Diptera: Tephritidae)

HORTICULTURAL ENTOMOLOGY Effect of Surround WP on Behavior and Mortality of Apple Maggot (Diptera: Tephritidae)

1,2 1 1 3 TRACY C. LESKEY, STARKER E. WRIGHT, D. MICHAEL GLENN, AND GARY J. PUTERKA

J. Econ. Entomol. 103(2): 394Ð401 (2010); DOI: 10.1603/EC09131 ABSTRACT Apple maggot, Rhagoletis pomonella (Walsh) (Diptera: Tephritidae), is a key pest in apple (Malus spp.) production areas located in the northeastern and midwestern United States and the eastern provinces of Canada. The development of Surround WP has offered a new approach for controlling apple maggot and other tephritid species, because this material is considered to be compatible with advanced integrated pest management and organic production systems. We conducted studies aimed at identifying the behavioral and biological effects of this material on apple maggots. SpeciÞcally, we examined the effect of Surround WP on the visual ecology of adult ßies under Þeld conditions, on tactile responses of ßies in semiÞeld trials, and on ßy mortality in laboratory- based-bioassays. We demonstrated that an even coating of white particles over a fruit-mimicking sphere surface reduced visual attractiveness. We also found that spotty-coated fruit-mimicking spheres (meant to mimic ripe fruit bearing an uneven coating of Surround WP) were perceived by ßies as not having the ideal round silhouette shape stimulus. Surround WP served as a tactile deterrent; the residence time of females introduced on to treated fruit was much shorter compared with untreated fruit. Surround WP also had a toxic effect on both adult apple maggot and Rhagoletis suavis (Loew); ßies exposed to and forced to stand on Surround-treated surfaces died in Ͻ2 d in all trials. The combined effectiveness of Surround WP is based on a reduction in the attractiveness of fruit-based visual cues, an increase in the likelihood of ßies leaving treated surfaces due to tactile deterrence, and a potential for increased mortality due to exposure to Surround WP particles.

KEY WORDS Surround WP, kaolin, particle Þlm technology, apple maggot, behavior

The apple maggot, Rhagoletis pomonella (Walsh) Apple maggot is a key pest in apple production in (Diptera: Tephritidae), is a native species originally the northeastern and midwestern United States as well found throughout eastern North America that bred as eastern Canada (Agnello et al. 2006). If no control principally in native hawthorn (Crataegus spp.). Later, measures are used, damage can be severe; samples it expanded its host range to include apple (Malus from unmanaged trees in New England taken over 25 spp.) with reports of economic damage to New En- yr revealed an average of 91% fruit damage (Prokopy gland apple crops as early as the 1860s (Walsh 1867). 2003). Growers typically apply an average of three The geographic range occupied by this pest has ex- insecticide applications to the entire apple orchard panded, and it is now found in all apple-growing re- (Prokopy et al. 1990) and historically have relied on gions throughout the United States (Ali Niazee 1988). organophosphates such as azinphosmethyl and phos- Recently, a model designed to simulate the potential met. However, the review of tolerances for organo- economic impact of apple maggot in Washington state, phosphates under the 1996 Food Quality Protection the largest apple producer in the United States, pre- Act has resulted in cancellations or increased restric- dicted that this insect will spread throughout all apple- tions on the use of these materials. These regulatory growing regions of the state within the next several changes have led to studies that identiÞed several decades, highlighting the importance of development effective “reduced-risk” insecticides labeled for use and implementation of mitigation procedures (Zhao against apple maggot on apple (Reissig 2003). et al. 2007). For organic production systems, the options for effectively controlling apple maggot are far more lim- ited, rendering commercially viable organic production much more difÞcult to achieve. In the past de- Mention of trade names or commercial products in this publication is solely for the purpose of providing speciÞc information and does not cade, the development of Surround WP from kaolin imply recommendation or endorsement by the U.S. Department of clay (aluminum silicate hydroxide) and referred to as Agriculture. “particle Þlm technology” (Glenn et al. 1999), has 1 USDAÐARS, Appalachian Fruit Research Station, 2217 Wiltshire offered a new approach for controlling fruit-feeding Rd., Kearneysville, WV 25430-2771. 2 Corresponding author, e-mail: [email protected]. pests (Glenn et al. 1999; Knight et al. 2000; Unruh et 3 USDAÐARS, 1301 N Western Rd., Stillwater, OK 74075-2714. al. 2000; Puterka et al. 2000, 2005). However, the mech- April 2010 LESKEY ET AL.: BEHAVIOR AND MORTALITY OF THE APPLE MAGGOT 395 anism of action of this material is based on creating a variation associated with olfactory and visual stimuli kaolin-based particle barrier on the plant surface, so provided by the presence and abundance of ripening understanding how it affects the behavior and biology apples. After removal of fruit, the canopy of three trees of the targeted pest is important in developing an per row was treated every 2 wk with 3% Surround WP effective deployment strategy for this material. Pur- (SWP) (25 lb SWP/100 gal water) by using an orchard ported mechanisms of action against targeted insect blast sprayer (1.5 mph and 100 psi) from 12 July to 29 pests have included repellency, tactile or visual cue September. The remaining three trees per row were interference, impairment or disruption of oviposition used as untreated test trees. and feeding activity, and decreased longevity and sur- Apple maggots respond optimally to fruit-mimick- vivorship (Glenn and Puterka 2005, Bostanian and ing visual stimuli provided by dark red or black, 7.5Ð Racette 2008). 9.0-cm spheres (Prokopy 1968), so manipulating the Among tephritid species, several mechanisms have stimulus to resemble the appearance of apples coated been reported. For example, the Western cherry fruit with Surround WP should allow us to quantify the ßy, Rhagoletis indifferens Curran, oviposited signiÞ- impact of this particle Þlm coating on visual response cantly fewer eggs in cherries treated with Surround of apple maggots. Using 9-cm reusable plastic sphere WP compared with untreated cherries in choice and traps (Great Lakes IPM, Vestaburg, MI), we con- no-choice assays (Yee 2008). Studies of the foraging structed the following visual-sphere treatments: 1) red behavior of blueberry maggot, Rhagoletis mendax Cur- spheres (optimal visual stimulus for apple maggots); ran, females exposed to Surround-treated and un- 2) white spheres (suboptimal visual stimulus designed treated blueberries revealed that females spent sig- to mimic ripening apples fully coated with Surround niÞcantly less time walking on blueberries coated with WP); or 3) red spheres randomly splattered on the Surround WP and oviposited signiÞcantly less fre- surface with white paint (suboptimal visual stimulus quently indicating that Surround particles either hin- designed to mimic ripening apples covered with a dered perception of host speciÞc stimuli (Lemoyne et spotty coating of Surround WP). Within each treated al. 2008) or served as a tactile deterrent to females and untreated tree canopy, two spheres of the same forced to stand on Surround-treated surfaces. Villan- visual treatment were deployed on opposing sides of ueva and Walgenbach (2007) evaluated the effect of the tree canopy, and all spheres were coated with a Surround WP on apple maggot populations in apple thin layer of Tangletrap. All test trees were baited with orchards in North Carolina and reported that the per- a 2-ml vial of Þve-component apple volatile lure blend centage of infested fruit in plots protected by Sur- (Zhang et al. 1999) to reduce variation in numbers of round was equivalent to plots treated with azinphos- responding ßies by providing equivalent release rates methyl or spinosad, indicating that oviposition was of attractive olfactory stimuli. When Surround WP interrupted in some way. They also observed that was being applied to test tree canopies, spheres and fewer adults alighted on Surround-treated foliage and apple volatile lures were covered with plastic bags. fruit under Þeld conditions, presumably because the Beginning 21 July, all spheres were checked weekly white coating provided by Surround interfered with for adult apple maggots; the number of ßies captured visual cues used by ßies to locate host trees and fruit. on each sphere treatment and the sex of each ßy was Here, we report the results of studies designed to recorded. Data were square-root transformed to ho- elucidate potential behavioral and biological effects of mogenize the variance. The mean number of apple Surround WP on adult apple maggot to develop a maggots captured per treatment throughout the test rational deployment strategy for this material. Specif- period was compared using a one-way analysis of vari- ically, we examined the effect of Surround WP on the ance (ANOVA) followed by TukeyÕs honestly signif- visual ecology of adult ßies under Þeld conditions, on icant difference (HSD) test (P Ͻ 0.05; SAS Institute tactile responses of ßies in laboratory trials, and on ßy 2003). mortality in laboratory-based bioassays. For ßy mor- Tactile Effects. Direct observations of female apple tality trials, we also evaluated congeneric Rhagoletis maggot behavior were conducted in the laboratory to suavis (Loew) to determine whether ßy mortality evaluate the tactile response to Surround WP. Apple from exposure to Surround WP particles was similar maggot pupae, obtained from infested apples in the for closely related species. Þeld (Roitberg et al. 1982) were stored in a refriger- ator at Ϸ3ЊC until needed. Pupae (200 per group) were placed in a small incubator at 25ЊC and upon Materials and Methods emergence (4Ð5 wk), ßies were placed in 30-cm3 Visual Effects. A 2-ha apple orchard located at the Plexiglas cages with water, sugar, and a protein source Appalachian Fruit Research Station (Kearneysville, consisting of enzymatic yeast hydrolysate. Flies re- WV) planted in 1998 and consisting of ÔSun FujiÕ and mained in cages for 14Ð21 d to ensure sexual maturity ÔCrimson GalaÕ on M.9 rootstock was used for this before being assayed. study from July to September 2004. Throughout the Fruit used for these trials included ÔFujiÕ apples season, the orchard was treated with conventional harvested from experimental orchards at the Appala- fungicides and herbicides, but no insecticides. In early chian Fruit Research Station, Kearneysville, WV, and July, six trees per row in 10 rows were designated as mature hawthorn collected from the University of test trees for subsequent treatment regimes. All fruit Massachusetts, Amherst, MA, campus that had been were removed from these trees to eliminate sources of protected from oviposition by wild females by bagging 396 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 2 fruiting limbs in late June. Fruit were treated with 3 or Ϸ50% RH. In total, 30 ßies of each species (15 male/15 6% Surround WP formulations to yield either spotty female) were exposed to each treatment. Fly condi- coverage by using a trigger bottle or full coverage by tion (alive, moribund, or dead) and position (dish or dipping fruit in the formulation. Control fruit were refuge) were assessed daily for 20 consecutive days. sprayed with water. Fruit were then placed in a fume For each trial, data were analyzed using the GLM hood to dry before bioassay. procedure (SAS Institute 2003) to construct ANOVA A female ßy was introduced directly onto the sur- tables for mean survivorship after exposure to 1.5, 3.0, face of a fruit using a probe Þtted with a strip of Þlter and 6.0% Surround WP treatments or to a water- paper dipped in 20% sucrose solution and was per- treated control. Dependent variable data were subject mitted to settle on the fruit for 20 s. If the ßy left the to a square-root transformation if homogeneity of vari- fruit in Ͻ20 s, it was returned to the fruit immediately. ance assumptions were violated according to LeveneÕs If the ßy rejected the fruit two more times (remaining test for Homogeneity (SAS Institute 2003). Each on the fruit for Ͻ20 s), the ßy was considered as unÞt model evaluated the effect of Surround treatment and for testing and the trial was discarded (Papaj and sex. If the effect of sex or treatment was not signiÞcant, Prokopy 1988, Roitberg 1989, Barry et al. 2004). Upon it was dropped from the model. When the GLM in- settling, each tested female was observed continu- dicated signiÞcant differences, multiple comparisons ously for up to 10 min. For each trial, the total resi- were calculated using TukeyÕs HSD test (P Ͻ 0.05). dence time spent on the fruit, time spent foraging (including walking, feeding, and ovipositing), and the Results time spent grooming were recorded. Values were compared among untreated fruit and fruit coated with Visual Effects. The number of adult apple maggots full or spotty 3% or 6% SWP treatments for hawthorn captured per treatment was signiÞcantly different and apple using a one-way ANOVA followed by (F ϭ 50.62; df ϭ 5, 54; P Ͻ 0.001), with more ßies TukeyÕs HSD (P Ͻ 0.05). Percentage data were sub- captured on red spheres deployed in untreated can- jected to an arcsine square-root transformation. Other opies compared with any other treatment, followed by data were not transformed as they met the homoge- red spheres deployed in treated canopies, which was neity of variance assumptions according to LeveneÕs signiÞcantly greater than white or spotty spheres de- test (SAS Institute 2003). ployed in treated or untreated canopies. The lowest Mortality. To examine the impact of exposure to captures were recorded on spotty spheres deployed in Surround particles on ßy survivorship, individuals treated canopies (Fig. 1). Throughout the season, sig- were placed in single-ßy containers [100- by 15-mm niÞcantly more ßies were captured on red spheres petri dishes, with all interior surfaces uniformly coated deployed in untreated canopies compared with any with a 0.25-mm-thick layer of molten wax (TissuePrep other treatment with the exception of the last two 2, Fisher, Fair Lawn, NJ) to approximate the waxy sample dates in which very few ßies were captured cuticle of fruit and foliage] treated with water (con- (Fig. 2). trol) or 1.5, 3.0, or 6.0% Surround WP by using a Tactile Effects. Hawthorn. There were signiÞcant high-volume, low-pressure, air-driven siphon-canister differences among treatments in total residence time paint spray gun (Sharpe Manufacturing Co., Minne- on fruit (F ϭ 6.21; df ϭ 4, 91; P Ͻ 0.001), time spent apolis, MN). All interior surfaces of dishes received a resting on fruit (F ϭ 4.17; df ϭ 4, 91; P ϭ 0.004), and single application (to drip) of test solutions and were foraging activity (F ϭ 7.53; df ϭ 4, 91; P Ͻ 0.001), with allowed to evaporate completely before test ßies were shortest total residence time and shortest time spent placed in dishes. resting or foraging on hawthorns treated with 6% Sur- For trials of apple maggot, dishes were provisioned round WP (Table 1). There also were signiÞcant dif- with either 1) no resources, 2) 50 ␮l of water (water ferences in proportional time spent grooming on fruit resource only), 3) 100 ␮l water (water resource only), among treatments (F ϭ 5.66; df ϭ 4, 91; P Ͻ 0.001), 4) 100 ␮l of 20% aqueous sucrose solution (water and with signiÞcantly less time spent grooming on un- food resources), or 5) 1 ml of 20% aqueous sucrose treated fruit compared with all SWP treatments (Ta- solution dispensed onto cotton wick (water and food ble 1). In total, 13 ßies oviposited in untreated fruit resources) that also provided an untreated refuge on compared with three and zero for 3% and 6% full SWP which ßies could stand and avoid exposure to treated treatments, respectively, and seven and three for 3 and surfaces. 6% spotty SWP treatments. R. suavis were obtained from infested walnuts col- Apple. Differences in total residence time (F ϭ lected in the Þeld at the University of Massachusetts 2.43; df ϭ 4, 95; P ϭ 0.0528) and time spent resting on at Amherst and treated in the same manner as de- apple (F ϭ 1.64; df ϭ 4, 95; P ϭ 0.170) were not scribed above. For trials with R. suavis, dishes were signiÞcantly different among treatments although fe- provisioned with either 1) no resources, 2) 50 ␮lof males exposed to 6% SWP treatments had shortest water (water resource only), or 3) 1 ml of 20% aqueous residence times and spent less time resting compared sucrose solution dispensed onto cotton wick (water with all other treatments (Table 2). Foraging activity and food resources with untreated refuge). was signiÞcantly different among treatments (F ϭ Individual ßies were transferred from Plexiglas 2.49; df ϭ 4, 95; P ϭ 0.0481), with signiÞcantly less time cages to treated dishes, and dishes were held in a spent foraging on the 6% full SWP treatment com- greenhouse under Þltered natural light at 25ЊC and pared with 3% spotty SWP treated fruit (Table 2). April 2010 LESKEY ET AL.: BEHAVIOR AND MORTALITY OF THE APPLE MAGGOT 397

120

a 100

60 b

Mean No. Per Treatment Mean No. Per c 20 cd cd d

0 Red + Red + White + White + Spotty + Spotty + Untreated Treated Untreated Treated Untreated Treated Canopy Canopy Canopy Canopy Canopy Canopy Fig. 1. Mean number apple maggot Ϯ SE captured on red, white, or spotty sticky-coated spheres deployed in apple tree canopies treated with Surround WP or left untreated from 12 July to 29 September 2004.

There were no signiÞcant differences in proportional were signiÞcant differences among treatments (F ϭ time spent grooming on fruit among treatments (F ϭ 157.38; df ϭ 3, 156; P Ͻ 0.001), with ßies in the un- 076; df ϭ 4, 95; P ϭ 0.554). treated control surviving signiÞcantly longer than Mortality. Apple Maggot. When ßies were not pro- adults exposed to Surround WP treatments. vided with any resources (food or water), they died When adults were provided with 20% sucrose so- very quickly in all treatments (Table 3). Because there lution presented as a refuge there were still signiÞcant was no effect of Surround treatment, the term was differences among treatments (F ϭ 35.30; df ϭ 3, 116; removed from the model. However, the effect of sex P Ͻ 0.001); survivorship increased to 80% in the un- was signiÞcant (F ϭ 9.58; df ϭ 1, 158; P ϭ 0.002) and treated control, but was only 43.3, 23.3, and 6.7% in the female ßies (0.91 d Ϯ 0.07 SE) lived signiÞcantly 1.5, 3.0, and 6.0% in Surround WP treatments, respec- longer than male ßies (0.62 d Ϯ 0.06, mean Ϯ SE). For tively (Table 3). ßies provided with 50 ␮l of water, 100 ␮l of water, or R. suavis. When no resources were provided, ßies 20% sucrose solution, the effect of sex was not signif- died very quickly with average survivorship being less icant and was removed from the models. There were than one day for all treatments (Table 4). Unlike apple signiÞcant differences in survivorship among treat- maggot, the effect of sex was not signiÞcant and it was ments for ßies provided with 50 ␮l(F ϭ 16.58; df ϭ 3, removed from the model. However, the effect of treat- 156; P Ͻ 0.001) and 100 ␮l of water (F ϭ 15.51; df ϭ ment was signiÞcant (F ϭ 3.02; df ϭ 1, 156; P ϭ 0.0317), 3, 156; P Ͻ 0.001). In both trials, ßies survived signif- with ßies in untreated dishes living signiÞcantly longer icantly longer in the untreated control compared with than those exposed to dishes treated with 1.5% SWP all Surround WP treatments (Table 3). When ßies (Table 4). For adults provided with 50 ␮l of water, the were provided with a 20% sucrose solution, there still effect of sex was not signiÞcant and was removed from

5 Mean No. Flies Per Trap Mean No. Flies Per

0 21-J 2 4- 11-Aug 18-A 25-Aug 1 8- 15-Sep 2 29-Sep 8-Ju Au -Sep Sep 2-Sep u u l l g g

Sample Date

Red + Untreated Canopy Red + Treated Canopy White + Untreated Canopy White + Treated Canopy Spotty + Untreated Canopy Spotty + Treated Canopy Fig. 2. Mean number of apple maggot Ϯ SE captured per sphere on each sample date throughout the trapping period. 398 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 2

Table 1. Mean total residence time, time spent resting, time spent foraging and time spent grooming by female apple maggot introduced onto untreated hawthorns or onto hawthorns treated with 3 or 6% spotty or full SWP treatments

Total residence time Resting Foraging Time spent grooming Treatment (mean s Ϯ SE) (mean s Ϯ SE) (mean s Ϯ SE) (mean % Ϯ SE) Untreated 495.3 Ϯ 43.3a 348.2 Ϯ 41.8a 229.2 Ϯ 36.3a 2.1 Ϯ 0.3b 3% Spotty 346.3 Ϯ 55.0ab 216.6 Ϯ 48.7ab 166.7 Ϯ 38.2ab 34.0 Ϯ 8.6a 6% Spotty 291.4 Ϯ 57.0b 217.9 Ϯ 53.6ab 90.9 Ϯ 27.7b 34.2 Ϯ 7.1a 3% Full 164.9 Ϯ 39.2b 103.0 Ϯ 34.7b 63.4 Ϯ 8.7b 26.1 Ϯ 4.2a 6% Full 244.4 Ϯ 57.1b 158.0 Ϯ 47.4b 52.5 Ϯ 11.5b 33.5 Ϯ 6.5a

Values followed by different letters within the same column are signiÞcantly different according to TukeyÕs HSD test (P Ͻ 0.05). the model. There were signiÞcant differences among spheres. Contrast of the darkly colored red sphere treatments (F ϭ 28.32; df ϭ 3, 156; P Ͻ 0.001), with ßies with the surrounding background is an essential com- in the untreated control living signiÞcantly longer ponent of the visual stimulus for foraging apple mag- compared with any SWP treatment. When ßies were got. Adult ßies are able to detect the round silhouette provided with 20% sucrose solution presented as a of a dark sphere reßecting low light intensity more refuge, survivorship increased to 86.7% in the un- readily when viewed against a more brightly lit con- treated control and 26.7, 16.7, and 13.3% in the 1.5, 3.0, trasting background (Prokopy 1968, 1973; Owens and and 6.0% Surround WP treatments, respectively. In Prokopy 1984). In the case of spotty-coated spheres this case, the effect of sex (P ϭ 0.033) and treatment (meant to mimic ripe apples bearing an uneven, spotty (P Ͻ 0.001) were signiÞcant (F ϭ 22.00; df ϭ 4, 115; P Ͻ coating of Surround WP), foraging ßies probably per- 0.001). Male ßies survived signiÞcantly longer (10.72 ceived them as not having the ideal round shape sil- d Ϯ 0.37) than female ßies (9.80 d Ϯ 0.41), and ßies in houette stimulus due to the uneven coloration and untreated controls lived signiÞcantly longer compared reßective light intensity of the sphere surface. When with those exposed to SWP treatments (Table 4). these spotty-coated spheres were deployed within Surround-treated canopies, ßy response decreased even further. Based on spectrophotometer and spec- Discussion trometer studies, the white portions of the sphere Once an apple maggot reaches a host tree, it be- surface (Owens and Prokopy 1984) and the Surround- comes a visual specialist within the canopy foraging for treated foliage (Glenn et al. 2002, 2005) reßect more host fruit (Prokopy and Owens 1978). Shape, size, and light than the darker portions of the red sphere sur- color of the host fruit are key visual cues used by adult face, contributing to the disruption of the contrast of ßies and were identiÞed and used to create a super- the sphere shape stimulus against the background, normal visual stimulus for foraging ßies: a red, round, essentially camoußaging the sphere within the tree 7.5Ð9.0-cm-diameter sphere that is visually more at- canopy. tractive than apples themselves (Prokopy 1968, 1977). In addition, Surround WP also seems to have ad- Thus, it is not surprising that white spheres meant to verse tactile effects on adult tephritids. Lemoyne et al. visually mimic Surround-coated apples were less vi- (2008) found that female blueberry maggots spent sually stimulating than red spheres in our Þeld studies signiÞcantly more time walking and exhibited more reported here, as reported previously by Prokopy walking bouts on untreated blueberries compared (1968). Furthermore, Villanueva and Walgenbach with kaolin-treated blueberries in choice tests. Fe- (2007) found that fewer apple maggot alighted on males also spent signiÞcantly more time grooming Surround-coated red ÔRome BeautyÕ apples compared themselves when alighting on Surround-treated fruit. with untreated apples in Þeld-based choice tests, again In our studies, when female apple maggot were in- indicating that the presence of a white coating on the troduced to apple or hawthorn treated with full or fruit diminished the overall visual attractiveness of the spotty Surround WP treatments or to untreated fruit, stimulus. the total residence time on Surround-treated fruit was However, we found that spotty-coated spheres lower than on untreated fruit. Flies also spent less time were visually less attractive than white spheres or red resting and foraging when introduced to Surround-

Table 2. Mean total residence time, time spent resting, time spent foraging and time spent grooming by female apple maggot introduced onto untreated apples or onto apples treated with 3 or 6% spotty or full SWP treatments

Total residence time Resting Foraging Time spent grooming Treatment (mean s Ϯ SE) (mean s Ϯ SE) (mean s Ϯ SE) (mean % Ϯ SE) Untreated 340.0 Ϯ 49.3 133.3 Ϯ 30.1 216.6 Ϯ 36.9ab 14.9 Ϯ 2.8 3% Spotty 269.9 Ϯ 44.1 117.9 Ϯ 40.3 280.6 Ϯ 77.1a 21.1 Ϯ 5.2 6% Spotty 324.2 Ϯ 49.9 209.4 Ϯ 41.1 175.7 Ϯ 49.9ab 18.9 Ϯ 3.2 3% Full 261.1 Ϯ 49.6 125.9 Ϯ 41.5 134.5 Ϯ 27.3ab 13.0 Ϯ 2.3 6% Full 151.1 Ϯ 44.8 78.5 Ϯ 30.1 84.5 Ϯ 28.4b 13.9 Ϯ 5.3

Values followed by different letters within the same column are signiÞcantly different according to TukeyÕs HSD test (P Ͻ 0.05). April 2010 LESKEY ET AL.: BEHAVIOR AND MORTALITY OF THE APPLE MAGGOT 399

Table 3. Mean survivorship and % survivorship for apple maggot placed in untreated dishes (control) or in dishes treated with 1.5, 3.0, or 6.0% SWP and provided with no resources, 50 ␮l of water only, 100 ␮ l of water only, 20% sucrose solution or 20% sucrose solution presented as a refuge, and observed for 20 d

No resources 50 ␮l of water 100 ␮l of water Sucrose solution Sucrose solution ϩ Treatment (mean d Ϯ SE) (mean d Ϯ SE) (mean d Ϯ SE) (mean d Ϯ SE) refuge (mean d Ϯ SE) Control 1.05 Ϯ 0.12a (0.0) 1.60 Ϯ 0.10a (0.0) 1.73 Ϯ 0.08a (0.0) 14.85 Ϯ 0.99a (52.5) 13.13 Ϯ 0.32a (80.0) 1.5% SWP 0.65 Ϯ 0.08a (0.0) 1.03 Ϯ 0.15b (0.0) 1.33 Ϯ 0.11b (0.0) 1.88 Ϯ 0.29b (0.0) 10.37 Ϯ 0.60b (43.3) 3.0% SWP 0.60 Ϯ 0.09a (0.0) 0.45 Ϯ 0.12c (0.0) 1.05 Ϯ 0.11bc (0.0) 1.28 Ϯ 0.18b (0.0) 9.60 Ϯ 0.46b (23.3) 6.0% SWP 0.75 Ϯ 0.09a (0.0) 0.52 Ϯ 0.13c (0.0) 0.83 Ϯ 0.09c (0.0) 1.58 Ϯ 0.15b (0.0) 6.47 Ϯ 0.42c (6.7)

Values followed by different letters within the same column are signiÞcantly different according to TukeyÕs HSD test (P Ͻ 0.05). Values in parentheses are percentage. treated fruit compared with untreated fruit, with sig- served coupled with the greater proportion of time niÞcant differences recorded with hawthorn. Al- spent grooming when females were introduced on though apple-origin host races of apple maggots are Surround-treated fruit compared with untreated fruit not attracted over long distances to hawthorn odors in in our studies. Further evidence for the tactile deter- the Þeld (Linn et al. 2003), naive ßies of both apple and rent hypothesis was observed in our laboratory-based hawthorn origin accept hawthorn fruit as an oviposi- mortality trials; in trials in which food was provided in tion substrate at a much higher rate than apples the form of a refuge (sucrose-laden wicks) ßies were (Prokopy et al. 1982, 1985, 1988; Prokopy and Papaj almost always found standing on the refuge rather 1988). In this study, we assessed tactile responses on than on Surround-treated surfaces, often to the point both apple fruit (as the larval host and protected where the ßy became immobilized in the drying su- economic resource) and hawthorn fruit (as the an- crose solution. cestral host and preferred oviposition substrate). Interestingly, Surround exposure seems to be lethal Combined, these assessments provide a more rigorous to both apple maggot and R. suavis. When ßies were evaluation of Surround WP as a potential crop pro- provided with resources (food and/or water), ßies tectant based on tactile deterrence. exposed to untreated surfaces lived signiÞcantly Lemoyne et al. (2008) pointed to the potential for longer than those exposed to Surround-treated sur- Surround particles to hinder female perception of faces. In fact, apple maggot provided with a sucrose stimuli associated with host fruit surface and thus, solution lived on average Ϸ14 d in the untreated con- subsequent rejection of fruit based on a lack of host trol, but Ͻ2 d for all Surround treatments. When the recognition. Although we believe that particle Þlm sucrose solution was presented as a refuge for both could interfere with apple maggot perception of stim- apple maggot and R. suavis, survivorship time did uli present on the host surface, we did observe ovi- increase for both species, but those exposed to Sur- position by female apple maggot in hawthorns (but round still survived for a signiÞcantly shorter time not apples) treated with Surround WP, though much compared with those exposed to untreated surfaces. less frequently than in untreated hawthorns. Similarly, These results are different from those reported by Yee (2008) found that oviposition by cherry fruit ßies Liburd et al. (2003) who found that Surround was not on Surround-treated cherries was 36ϫ and 10ϫ less toxic to blueberry maggots. However, our laboratory- than in untreated cherries in no-choice and choice based bioassay methods ensured that ßies were forced experiments, respectively. Thus, at least for apple to contact the material. We cannot be certain of the maggot and cherry fruit ßy, females seem to be able to detect the host, despite the presence of the Surround mode of action, but we suspect that adherence of on the surface. However, the particles themselves particles to the mouthparts of the ßy based on mi- probably serve as a powerful tactile irritant or deter- croscopy studies (S.E.W. et al., unpublished data) may rent based on the shorter total residence times ob- have impeded uptake of food and water. Alternatively, particles may have blocked spiracles or led to desic- cation. -Table 4. Mean survivorship ؎ SE and % survivorship for Apple maggot probably avoid Surround-treated sur walnut husk ﬂies placed in untreated dishes (control) or in dishes faces if possible, diminishing the intensity of lethal treated with 1.5, 3.0, or 6.0% SWP and provided with no resources, 50 ␮ l of water only, or 20% sucrose solution presented effects. Thus, a rational deployment strategy that ex- as a refuge and observed for 20 d ploits the behavioral effects of Surround rather than relying on lethality must be considered. Although a No resources 50 ␮l water Sucrose solution ϩ Treatment spotty coating rather than an even coating of Surround (mean d Ϯ SE) (mean d Ϯ SE) refuge (mean d Ϯ SE) WP on the fruit surface more effectively disrupts ßy Control 0.85 Ϯ 0.10a (0.0) 2.05 Ϯ 0.11a (0.0) 13.40 Ϯ 0.24a (86.7) 1.5% SWP 0.50 Ϯ 0.08b (0.0) 0.88 Ϯ 0.12b (0.0) 9.93 Ϯ 0.45b (26.7) perception of the round silhouette provided by a fruit, 3.0% SWP 0.78 Ϯ 0.09ab (0.0) 0.68 Ϯ 0.12b (2.5) 9.60 Ϯ 0.50bc (16.7) an even coating is more likely to reduce overall res- 6.0% SWP 0.83 Ϯ 0.09ab (0.0) 0.83 Ϯ 0.23b (0.0) 8.10 Ϯ 048c (13.3) idence time on fruit and surrounding foliage, as Sur- round seems to serve as a powerful tactile deterrent. Values followed by different letters within the same column are signiÞcantly different according to TukeyÕs HSD test (P Ͻ 0.05). Thus, applying an even coating probably provides Values in parentheses are percentage. greater overall protection, but if spray equipment does 400 JOURNAL OF ECONOMIC ENTOMOLOGY Vol. 103, no. 2 not produce a perfectly even Þnish (as sometimes tree-fruit pest management. CABI Press, Oxforshire, occurs with typical air blast sprayers used in or- United Kingdom. chards), a spotty coating may serve as an effective Lemoyne, P., C. Vincent, S. Gual, and K. Mackenzie. 2008. visual disruptant for foraging ßies. Kaolin affects blueberry maggot behavior on fruit. J. A more effective approach may be to use Surround Econ. Entomol. 101: 118Ð125. as part of a pushÐpull strategy. A pushÐpull strategy Liburd, O. E., E. M. Finn, K. L. Pettit, and J. C. Wise. 2003. Response of blueberry maggot ßy (Diptera: Tephritidae) uses repellents or deterrents to push insects away from to imidicloprid-treated spheres and selected insecticides. a protected resource or crop in combination with Can. Entomol. 135: 427Ð438. attractants to pull insects toward an attractive, but Linn, Jr., C., J. L. Feder, S. Nojima, H. R. Dambroski, S. H. economically insigniÞcant resource (Cook et al. Berlocher, and W. Roelofs. 2003. Fruit odor discrimina- 2007). In this case, Surround WP serves to push insects tion and sympatric host race formation in Rhagoletis. away from the protected apple crop, whereas an at- Proc. Natl. Acad. Sci. U.S.A. 100: 11490Ð11493. tractive resource can be deployed to pull foraging Knight, A. L., T. R. Unruh, B. A. Christianson, G. J. Puterka, apple maggots. An effective target for this “pull” ap- and D. M. Glenn. 2000. Effects of a kaolin-based particle proach may be the apple-mimicking attracticidal Þlm on obliquebanded leafroller (Lepidoptera: Tortrici- spheres baited with attractive olfactory stimuli dae). J. Econ. Entomol. 93: 744Ð749. Owens, E. D., and R. J. Prokopy. 1984. Habitat background (Prokopy and Mason 1996, Green and Wright 2009). characteristics inßuencing Rhagoletis pomonella (Walsh) Such a multicomponent system could provide effec- (Dipt., Tephritidae) ßy response to foliar and fruit mim- tive behaviorally based control for this key tree fruit ics. Z. Ang. Entomol. 98: 98Ð103. pest. Papaj, D. R., and R. J. Prokopy. 1988. The effect of prior adult experience on components of habitat preference in the apple maggot ßy (Rhagoletis pomonella). Oecologia Acknowledgments 76: 538Ð543. Prokopy, R. J. 1968. Visual responses of apple maggot ßies, We thank Torri Hancock, John Cullum, Robbie Alleman, Rhagoletis pomonella: orchard studies. Entomol. Exp. and J. 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