Journal of Sustainable Agriculture Key and Secondary Arthropod Pest

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Key and Secondary Arthropod Pest Population Trends in Apple Cultivated over Four Seasons with No Insecticides and a Legume Cover K. Mullinixa; M. B. Ismanb; J. F. Brunnerc a Kwantlen Polytechnic University, Institute for Sustainable Horticulture, Surrey, British Columbia b University of British Columbia, Faculty of Land and Food Systems, Vancouver, British Columbia c Washington State University, Department of Entomology, Tree Fruit Research and Extension Center, Wenatchee, Washington, USA

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To cite this Article Mullinix, K. , Isman, M. B. and Brunner, J. F.(2010) 'Key and Secondary Arthropod Pest Population Trends in Apple Cultivated over Four Seasons with No Insecticides and a Legume Cover', Journal of Sustainable Agriculture, 34: 6, 584 — 594 To link to this Article: DOI: 10.1080/10440046.2010.493363 URL: http://dx.doi.org/10.1080/10440046.2010.493363

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Key and Secondary Arthropod Pest Population Trends in Apple Cultivated over Four Seasons with No Insecticides and a Legume Cover

K. MULLINIX1,M.B.ISMAN2, and J. F. BRUNNER3 1Kwantlen Polytechnic University, Institute for Sustainable Horticulture, Surrey, British Columbia 2University of British Columbia, Faculty of Land and Food Systems, Vancouver, British Columbia 3Washington State University, Department of Entomology, Tree Fruit Research and Extension Center, Wenatchee, Washington, USA

The reduced use of insecticides in apple orchards has caused many to expect secondary pests to become a serious problem. To assess the validity of this concern, we monitored arthropod populations in apple orchards cultivated with no insecticides and an alfalfa or grass cover over four seasons. Codling moths became economically injurious, while leafroller populations declined to sub-economic levels. No other species caused economic injury. Our results suggest that secondary pests may be, to some extent, pesticide induced. We did not observe any signiﬁcant effect of cover treatment on arthropod populations. However, some evidence suggests that an alfalfa cover may contribute modestly to increased biological control.

KEYWORDS apple, Malus domestica, biological control, ground

Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 cover, key pest, secondary pest, natural enemy conservation, pest management, pesticide induced

INTRODUCTION

In northwest North America, as elsewhere, apple producers generally rely on broad-spectrum insecticides for insect pest management (Hull et al. 1983; Jones et al., 2002). When broad-spectrum pesticides are used to control key pests in agro-ecosystems, previously non-pest, secondary, or occasional pest

Address correspondence to K. Mullinix, Kwantlen Polytechnic University, Institute for Sustainable Horticulture, 12666–72nd Avenue, Survey, British Columbia V3W 2M8, Canada. E-mail: [email protected]

584 Apple Pests with No Insecticides Over Four Years 585

species often become problematic as a result of the elimination or reduction of natural control agents (Beers, 1998; Carl, 1996; Luna and House, 1990; National Research Council, 1996). Flint and van den Bosch (1981) observed that the pesticide revolution “ushered in a whole new spectrum of previously unknown pests” and Croft (1982) noted that many apple pests reach seri- ously problematic levels because their natural enemies are adversely affected by pesticides. It has been shown that arthropod community dynamics in apple are dependent upon pest management regimes (Bostanian et al., 2001; Brown, 1993; Brown and Schmitt, 2001; Brown and Adler, 1989; Gut et al. 1995; Niemczyk, 1997; Polesney, 1996; Trimble and Vickers 2000; Walters, 1973). In modern apple orchard systems, the extensive use of pesticides likely influences species diversity and stability by greatly reducing the number of arthropod species and favoring species with high dispersal and rapid re- colonization capabilities as well as those tolerant or resistant to pesticides (Croft and Hull, 1983). Additionally, agroecology holds that plant diversity affects arthropod communities and densities. Increased floral diversification and vegetal archi- tectures have, in many cases, been demonstrated to reduce pest incidence by supporting populations of natural enemies or through direct deterrent effects on herbivore pests (Altieri, 1994; Andow, 1991; Bugg and Pickett, 1998). Contemporary apple agro-ecosystems, which utilize broad-spectrum pesticide regimes and eschew plant diversity may create or exacerbate arthropod pest problems. However, even in the most intensively managed agro-ecosystems biological and ecological processes remain fundamental to pest occurrence and management (National Research Council, 1996) and as such, sustained management of pests ultimately lies in ecologically and systems-based solutions (Lewis et al., 1997). The advent of pheromone based mating disruption for the management of codling moth (Cydia pomenella), the key arthropod pest of apple in the U.S. northwest, and concomitant Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 reduction in broad-spectrum insecticide application for its control, presents the opportunity to enhance biologically based pest management in northwest apple orchards. However, many growers fear severe, economically devastating pest incidence with such a regime. Maxwell (1999) suggests there are two philosophical approaches to experimentation leading to ecologically based pest management. The first assumes that through “reductionist investigation” we can develop prescrip- tive management tactics. The second relies on the study of general patterns of variations and behavior in pest populations and communities in response to manipulations. Per the latter approach, our study addressed two hypothe- ses: (1) pest populations are reduced in orchards with an alfalfa cover crop: and (2) secondary pests decline over time in the absence of broad spectrum insecticide use. 586 K. Mullinix et al.

MATERIALS AND METHODS

This study was conducted in north central Washington State over four growing seasons. Plots for this experiment were established in a 3.12-hectare block of 5th leaf, mature- bearing, Fuji (BC 2)/ M9 apple (Malus domestica Borkh). Trees were planted 1.2m x 4.0m (1,977 trees/ha), trellised and trained to a central axis. The block was divided into six contiguous half-hectare plots, configured to maximize distance between a designated 0.12 ha core sampling-area situ- ated in the center of each plot. At least 31.6 m separated each core-sampling area from adjacent ones. A randomized block design was utilized for this experiment (Davis, 2000). Experimental treatments were (1) alfalfa cover and (2) grass cover (= control). The grass cover of tall fescue (Festuca arundinnacea Schreb.) and perennial ryegrass (Lolium pereene L.) is representative of a standard cover in Washington orchards. The alfalfa (Medicago sativa L., cv. Vernal) used is a low vigor, drought tolerant cultivar. Plots were sown with their respective covers in mid-May of the initial year of the experiment. The orchard block was farmed utilizing standard practices with the exception of arthropod pest management. Pheromone-based mating disruption technique alone was used for codling moth management. Isomate-C (Pacific Biocontrol, Vancouver, WA) pheromone loaded emitters were dis- pensed in all treatment plots, per standard recommendation, at a rate of 500 emitters/ha. This was considered a low rate. Other than a single, delayed dormant superior oil application (at 11.3 l /378 l of water) no insecticide treatments were utilized in the plots for arthropod management during growing seasons. However, carbaryl (Sevin XLR) was used, per standard practice, as a fruitlet thinner, tank mixed with other non-insecticidal growth regulat- ing substances and a surfactant, in the first two experimental seasons but eliminated thereafter. Rate of carbaryl fruitlet thinner applications was 0.23 Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 or 0.5 l / 379 l water, depending on the season. Routinely used monitoring methods (Beers et al., 1993: Edwards, 1998; Swezey et al., 2000) were utilized to assess arthropod populations during the course of the experiment. The following lists arthropods monitored and reported on herein:

1. Codling moth adults and larvae, Cydia pomenella, 2. Pandemis leafroller larvae, Pandemis pyrusana 3. Aphids: green apple aphid, Aphis pomi De Geer; apple grain aphid, Rhopalosiphum ﬁtchii (Sanderson); rosy apple aphid, Dysaphis plan- taginea Passerini 4. Mullein bug, Campylomma verbasci (Meyer) 5. Lygus bug, Lygus lineolaris (Palisot de Beauvois) Apple Pests with No Insecticides Over Four Years 587

6. Stinkbugs: consperse, Euschistus conspersus Uhler; green, Acrosternum hilare (Say) 7. Western ﬂower thrips, Frankliniella occidentalis (Pergande) 8. White apple leafhopper, Tyhlocyba pomaria McAtee 9. Western tentiform leafminer, Phyllonorycter elmaella (Doglanar & Mutuura) 10. Phytophagous mites: McDaniel spider mite, Tetranychus mcdanieli McGregor; two-spotted spider mite, Tetranychus urticae Koch; and European red mite, Panonychus ulmi (Koch) 11. Predaceous mites: Typhlodromus occidentalis (Nesbitt) and Zetzellia mali (Ewing) 12. Various generalist predators and leafroller parasitoids (see results).

Each year, insect pest damage to harvested fruit was estimated by ran- domly selecting 100 cull apples from harvested fruit in each plot. Cause of damage was determined by visual inspection. All arthropod-related causes of damage for each apple were identiﬁed; as such any given apple may have exhibited multiple reasons for being deemed a cull. Analysis of Variance (ANOVA) was used to compare between treatments in single years only and are thus reported as population trends over time (Cochran, 2000).

RESULTS

Mean weekly trap catch of first and second generation adult codling moth generally increased during the study and in year four was substantially greater than in previous years. There were no significant differences, for either generation, between cover treatments in any year. Codling moth lar- val injury to fruits was greatest in year four for both covers. Comparatively, Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 in year two, no injury was detected. In years one (F = 206.15, ldf = 1, 4; p < 0.001), three (F = 34597.12; df = 1, 4; p < 0.001), and four (F = 52.20, df = 1, 4: p = 0.001), first generation codling moth fruit injury was significantly greater in the control (grass) than in the alfalfa treatment plots. Overwintered Pandemis leafroller infested only 0.43% of tight cluster flower buds in the alfalfa cover plots and 0.89% in control plots the first year. In alfalfa plots densities increased to 2.4% in year two, exploded to 42% in year three but then subsided substantially in year four to 5.4%. Population levels in the grass plots followed a very similar pattern, increasing to 0.23% in year two, 40% in year three and dropping to 4.9% in year four. There were no significant differences between cover crop treatments in years one, three, and four but year two alfalfa plot infestation level was significantly greater (F = 17.0; df = 1, 4; p = 0.014) than the grass plot level, though both were relatively low. 588 K. Mullinix et al.

Petal fall Pandemis leafroller population assessments indicated, for both treatments, the same pattern evidenced at tight-cluster. In alfalfa cover plots the rate of shoots infested per tree at the start of the study was 0.78% but rose to 19.77 % in year two, 38.77% in year three and then fell to 12.92% in year four. In grass cover plots, year one shoot infestation levels were somewhat lower, 0.33%, than in the alfalfa treatment but showed similar increase in year two, 18.77%, peaked at 57.77% in year three then declined to 11.56% in year four. In the first two years, infestation levels did not differ between cover treatments. However in year three the shoot infestation level for the grass treatment (57.77%) was significantly greater (F = 11.88; df = 1, 4; p = 0.026) than for the alfalfa treatment (38.77%). Conversely, in year four infestation levels were significantly greater for alfalfa plots than for grass plots (F = 17.56; df = 1, 4; p = 0.013). No apple grain or green apple aphids were detected in the final year (four) of the study but the penultimate year had the highest number of colonized shoots when alfalfa plots averaged 23.93 colonized shoots and grass plots averaged 13.93 colonized shoots. In no year did infestation levels differ significantly between treatments. Rosy apple aphid infestations were greatest the final year of the study with 9.56 colonies per grass plot and 7.89 per alfalfa plot. Infestation levels, between cover treatments, were not significantly different from one another in any year. Aphid predators observed (data not shown) included ladybird beetles and their larvae, (Hippodamia convergens Guein-Meneville or Coccinella transversoguttata richardsoni Brown); green lacewing adults and larvae, Chrysoperla carnea (Stephens) or C. nigricornis Burmeister; Deraeocoris brevis piceatus (Knight); damsel bug, Nabis spp.; syrphid fly larvae, Scaeva pyrastri (Linneaus) or Eupeodes volucris Osten Sacken; predaceous midge, Aphidoletes aphidimyza; minute pirate bug, Anthocoris spp. or Orius spp.; and spiders (Araneae). Ladybird beetles and their larvae were observed in the greatest quantities and were most abundant the last year of the study. Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 Green lacewing adults and their predaceous larvae were also frequently found in aphid colonies. Lacewing larvae were only observed in the last 2 years, while adults were observed in all years. Lacewing eggs were frequently observed the last two years as well. Likewise spiders were observed in association with aphids in years three and four only; none were present in year two. Syrphid fly and minute pirate bug were noted only in years three and four. Finally predaceous midges were relatively abundant in the final year (four) of the study after only a very few were observed the year before and none the first two years. European red mite, McDaniel spider mite, two spotted spider mite and apple rust mite populations all declined over the course of the study in both cover treatments. In no year of the study was there a significant difference in population levels of any of these phytophagous mites between cover Apple Pests with No Insecticides Over Four Years 589

crop treatments. Predator mite, Zetzellia mali (Ewing) and Galadromus occidentalis Koch, populations were also greatest in the first year of the study for both cover treatments but there were no differences between treatments. Likewise there were no differences in populations of predatory mites between cover for the last three years of the study. Lygus bug counts were, overall, highest in alfalfa plots and increased in each successive year of the experiment. In year four, alfalfa plot lygus bug beating tray counts were significantly greater (F = 4.77; df = 1, 22; p = 0.039) than for the grass treatments. In the previous 3 years, there were no significant differences between cover treatments. Mullein bug populations were highest, for both treatments, in year two of the study. In year four mullein bug populations in the alfalfa plots were not appreciably greater than year one populations and in no year did populations differ significantly between cover treatments. Stinkbugs were all but absent in the spring for both cover crop treatments in all years of the study. In no year were populations significantly greater in either cover crop treatment. However, stinkbug injury was evident at harvest (Table 1). Populations of western flower thrips vacillated greatly between cover crop type and years, throughout the study. The greatest population levels, for both treatments, occurred in the first year and in the final year (four). Alfalfa plot populations were significantly greater than in control (grass) plots in year one (F = 28.32; df = 1, 16; p < 0.001) but in subsequent years there were no significant differences between treatments. White apple leafhopper nymph densities were greatest in year two for both treatments, 1.1/leaf for alfalfa plots and 1.0/leaf for grass plots, but did not differ significantly. Only in year one were alfalfa plot populations significantly greater than in grass plots (F = 8.05; df = 1,358; p = 0.004). In other years and for both treatments, densities ranged from 0.3 to 0.68 nymphs per leaf but did not differ significantly from one another. Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010

TABLE 1 Estimated Percent of Cull Fruit with Arthropod Pest Injury in Alfalfa and Grass ∗ Cover Crop Plots, by Year

Alfalfa cover Grass cover

Species 1999 2000 2001 2002 1999 2000 2001 2002

Codling moth 1.0 0.0 4.7 9.0 1.0 0.0 7.0 11.0 Leafroller 12.0 33.0 17.0 7.0 15.0 37.0 15.3 7.6 Lygus bug 0.0 0.0 2.0 2.3 2.0 0.0 3.0 1.3 Stinkbug 23.0 14.0 2.0 1.0 12.0 10.0 1,0 0.6 ∗ Estimates based on damage to harvested fruit in bins. Field sorting of culls during harvest was performed. Cullage not necessarily exclusively from injury caused by a single pest. No damage was attributed to aphids, mullein bugs or thrips in either treatment or in any year. 590 K. Mullinix et al.

The greatest western tentiform leafminer populations occurred in year two. Alfalfa treatment plots had an average of 0.09 mines/ leaf, while grass had an average 0.1 mines/ leaf. Infestation levels did not differ signiﬁcantly between treatments. In the last 2 years, none were found in either treatment. Only codling moth, leafroller, lygus bug and stinkbug damage to harvested fruit was evident (Table 1). Codling moth injury increased each year commensurate with population. Leafroller cullage was greatest in year two, while year four damage was less than that observed in year one. Stinkbug fruit injury was greatest years one and two and substantially less in the last 2 years. By the end of the experiment only codling moth injury was economically important.

DISCUSSION

Leafrollers are the secondary pest most feared by growers to become problematic in a reduced broad-spectrum pesticide regime in northwest North American apple orchards (Knight, 2001). In our study populations became alarmingly prevalent but in year four declined to non-economically injurious levels. A granulovirus (GV) was likely responsible for the decline in leafroller populations (Lacey et al., 2001; Pfannenstiel et al., 2004). Confirmation that Pandemis leafroller larvae were infected with this virus was made via evaluation of symptoms (Lacey, personal communication, 2002). This pathogen may become an important management tool in an ecologically based Pandemis leafroller management regime. Leafroller parasitism rates were low to moderate throughout our study (data not reported) but did contribute to leafroller mortality. However, data suggest that the alfalfa cover may have modestly encouraged leafroller parasitoid activity. Additionally, generalist predators may have contributed to leafroller Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 biological control in test plots (Bostanian et al., 1984). Anecdotal evidence indicated that spiders (Araneae) and earwigs, Forficula auricularia (Linnaeus) became increasingly prevalent. In year four they became particularly abundant and were commonly found in leafroller retreats. They were also increasingly detected in spring limb taps. Identification, quan- tification and investigation into the potential for spiders (Bostanian, 2001), earwigs and other generalist predators to contribute to biological control of leafrollers (as well as other arthropod pests of apple) is warranted. Mullein bug populations vary from season to season in convention- ally managed orchards. As such the variation in population levels in our experimental plots were not unusual. In addition to feeding on fruitlets in the spring, mullein plant bug is also a predator of soft-bodied insects so elevated populations may contribute to biological control of other species (Beers et al., 1993). Apple Pests with No Insecticides Over Four Years 591

Stinkbugs were not detected in the spring but stinkbug damage was evident at harvest suggesting that they likely immigrated later in the summer as native vegetation desiccated (Beers et al., 1993). Lygus bug is of particular concern with the use of alfalfa as an orchard cover. Alfalfa, a preferred host plant of this insect, can support large populations with the potential to move into apple trees, particularly after mowing (Beers et al., 1993). Despite higher lygus bug populations in alfalfa cover plots no fruit injury was detected (Table 1). Alternate row mowing, separated by a week or more, may have discouraged their movement from the alfalfa cover to tree canopies and may be an important lygus bug management tool when alfalfa is planted as an orchard cover. It appears that generalist predator populations increased, in both cover treatments, in the absence of broad-spectrum insecticides during the course of this study and were most prevalent the final year. Additionally, the composition of the generalist predator community changed over the course of this study. Although most generalist predator populations did not differ between covers treatments (with the exception of ladybird beetle and lacewing), it is noteworthy that all species, except Deraeocoris, were numerically more abundant in alfalfa cover plots in the final study year. Codling moth populations become excessive by year four, causing unacceptable economic injury (Table 1). Fruit injury estimates would have been much greater had damaged fruit not been removed during the growing season in an effort to limit escalating populations. This was the first time mating disruption as a standalone measure failed to adequately control codling moth in this orchard. We attribute this to several factors. First, a low rate (500 Isomate C-plus dispensers per hectare) of pheromone treatment was used and placement may not have been optimal. Most importantly, external pest pressure increased substantially during our study because surrounding area orchards were not managed for codling moth as intensively or aggressively as usual. Many orchards were abandoned and left without adequate codling Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 moth management. Also, an apple-packing facility began stockpiling large quantities of storage bins, a verified source of mated female codling moth, very nearby. Thus it is nearly certain that local codling moth populations built up over the years of the study as a result of these external pressures.

CONCLUSION

With the exception of codling moth and possibly leafroller in years two and three, none of the arthropod species generally considered potential pests of apple caused what could be considered economic damage to fruit in the absence of insecticides.This suggests that many secondary insect and mite pests may be primarily pesticide-induced and biological controls, if not disrupted, may be sufficient to consistently maintain their populations below economically damaging levels. Alfalfa, as a cover crop, had only a modest influence on pest populations and this was seldom statistically significant. 592 K. Mullinix et al.

Leafroller populations did increase in year three causing concern, but in year four diminished to non-economic levels suggesting that routine pesticide intervention for leafroller management may not be required. Mortality factors lagged behind leafroller population growth in our study; as such some economic injury may occur before biological control takes effect. Approaches to minimize leafroller economic injury while not curtailing the development of biological control should be explored, or perhaps a longer-term economic time frame is appropriate. Generalist predator populations increased somewhat during the 4-year study, but cover crop manipulation did not appreciably influence this change. Additionally, the composition of the generalist predator community changed over the course of this study. Lygus bug, of particular concern with the use of alfalfa as a cover did not achieve pest status though populations in alfalfa plots did increase. Alternate row mowing may be an important lygus bug management tool when alfalfa is planted as part of the orchard cover to supply nitrogen and offer refugia and food for beneficial arthropod species. Substantially more aggressive management of codling moth was called for in this regime, including possibly, as suggested by Lewis et al. (1997), the last resort back-up use of insecticides. The challenge will be to design an integrated management strategy for codling moth that will not disrupt the biological control of the myriad secondary pest species that may not be problematic in the absence of pesticides. Our findings provide modest evidence that a flowering broadleaf cover, such as alfalfa, may contribute to natural biocontrol. Continued investigation of this and other methods for the management of codling moth is warranted. Anecdotally, we can report that under the same management regime, leafroller populations remained at sub-economic levels for an additional 3 post-experimental years as did other secondary pest species. Codling moth populations were ultimately brought under control using a combination of mating disruption, sanitation and codling moth granulovirus (Cyd-X, Certis Downloaded By: [Mullinix, K.] At: 20:24 13 August 2010 USA, Columbia, MD) application. The results of our study are sufficiently encouraging to warrant further investigation, on a larger scale and in diverse locations, with the objective of verifying results and evoking an ecologically based pest management regime in apple orchards.

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