replacement of broad‐spectrum insecticides with spray prod‐ucts with fewer indirect effects (insect growth regulators, sulphur, plant extract oils) pre‐bloom in bIPM and organic plots may have allowed better survivorship of these overwintering insects and thus greater abundance of subsequent summer generations. In summer, two to three applications of products like thiamethoxam, spinetoram, novaluran and spirotetramat (Actara, Delegate, Rimon and Ultor) in conventional programmes known to have significant impact on natural enemies (Mills et al., 2016) were replaced by more selective products in organic and bIPM (neem‐, petroleum‐, and plant extract‐based oils) allowing natural enemy abundance andbiologicalcontrolpotentialtogrow(Tables6‒9).

It is not surprising that bIPM programmes were able to conserve natural enemies. Burts (1983) and Alway (2002) also found that bIPM

programmes increased numbers of T. insidiosus, D. brevis and C. ver‐basci. However, the numbers of natural enemies collected in this study were much smaller for some species and greater for others. Compared with Alway (2002) T. insidiosus populations of 0.6–0.65 per tray during August were twice as high, but Alway found nearly two times the number of the D. brevis we report. In both our study and in Alway (2002), C. verbasci numbers were variable year to year. This may be due to different components used in spray programmes where Alway reported using more insect growth regulators [e.g. me‐thoxyfenozide (Intrepid) for codling moth] during summer months. Interestingly, this study found very few Anthocoris where past stud‐ies in South Central Washington found up to 1.3 per tray (Burts, 1983). The absence of Anthocoris in the Wenatchee region (and its occurrence in nearby Yakima) was noted by Horton et al. (2012) and may be caused by geographic differences. It is notable that differ‐ences were seen so quickly in this study, as early as the first year of converting to a new programme, while in past studies, two or three years were sometimes needed for natural enemy assemblages to rebound. In later years, these plots may display larger numbers of natural enemies more similar to previous studies.

Information from this study about seasonal occurrence of natural enemies could be useful to determine spray timings which balance low impact on natural enemy populations and high efficacy on pests. Pre‐bloom natural enemy abundance was very low. Potentially broad‐spectrum insecticides (organophosphates – malathion and chlorpyrifos) often used during this pre‐bloom period would have less impact on natural enemies. For example, overwintering

Plot Treatment Pre‐bloom spraysb Post‐bloom spraysb,c Score

13 ORG Kaolin + kaolin/sulphur + kaolin Azadirachtin/calcium carbonate + azadirachtin/rosemary oil + spinosad/azadirachtin/CM granulosis virus/rose‐mary oil + azadirachtin/CM granulosis virus/rosemary oil + azadirachtin/CM granulosis virus + diatomaceous earth + azadirachtin/pyrethrin

44.1

16 ORG Lime sulphur + kaolin/sulphur + kaolin/sulphur/azadirachtin

Azadirachtin/Bacillus thuringiensis subsp. kurstaki + azadirachtin/CM granulosis virus x7 + lime sulphur

54.4

22 ORG Kaolin/lime sulphur + kaolin/calcium carbonate Azadirachtin/rosemary oil + rosemary oil + azadirachtin +kaolin/azadirachtin + kaolin/azadirachtin

38.8

25 ORG Kaolin/lime sulphur + kaolin/azadirachtin Kaolin/azadirachtin + calcium carbonate/azadirachtin + spi‐nosad/azadirachtin/CM granulosis virus + calcium carbon‐ate/azadirachtin + azadirachtin/rosemary oil x4

46.5

28 ORG Lime sulphur + kaolin +azadirachtin Azadirachtin/Bacillus thuringiensis subsp. kurstaki + azadirachtin/CM granulosis virus + spinosad +azadirachtin/CM granulosis virus ×3

35.1

Abbreviations: bIPM, biologically based IPM; CONV, Conventional; ORG, organic.aProjected natural enemy impact was calculated for each spray used during the season in each plot. Individual product ratings for western predatory mites, mite predators, coccinellids, lacewings and predatory true bugs were converted to numerical ratings from low (1), low to medium (2), medium (3), medium to high (4) and high (5) given in the Washington State University Crop Protection Guide (DuPont et al., 2018). An individual product's score is the average of the rating for each of the five natural enemy types. A plot's score is the sum of the score for each spray used where higher scores equal higher natural enemy impact. bSprays included petroleum oil. cSprays included calcium chloride. d(×2, ×3, ×4, ×7) denotes the same spray used 2–7 times in a row.

TA B L E 8   (Continued)

     |  119DuPONT aND JOHN STROHM

TAB

LE 9

 Pe

stic

ide

prog

ram

mes

and

nat

ural

ene

my

impa

ct s

core

s 20

18a

Plot

Trea

tmen

tPr

e‐bl

oom

spr

aysb

Post

‐blo

om s

pray

sb,c

Scor

e

2CO

NV

Kao

lin +

kao

lin/m

alat

hion

/chl

orpy

rifos

+ k

aolin

/cal

cium

ca

rbon

ate/

acet

amip

rid/p

yrid

aben

/nov

alur

onC

alci

um c

arbo

nate

/thi

amet

hoxa

m/a

bam

ectin

/nov

alur

on +

cal

cium

car

bon‐

ate/

spiro

tetr

amat

/nov

alur

on +

spi

neto

ram

/bife

naza

te +

thia

met

hoxa

m/

abam

ectin

+ b

upro

fezi

n/sp

irodi

clof

en/s

piro

tetr

amat

+ s

pine

tora

m/

acet

amip

rid/c

yflu

met

ofen

91.7

4CO

NV

Kao

lin +

cal

cium

car

bona

te/c

hlor

pyrif

os/m

alat

hion

+ c

alci

um

carb

onat

e/no

valu

ron/

abam

ectin

Cal

cium

car

bona

te/s

piro

tetr

amat

/nov

alur

on +

cal

cium

car

bona

te/b

upro

‐fe

zin/

spiro

tetr

amat

/eto

xazo

le +

spi

neto

ram

/im

idac

lopr

id/h

exyt

hiaz

ox/

spiro

dicl

ofen

+ s

pine

tora

m/s

piro

dicl

ofen

+ b

upro

fezi

n +b

ifena

zate

66.3

7CO

NV

Kao

lin/c

alci

um c

arbo

nate

/ace

tam

iprid

/pyr

idab

en/n

oval

uron

Cal

cium

car

bona

te/t

hiam

etho

xam

/aba

mec

tin/n

oval

uron

+ c

alci

um c

arbo

n‐at

e/no

valu

ron/

spiro

tetr

amat

+ s

pine

tora

m/b

ifena

zate

+ th

iam

etho

xam

/ab

amec

tin +

bup

rofe

zin/

spiro

tetr

amat

/spi

rodi

clof

en +

spi

neto

ram

/ac

etam

iprid

/cyf

lum

etof

en

38.1

11CO

NV

Kao

lin/c

hlor

pyrif

os/m

alat

hion

+ n

oval

uron

/lam

bda‐

cy‐

halo

thrin

/aba

mec

tin +

nov

alur

on/t

hiam

etho

xam

/ab

amec

tin

Nov

alur

on/s

piro

tetr

amat

+ s

pine

tora

m +

thia

met

hoxa

m/

fenp

yrox

imat

e +

spin

etor

am/c

yflu

met

ofen

+ im

idac

lopr

id84

14CO

NV

Kao

lin +

kao

lin/m

alat

hion

/chl

orpy

rifos

+ k

aolin

/cal

cium

ca

rbon

ate/

acet

amip

rid/p

yrid

aben

/nov

alur

onC

alci

um c

arbo

nate

/thi

amet

hoxa

m/a

bam

ectin

/nov

alur

on +

cal

cium

car

bon‐

ate/

spiro

tetr

amat

/nov

alur

on +

spi

neto

ram

/bife

naza

te +

thia

met

hoxa

m/

abam

ectin

+ b

upro

fezi

n/sp

irodi

clof

en/s

piro

tetr

amat

+ s

pine

tora

m/

acet

amip

rid/c

yflu

met

ofen

91.7

17CO

NV

Kao

lin/s

ulph

ur +

kao

lin/n

oval

uron

/ace

tam

iprid

Nov

alur

on/s

piro

tetr

amat

+ n

oval

uron

/spi

rote

tram

at/s

pine

tora

m +

thia

‐m

etho

xam

/fen

pyro

xim

ate/

imid

aclo

prid

+ a

ceta

mip

rid/a

zadi

rach

tin/

spiro

dicl

ofen

+ s

pine

tora

m/c

yflu

met

ofen

/im

idac

lopr

id

73.5

20CO

NV

Kao

lin/s

ulph

ur/C

obal

t Adv

ance

d/m

alat

hion

+ a

ceta

mip

rid/

nova

luro

nC

alci

um c

arbo

nate

/spi

neto

ram

/nov

alur

on +

cal

cium

car

bona

te/s

piro

te‐

tram

at/n

oval

uron

+ s

pine

tora

m/t

hiam

etho

xam

+ c

alci

um c

arbo

nate

/sp

irote

tram

at/s

piro

dicl

ofen

+ s

pine

tora

m/i

mid

aclo

prid

/cyf

lum

etof

en

74.5

1bI

PMK

aolin

+ k

aolin

/sul

phur

/difl

uben

zuro

n +

kaol

in/c

alci

um

carb

onat

e/di

flube

nzur

onC

alci

um c

arbo

nate

/pyr

ipro

xyfe

n x2

d + c

alci

um c

arbo

nate

/aza

dira

chtin

x3

+ ro

sem

ary

oil/a

zadi

rach

tin x

245

.1

3bI

PMC

alci

um c

arbo

nate

/nov

alur

on/a

bam

ectin

Cal

cium

car

bona

te/n

oval

uron

/spi

rote

tram

at +

cal

cium

car

bona

te/

azad

irach

tin +

cal

cium

car

bona

te/a

zadi

rach

tin/s

piro

dicl

ofen

+ c

alci

um

carb

onat

e +

azad

irach

tin/s

piro

dicl

ofen

+ b

upro

fezi

n +b

ifena

zate

41.2

5bI

PMK

aolin

+ k

aolin

/sul

phur

/pyr

ipro

xyfe

n +

kaol

in/c

alci

um

carb

onat

e/py

ripro

xyfe

nC

alci

um c

arbo

nate

/aza

dira

chtin

x3

+ ca

lciu

m c

arbo

nate

+ c

alci

um c

arbo

n‐at

e/az

adira

chtin

x2

+ ro

sem

ary

oil/a

zadi

rach

tin41

.1

6bI

PMLi

me

sulp

hur +

kao

lin +

kaol

in/c

alci

um c

arbo

nate

/py

ripro

xyfe

nC

alci

um c

arbo

nate

/aza

dira

chtin

/pyr

ipro

xyfe

n +

calc

ium

car

bona

te/

azad

irach

tin x

3 +

rose

mar

y oi

l/aza

dira

chtin

+ ro

sem

ary

oil/a

zadi

rach

tin33

.4

9bI

PMK

aolin

+ k

aolin

/sul

phur

/pyr

ipro

xyfe

n +

kaol

in/c

alci

um

carb

onat

e/py

ripro

xyfe

nC

alci

um c

arbo

nate

/aza

dira

chtin

x2

+ ca

lciu

m c

arbo

nate

+ c

alci

um c

arbo

n‐at

e/az

adira

chtin

x2

+ bi

fena

zate

+ro

sem

ary

oil/a

zadi

rach

tin x

243

.5

12bI

PMK

aolin

+ k

aolin

/lim

e su

lphu

r + k

aolin

/cal

cium

car

bona

te/

pyrip

roxy

fen

Cal

cium

car

bona

te/a

zadi

rach

tin/p

yrip

roxy

fen

+ ca

lciu

m c

arbo

nate

/az

adira

chtin

x2

+ O

il x3

36.1

15bI

PMK

aolin

/sul

phur

/aza

dira

chtin

+ a

zadi

rach

tinA

zadi

rach

tin +

aza

dira

chtin

/CM

gra

nulo

sis

viru

s +

azad

irach

tin x

427

.7

(Con

tinue

s)

120  |     DuPONT aND JOHN STROHM

Plot

Trea

tmen

tPr

e‐bl

oom

spr

aysb

Post

‐blo

om s

pray

sb,c

Scor

e

18bI

PMLi

me

sulp

hur +

kao

lin +

abam

ectin

/aza

dira

chtin

Aza

dira

chtin

/Bac

illus

thur

ingi

ensis

sub

sp. k

urst

aki +

aza

dira

chtin

/CM

gr

anul

osis

viru

s +

azad

irach

tin +

azad

irach

tin +

spi

neto

ram

/thi

amet

h‐ox

am +

cal

cium

car

bona

te/s

piro

tetr

amat

/thi

amet

hoxa

m +

spi

neto

ram

/sp

irodi

clof

en +

ace

tam

iprid

/fen

pyro

xim

ate

+ sp

inet

oram

/ace

tam

iprid

/cy

flum

etof

en

70.2

8O

RGK

aolin

+ li

me

sulp

hur +

kao

lin/s

ulph

ur +

kao

lin/B

acill

us th

ur‐

ingi

ensis

sub

sp. k

urst

aki

Cal

cium

car

bona

te/a

zadi

rach

tin x

2 +

rose

mar

y oi

l/aza

dira

chtin

x2

73.8

10O

RGK

aolin

/sul

phur

+ k

aolin

/lim

e su

lphu

r + k

aolin

/cal

cium

car

‐bo

nate

+ c

alci

um c

arbo

nate

/aza

dira

chtin

Spin

osad

/aza

dira

chtin

/CM

gra

nulo

sis

viru

s x3

+ a

zadi

rach

tin/C

M g

ranu

losi

s vi

rus

x4 +

lim

e su

lphu

r47

.1

13O

RGK

aolin

/sul

phur

+ k

aolin

/sul

phur

+ k

aolin

/cal

cium

car

bona

te/

azad

irach

tinC

alci

um c

arbo

nate

/aza

dira

chtin

/Isa

ria fu

mos

oros

ea a

popk

a st

rain

97/

pyre

thrin

+ c

alci

um c

arbo

nate

/aza

dira

chtin

/Isa

ria fu

mos

oros

ea a

p‐op

ka s

trai

n 97

+ s

pino

sad/

azad

irach

tin/C

M g

ranu

losi

s vi

rus/

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TAB

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 (C

ontin

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     |  121DuPONT aND JOHN STROHM

C. verbasci reside in eggs inserted into the bark of pear trees and in extra‐orchard habitat and do not emerge until bloom timing or just after. Consequently, early sprays may not be damaging. However, the replacement of broad‐spectrum insecticides with softer spray products (insect growth regulators, sulphur plant extract oils) pre‐bloom in bIPM and organic plots may have allowed better survivor‐ship of natural enemies in overwintering sites (e.g. bark crevices) and thus greater abundance of subsequent summer generations. From bloom through early and late summer, natural enemies were active in organic and bIPM orchards, thus broad‐spectrum materials during this period will likely negate biological control potential.

Producers in Washington have dealt with difficult psylla pres‐sure and waning product effectiveness for decades (van de Baan, Croft, & Burts, 1990; Unruh, 1990; Unruh, Shearer, Hilton, & Chiu, 2015; Van de Baan & Croft, 1990). In response to extremely high pressure, conventional spray programmes have become more aggressive reducing natural enemy populations to low levels. Biological‐based IPM programmes have the potential to conserve natural enemies providing biological control in late summer when conventional sprays often fail due to pesticide resistance and in‐ability to penetrate dense canopies. This study supports the grow‐ing body of literature showing the ability of pear IPM programmes to maintain natural enemy populations. Subsequent work will de‐termine in which programmes and at what natural enemy thresh‐olds pear growers can optimize profits with unmarked fruit and low costs.

ACKNOWLEDG EMENTS

Funding for this project provided by Washington Specialty Crop Block Grant #K1986. Thank you to collaborators Elizabeth Beers and Louis Nottingham. Thank you to the fabulous orchardists who hosted field plots including: Mike George, Lone Pine Orchards; Josh Hill & Keith Goehner, K&L Orchards; Daryl & Greg Harnden, Harnden Orchards; Darrin & Ed Kenoyer, Kenoyer Orchards; Scott McManus, Yaksum Orchard; Greg & Sam Parker, Parker Orchards; Rudy Prey, Prey's Fruit Barn and Orchard; Kameron & Kerry Miller, K&K Orchards; Mike & Ray Schmitten, Schmitten Orchards; Ben & Dick Smithson, Smithson Ranch. Thank you to collaborating field staff: Bob Gix & Greg Rains, Blue Star Growers; Scott Cummings & Chuck Weaver, Chamberlin Ag; Neil Johnson, Northwest Wholesale; Mike Pflugrath & Ryan Robinson, Wilbur‐Ellis. The work could not be done without technical staff: Dylan Baty, Schaefer Buchanan, Jared Dean, and Andi Terrizas. Campylomma verbasci lures donated by G.T. Bolmfalk, Scentry Biologicals.

CONFLIC T OF INTERE S T

No conflict of interest by authors is known.

AUTHORS' CONTRIBUTIONS

STD and CJS conceived research. STD and CJS conducted ex‐periments. STD and CJS analysed data and conducted statistical

analyses. STD and CJS wrote the manuscript. STD secured funding. All authors read and approved the manuscript.

DATA AVAIL ABILIT Y S TATEMENT

Data will be deposited into the WSU data repository ‘Research Exchange’ (https ://resea rch.libra ries.wsu.edu/xmlui/ ) following pub‐lication of results.

ORCID

Sara Tianna DuPont https://orcid.org/0000‐0001‐5867‐1497

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How to cite this article: DuPont ST, John Strohm C. Integrated pest management programmes increase natural enemies of pear psylla in Central Washington pear orchards. J Appl Entomol. 2020;144:109–122. https ://doi.org/10.1111/jen.12694