TY - JOUR
AU - Collins, Judith, A
AB - Abstract Over a period of 5 yr (2012–2016), we conducted laboratory and field studies on activity, movement, and response to trap placement of adult Drosophila suzukii (Matsumura) in wild blueberry, Vaccinium angustifolium Aiton, fields in Maine. When measuring temporal patterns in fruit infestation, we found that D. suzukii females are most active in the morning and that they are 10 times more likely to lay eggs in blueberries at the top of the plant canopy compared with berries located in the lower part of the bush. Flies were found to be more abundant in fruit-bearing (crop) fields compared with pruned (vegetative) fields based on trap capture of adults. They are also most abundant along edges of fields compared with interiors. Trap efficiency is significantly better in traps 1.2 m above the ground and above the crop canopy of this low-growing crop plant than within the crop canopy. Three experiments involving the marking of laboratory-reared flies with fluorescent marker, their release, and capture with traps along a grid in fields suggest that: 1) fluorescent markers do not affect the distance moved of marked flies, 2) dispersal rates are not different between sexes, 3) there is little difference in the dispersal pattern through pruned fields and fruit-bearing fields, and 4) flies disperse at a low rate of 0.1–30 m per day, with an average of 5 m per day, but that long-distance dispersal over 1–2 km is feasible based on statistical model extrapolation. dispersal, wild blueberry, Vaccinium angustifolium, activity period, field edge Integrated pest management (IPM) relies on accurate monitoring techniques and effective control strategies that can suppress pest populations while conserving natural enemies and avoiding resistance (Van den Bosch and Stern 1962, Fernandez-Cornejo and Jans 1999). Even within the same pest species, IPM can vary widely across different regions and cropping systems (Karuppuchamy and Venugopal 2016). IPM decisions are based on a pest’s life cycle and the interaction between its crop host and the environment (Cupers et al. 2000). Before an IPM program can be developed, a solid understanding of a pest’s biology and its interaction with its host is necessary. This can include knowledge on optimal trapping methods, the pest’s activity period and reproductive parameters, and movement within the landscape. This can present a challenge for generalist pests that are found on a wide variety of hosts, as different crops may require different IPM strategies. Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) is an invasive vinegar fly from Asia that has established across North America, Europe, and South America (Hauser 2011, Cini et al. 2012, Deprá et al. 2014, Asplen et al. 2015) in a diverse array of soft-skinned crops including blackberries, blueberries, cherries, raspberries, and strawberries, among others (Lee et al. 2011, Little et al. 2017). Although most Drosophila species lay eggs in rotten or damaged fruit (Karageorgi et al. 2017), D. suzukii possesses a large, serrated ovipositor that allows females to place eggs into intact fruit (Atallah et al. 2014). Its unique life history has enabled it to become a cosmopolitan species that is capable of reproducing under a wide range of temperatures (Tochen et al. 2014) and on a large number of cultivated and native fruit, including wild blueberry (Lee et al. 2015, Poyet et al. 2015, Drummond et al. 2017). Wild (lowbush) blueberries Vaccinium angustifolium Aiton (Ericales: Ericaceae) are different from most other fruit cropping systems in the world in that they are not planted. Fields are established by clearing the forest overstory and encouraging the native understory blueberry plants to spread in the absence of plant competition through the use of weed control and soil amendments (Yarborough 2009). As a result of land management practices, most wild blueberry fields are surrounded by forested edges (Ballman and Drummond 2018). Wild blueberries also differ in that they are a low-growing shrub, less than 0.5 m tall, unlike the taller highbush blueberry, Vaccinium corymbosum L. (Ericales: Ericaceae) (Jones et al. 2014). Wild blueberries grow clonally, and plant characteristics such as berry size can vary greatly between and even within clones (Chiasson and Argall 2010, Bajcz and Drummond 2017, Qu and Drummond 2018). Wild blueberry fields in Maine are most often managed on a 2-yr cycle (Yarborough 2009). Year 1 is the prune year, where the plants are pruned and only vegetative and flower bud development occurs. Year 2 is the crop year, where bloom and the resulting berry crop occurs. Like many soft-skinned fruits, wild blueberry is a known host for D. suzukii, where it was first detected in Maine’s wild blueberry landscape in 2011 (Drummond et al. 2018). Since its introduction, growers and researchers have been collaborating to find ways to control this pest. Although numerous D. suzukii control methods have been studied, including early harvest (Leach et al. 2018), mass-trapping (Hampton et al. 2014, Alnajjar et al. 2017), attracticidal spheres (Rice et al. 2017), exclusionary netting (Alnajjar et al. 2017), and biological control (Chabert et al. 2012, Miller et al. 2015, Woltz et al. 2015, Ballman et al. 2017, Knoll et al. 2017, Stacconi et al. 2017, Woltz and Lee 2017, Zhu et al. 2017, Alnajjar et al. 2018), pesticides remain the most commonly used control method (Walton et al. 2016). As a consequence of the difficulty in controlling this pest, pesticide use has increased in a number of crops. A study by Van Steenwyk and Bolda (2015) reported up to a 4.8-fold increase of pesticide application in California cherry, which has greatly disrupted IPM practices. It is likely that pesticide use as a result of D. suzukii infestation is increasing and disrupting IPM in a number of other crops as well. This is certainly the case for wild blueberry in Maine (F. A. Drummond, personal observation), though if growers can utilize pest monitoring before insecticide applications, they may be able to reduce this negative impact. Pest monitoring is considered the cornerstone of IPM (Pedigo et al. 1986). Numerous studies have examined optimal D. suzukii trap designs and bait, though trap height is usually standardized within each study and not experimentally determined (Lee et al. 2012, 2013; Renkema et al. 2014; Burrack et al. 2015; Kirkpatrick et al. 2017; Renkema et al. 2018). Currently, traps appear to only capture a small portion (ca. 5%) of D. suzukii within a field (Alnajjar et al. 2018, Kirkpatrick et al. 2018). This highlights the need for more effective trap design, bait, and placement. Most advice regarding trap placement is to place it at the level of the fruit, but these recommendations are often based on studies conducted with relatively tall crop plants such as raspberries, cherries, and highbush blueberries (Dreves and Langellotto-Rhodaback 2011, Gerdeman et al. 2011, Spears et al. 2017, Wallingford et al. 2018). It is unclear if this is the best recommendation for short shrubby fruits such as wild blueberries. Equally important to IPM is understanding pest interactions with its host and environment (Cupers et al. 2000, Yarborough et al. 2017). Understanding these interactions can help growers maximize pesticide efficacy that in turn may reduce pesticide use by reducing the need for repeated applications. Drosophila suzukii is a cosmopolitan pest and will most likely require IPM techniques tailored to individual regions and crops. Although much research has been conducted over the past decade, effects of specific crop hosts and climate region on D. suzukii’s biology can vary tremendously (Bellamy et al. 2013, Lee et al. 2015, Klick et al. 2016, Ballman et al. 2017, Little et al. 2017, Ballman and Drummond 2018, Stockton et al. 2019). Oviposition and movement of D. suzukii are not always studied jointly in different host crop systems (Kinjo et al. 2012, Tochen et al. 2014, Wang et al. 2016, Alnajjar et al. 2018). Understanding the basic biology of a pest in its host crop helps growers make the best management decisions (Pedigo et al. 1986). In the wild blueberry agroecosystem, we studied how trap placement relative to the crop canopy affects catches of D. suzukii, oviposition site preferences and diurnal activity, and movement of adults in fields. We monitored the time it took to recolonize a field following an insecticide application, as well as the distance traveled within and into blueberry fields using mark, release, and capture studies. Materials and Methods Spotted-Wing Drosophila Colonies Drosophila suzukii populations were initially acquired from the Connecticut Agriculture Experiment Station in 2012. Subsequent additions of adult flies to the laboratory colony were acquired from University of Maine Cooperative Extension, Orono, ME. Flies were reared on Instant Drosophila Medium formula 4–24 (Carolina Biological Supply Co., Burlington, NC) and held in 7.3 × 2.0 cm Drosophila culture tubes in the laboratory at 20–23°C. Adult D. suzukii were transferred to new media every 2–3 wk. Trap Design and Bait For all trials, adult D. suzukii traps were made from 473-ml red polystyrene Solo cups with light-blocking lids. Seven to ten, 0.48-cm holes were evenly punched around the rim. The traps were baited with 118 ml of a sugar/yeast bait (5.07 g dry active yeast, 25.35 g sugar, 450 ml water; Drummond et al. 2017). Unless otherwise stated, traps were hung 0.61 m above the top of the blueberry canopy using 0.91 m plant stands and were placed along the field edges. Traps were returned to the lab and drained through a fine mesh sieve to identify and count flies (Drummond et al. 2017). Trap Height and Adult Captures In 2012, we studied adult D. suzukii trap capture rates in traps placed at the level of the wild blueberry canopy versus an elevated placement. Nineteen commercial wild blueberry fields were sampled weekly from 9 August 2012 to 1 October 2012. Traps were deployed in 3 fields in Waldo Co., 11 fields in Hancock Co., and 7 fields in Washington Co., Maine. All traps were placed along the blueberry field edge. In each field, two traps were placed in the blueberry plant canopy (<0.25 m above ground) and three traps were hung 1.2 m high from trees and shrubs along the field edge. In each field, traps were spaced 15 m apart from one another and alternated between the two trap locations (elevated vs canopy), starting and ending with a trap hung from a tree/shrub. Traps were left in the field for 1 wk before being replaced with freshly baited traps. Contents of the old traps were brought back to the laboratory for processing. In the laboratory, males and female D. suzukii were identified and counted. Because traps did not catch many flies until 23 August, statistical analysis of trap capture due to trap height was only conducted from 23 August to 1 October. Nested negative binomial generalized regression was used to assess week, field within week, trap height, and trap height × week effects on male, female, and total (male + female) fly trap captures. The nested models were fit as fixed effect (trap height) models nested within (trap location) using the MLE Generalized Regression JMP Platform (SAS Institute 2017). Model residuals did not deviate from the negative binomial error as determined by a χ2 deviance test (P > 0.05). Trap Location (Field Edge vs Field Interior) In 2012, nine commercial wild blueberry fields were also sampled by placing traps both in the field interior (30 m from the field edge) and in the shrub and tree line immediately along the field edge (within 1 m of blueberries). Traps were deployed in three fields in Waldo Co. and six fields in Hancock Co., Maine. Four traps were deployed in each field: two in the field interior within the wild blueberry plant canopy (<0.25 m) and two traps at a 1.2 m height above the ground along the field edge. No traps were hung at the 1.2 m height in the field interior, and so our comparison was traps in the lower tree/shrub canopy (1.2 m) along the blueberry field edge, compared with traps in the blueberry plant canopy in the blueberry field interior. Blueberry fields and field edges were sampled from 17 August to 17 September when many fields had been harvested. Traps were collected weekly and replaced with freshly baited traps. The collected traps were taken back to the laboratory for D. suzukii assessment as described previously. The statistical modeling followed an identical approach described in the previous section (trap height as fixed effects nested within trap location and the dependent variable being adult captures) using negative binomial generalized regression (SAS Institute 2017). Oviposition Site and Activity Period In August 2013, we tested D. suzukii’s spatial variation in infestation between nonshaded fruit at the top of wild blueberry stems and shaded fruit at the middle and bottom of stems. We also determined the activity period of oviposition. Both experiments were run at the University of Maine’s Blueberry Hill Experiment Station in Jonesboro, Washington County, ME. To test oviposition site, 25–32 berries per stem were collected from the nonshaded top of 10 stems; 19–30 berries per stem were collected from the lower half portion of 10 different stems that were shaded by foliage. Fruit from each stem were held in filter-paper lined, 7 cm, Petri dishes for 1 wk at 20–23°C and then processed for D. suzukii larvae using a modified salt extraction method described in Drummond et al. (2017). We then calculated the mean number of D. suzukii larvae per berry for each stem and compared infestation in shaded and nonshaded fruit. A weighted mixed (fruit per stem) analysis of variance (ANOVA; SAS Institute 2017) randomized complete block design (RCB, stem as a random effect or block) was used to measure the difference in larval infestation of fruit, on a per stem basis, between stem location/shading. Homogeneity of variance was tested graphically and conformance of the data to normality was tested using the Shapiro–Wilk test (Shapiro and Wilk 1965). To determine the activity period of oviposition, 20 laboratory-reared D. suzukii adults (a mixture of males and females) were placed in oviposition cages (20 × 23 cm, clear plastic hamster cage inverted and attached to a piece of plywood as a base). There were four cages each; each was set up at the same time and considered as a separate replicate. Cages had a 15-cm sleeve-lined hole, and each cage contained a diet cup with a cotton ball soaked with the standard sugar/yeast solution (Drummond et al. 2017). The flies were acclimated to the cages for 1 d, and then stems with ripe blueberries were placed in 100-ml glass beakers with water and placed in the cages. The sugar/yeast solution was removed, and the cages were placed outside to simulate natural lighting and temperature conditions. The old stems were removed and new stems were placed in the cages at 4-h intervals beginning at 0800 and continuing until 2000 h. For the final treatment, stems were placed in the cages at 2000 h and left until 0800 h. Stems were held at 20°C in the laboratory for 6 d after exposure, and then the fruit was removed from the stems, counted, and placed in Petri dishes lined with filter paper. After an additional 3 d, the fruit was processed for D. suzukii larvae using the salt extraction method (Drummond et al. 2017). Each oviposition time period was randomized and replicated four times with each cage considered a separate trial or replicate. A randomized complete block design (RCB, trial or replicate as block) fixed effects ANOVA (SAS Institute 2017) was used to analyze the differences in larval infestation of fruit (mean spotted-wing drosophila larvae/fruit) exposed to flies at different time periods as a proxy for oviposition activity period. We did not need to transform the data to meet the homogeneity of variance (assessed graphically) or normality (Shapiro–Wilk test) assumptions required by ANOVA. Colonization and Within-Field Movement Two different types of studies were conducted. The first involved reducing field resident adults in a fruit-bearing field with the use of an insecticide application and then monitoring the buildup of flies immediately after the application. The second type of study involved mark, release, and capture of flies at known distances from release sites over time. Post-pesticide Colonization of a Wild Blueberry Field The objective of the study was to determine how quickly flies recolonize a field after a pesticide application. This was a nonreplicated experiment. On 15 August 2013, the insecticide Delegate 30WG (425 gm/ha) was applied to a 2.4 ha fruit-bearing field at the University of Maine’s Blueberry Hill Research Farm in Jonesboro, Washington County, ME. The application was made prior to detectable fruit infestation. Therefore, we assumed that an increasing rate of flies captured in traps post-insecticide application measured the rate of recolonization of the field. The insecticide was applied with a tractor-mounted, CIMA P55D Atomizer L.V. sprayer in 189.3 liter of water per hectare. Immediately following the application, D. suzukii monitoring traps were placed 6.1 m apart in a 61 × 61 m grid in a 0.4 ha corner of the 2.4 ha field for a total of 121 traps. The grid was set so that one edge was along the field border and 6.1 m from the edge of the woods. There was a minimum of 61 m from the trial area to the other three field boundaries. A dirt road surrounded the study area. Each trap was numbered, and the traps were checked daily for 4 d post-application. The daily rate of colonization was estimated using Poisson regression on the collected time series of captures. The independent variable was distance from the field edge, and the dependent variable was number of flies captured at specific distances along each of the transects into the center of the field. A generalized linear model based on the Poisson as the error distribution and the log link function was used to estimate the daily colonization rate (SAS Institute 2017). Overdispersion in the Poisson was tested with the Pearson χ2, and the estimation algorithm was the Firth adjusted maximum likelihood (Firth 1993). Mark, Release, Capture Studies To study their dispersal patterns, laboratory-reared D. suzukii adults were released in pruned and fruit-bearing wild blueberry fields. To assess movement of D. suzukii adults into wild blueberry fields, three replicated experiments were conducted during 2014, 2015, and 2016. Details of the experimental design including field production status, trial start date, number of transects, and number of flies released for each trial are described in Table 1. Table 1. Within-field movement of spotted-wing drosophila in pruned and fruit-bearing fields Trial Year Field status Site location Transects (distance between transects) Start date No. of Drosophila suzukii released Frequency monitored (no. of days trapped) Released flies sex ratio Experiment 1 1 2014 Pruned Winterport, ME 5 (15m)a 8 July 1,481 not marked and released, 413 marked and released (prior to occurrence of wild D. suzukii) Daily (5 d) Unknown 2 2014 Pruned Winterport, ME 5 (15 m)a 7 Aug. 2,803 marked and released Daily (7 d) Unknown 3 2014 Pruned Winterport, ME 5 (15 m)a 10 Oct. 1,108 marked and released Daily (7 d) Unknown Experiment 2 1 2014 Fruit-bearing Jonesboro, ME 5 (15 m)a 28 Aug. 2,043 marked and released Daily (8 d) Unknown 2 2015 Fruit-bearing Jonesboro, ME 5 (15 m)a 14 July 2,820 not marked and released (prior to occurrence of wild D. suzukii) Daily (7 d) 50:50 Experiment 3 1 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 26 July 2,458 marked and released Every other day (7 d) 50:50 2 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 19 Aug. 1,891 marked and released Every other day (7 d) 50:50 3 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 7 Sept. 1,846 marked and released Every other day (7 d) 50:50 Trial Year Field status Site location Transects (distance between transects) Start date No. of Drosophila suzukii released Frequency monitored (no. of days trapped) Released flies sex ratio Experiment 1 1 2014 Pruned Winterport, ME 5 (15m)a 8 July 1,481 not marked and released, 413 marked and released (prior to occurrence of wild D. suzukii) Daily (5 d) Unknown 2 2014 Pruned Winterport, ME 5 (15 m)a 7 Aug. 2,803 marked and released Daily (7 d) Unknown 3 2014 Pruned Winterport, ME 5 (15 m)a 10 Oct. 1,108 marked and released Daily (7 d) Unknown Experiment 2 1 2014 Fruit-bearing Jonesboro, ME 5 (15 m)a 28 Aug. 2,043 marked and released Daily (8 d) Unknown 2 2015 Fruit-bearing Jonesboro, ME 5 (15 m)a 14 July 2,820 not marked and released (prior to occurrence of wild D. suzukii) Daily (7 d) 50:50 Experiment 3 1 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 26 July 2,458 marked and released Every other day (7 d) 50:50 2 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 19 Aug. 1,891 marked and released Every other day (7 d) 50:50 3 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 7 Sept. 1,846 marked and released Every other day (7 d) 50:50 aTrap spacing distances within transect (release point, 4, 7.6, 15, 30.5, 61, 122 m), 2–5 parallel transects 122 m in length. bTrap spacing distances within transect (50, 30, 10, 5, 2.5 m, release point, 2.5, 5, 10, 30, 50 m), 2 transects at right angles to each other and intersecting at the release point. Open in new tab Table 1. Within-field movement of spotted-wing drosophila in pruned and fruit-bearing fields Trial Year Field status Site location Transects (distance between transects) Start date No. of Drosophila suzukii released Frequency monitored (no. of days trapped) Released flies sex ratio Experiment 1 1 2014 Pruned Winterport, ME 5 (15m)a 8 July 1,481 not marked and released, 413 marked and released (prior to occurrence of wild D. suzukii) Daily (5 d) Unknown 2 2014 Pruned Winterport, ME 5 (15 m)a 7 Aug. 2,803 marked and released Daily (7 d) Unknown 3 2014 Pruned Winterport, ME 5 (15 m)a 10 Oct. 1,108 marked and released Daily (7 d) Unknown Experiment 2 1 2014 Fruit-bearing Jonesboro, ME 5 (15 m)a 28 Aug. 2,043 marked and released Daily (8 d) Unknown 2 2015 Fruit-bearing Jonesboro, ME 5 (15 m)a 14 July 2,820 not marked and released (prior to occurrence of wild D. suzukii) Daily (7 d) 50:50 Experiment 3 1 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 26 July 2,458 marked and released Every other day (7 d) 50:50 2 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 19 Aug. 1,891 marked and released Every other day (7 d) 50:50 3 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 7 Sept. 1,846 marked and released Every other day (7 d) 50:50 Trial Year Field status Site location Transects (distance between transects) Start date No. of Drosophila suzukii released Frequency monitored (no. of days trapped) Released flies sex ratio Experiment 1 1 2014 Pruned Winterport, ME 5 (15m)a 8 July 1,481 not marked and released, 413 marked and released (prior to occurrence of wild D. suzukii) Daily (5 d) Unknown 2 2014 Pruned Winterport, ME 5 (15 m)a 7 Aug. 2,803 marked and released Daily (7 d) Unknown 3 2014 Pruned Winterport, ME 5 (15 m)a 10 Oct. 1,108 marked and released Daily (7 d) Unknown Experiment 2 1 2014 Fruit-bearing Jonesboro, ME 5 (15 m)a 28 Aug. 2,043 marked and released Daily (8 d) Unknown 2 2015 Fruit-bearing Jonesboro, ME 5 (15 m)a 14 July 2,820 not marked and released (prior to occurrence of wild D. suzukii) Daily (7 d) 50:50 Experiment 3 1 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 26 July 2,458 marked and released Every other day (7 d) 50:50 2 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 19 Aug. 1,891 marked and released Every other day (7 d) 50:50 3 2016 Fruit-bearing Jonesboro, ME 2 (crossed 100 m)b 7 Sept. 1,846 marked and released Every other day (7 d) 50:50 aTrap spacing distances within transect (release point, 4, 7.6, 15, 30.5, 61, 122 m), 2–5 parallel transects 122 m in length. bTrap spacing distances within transect (50, 30, 10, 5, 2.5 m, release point, 2.5, 5, 10, 30, 50 m), 2 transects at right angles to each other and intersecting at the release point. Open in new tab One week prior to the start of each release of laboratory-reared adults, all fields were monitored with 15–20 traps to verify the absence or presence of naturally occurring wild flies. The bait used was our standard sugar/yeast mixture (5.07 g dry active yeast, 25.35 g sugar, 450 ml water, Drummond et al. 2019) deployed in the field in red Solo cups (see Trap design and bait section). The first release in 2014 was made prior to the detection of any naturally occurring wild flies, and so we released both fluorescent-marked and non-marked laboratory-reared flies to assess the effect of the fluorescent marker on dispersal. All other releases occurred when wild flies were present in the field; therefore, laboratory-reared flies were marked with fluorescent powder. Marking Methods Flies were marked with fluorescent powder in all three experiments. They were marked with either Neon Pink or Arc Orange DayGlo (DayGlo Color Corp., Cleveland, OH) fluorescent powder. In experiments 1 and 2, empty plastic Drosophila tubes (28.5 × 95 mm) were coated with a light layer of the powder. One hundred flies at a time were anesthetized with CO2, added to a tube, and then gently rolled in the powder. The marked flies were then immediately transferred to tubes containing standard Drosophila media. The flies were allowed to groom and rest for 24 h before the release to remove any excess fluorescent marker. Non-marked flies (experiment 1, trial 1 only) were handled in the same manner, but were rolled in a tube without the fluorescent marker. For experiment 3, 100 flies at a time were anesthetized with CO2 and held in 540-ml plastic deli cups on ice while the fluorescent marker was administered. A thin layer of marker was applied by spraying a puff of fluorescent marker from a bulb duster (Punchau Pest Control Bulb Duster). A moist cotton ball and pea-sized amount of commercial Instant Drosophila Medium formula 4–24 (Carolina Biological Supply Co., Burlington, NC) was added to each deli container, and flies were held for 24 h before release. To release, flies were tapped into Petri dishes. Any flies that had not flown away after 10 min were brought back to the laboratory, counted, and subtracted from the total to give an accurate number of released flies. In all three experiments, trap captured flies were examined under UV light (Black-Ray Longwave Ultraviolet Lamp, UVP, Upland, CA) for the presence of the fluorescent marker. Field Setup Experiment 1 involved three trials in 2014 using mark, release, capture of adults in a pruned wild blueberry field. Three temporal trials were located in a nonpesticide treated 15.7 ha pruned field in Winterport, Waldo Co., ME. There were five transects in each trial. Each transect was 122 m long and 15 m apart from one another; within transects, traps were placed at 4, 7.6, 15, 30.5, 61, and 122 m from the release point (field edge). Traps were changed and checked for flies daily for 5 d (trial 1) or 7 d (trials 2 and 3). The sex ratios of released and captured flies were not recorded. Experiment 2 was conducted in 2014 and 2015. The two trials took place (one in 2014 and one in 2015) in a different untreated fruit-bearing field each year at the University of Maine’s Blueberry Hill Research Farm in Jonesboro, Washington Co., ME. There were five transects in each trial. Each transect was 122 m long and 15 m apart from one another; within transects, traps were placed at 4, 7.6, 15, 30.5, 61, and 122 m from the release point (field edge). In trial 2, marked flies were released in a 50:50 sex ratio. The bait in the traps was changed, and all traps were checked daily for D. suzukii adults until no flies were caught for two consecutive days. In trial 2, sex was recorded for all captured flies. Experiment 3 involved three trials in 2016 to assess the within-crop field movement of D. suzukii. All trials were established in fruit-bearing fields at the University of Maine’s Wild Blueberry Farm in Jonesboro, ME. The sex ratio of the released flies was 50:50, and the sex of captured marked flies was recorded. Two, 100 m perpendicular intersecting transects were used, and flies were released at the point of intersection. Within transects, recapture cups were set at 2.5, 5, 10, 30, and 50 m from the central release point. Traps were checked and replaced every other day for 8 d. Statistical analysis of the mark, release, and capture studies was performed using JMP software (SAS Institute 2017). All analyses were based on zero-inflated Poisson regression (Hall 2000). This was used because a zero capture represents flies that do not disperse far enough, as well as flies that disperse but are not captured in traps. Flies may not have been captured at trap locations because of predation, bait degradation, or competition from fruit. Thus, the number of zeroes is more than might be expected from a theoretical Poisson density function. Distance moved into the wild blueberry field was estimated by using knowledge of the release point for each marked fly and then depending on the transect and distance into the field the fly was captured, the Pythagorean theorem was used to estimate a straight-line hypotenuse to the trap. A nonzero inflated Poisson regression was used to assess whether trial, transect, distance into the field, or transect × distance into the field were factors that affected capture of flies. In the first trial, we compared dispersal into the wild blueberry field between unmarked and marked (orange and pink powder) flies to determine whether marking flies with fluorescent marker had a deleterious effect on fly movement and would bias the estimated dispersal patterns. The comparison of marked and non-marked fly dispersal was based on the distance × fluorescent marker treatment interaction. Evidence of this interaction effect (P ≤ 0.05) was assumed to be indicative of a fluorescent marker effect on fly movement into the field after release. Experiments 2 and 3 compared male and female fly dispersal distances. A generalized linear Poisson model (SAS Institute 2017) with adjustment for zero inflation was used to estimate the number of flies captured after release (dependent variable). Distance, transect, and sex were fixed effect independent variables. In these analyses, the sex × distance interaction was used to determine whether one sex moved farther than the other sex (statistically significant sex × distance interaction). Results Trap Height and Adult Captures Significantly fewer D. suzukii were caught in traps placed on the ground (canopy-level traps, <0.25 m above ground) compared with elevated traps (1.2 m above ground) along the wild blueberry field edges. This was true for males (χ2(1) = 30.999, P < 0.0001), females (χ2(1) = 19.498, P < 0.0001), and total combined sexes (χ2(1) = 50.079, P < 0.0001). In addition, for males, females, and combined sexes, there was a significant interaction between week and trap height (P < 0.05). This interaction suggests that as the growing season progressed, a higher proportion of flies were caught in the elevated traps earlier in the season than later in the season (Fig. 1). Overall, by the end of the trapping period, ground canopy-level traps caught an average of 15.52 ± 4.06 cumulative flies, whereas elevated traps caught an average of 182.37 ± 45.19 cumulative flies. The seasonal trend in the proportion of flies captured in the elevated traps compared with the canopy-level traps was assessed by regression of week (reciprocal transformed) on the proportion of flies in the elevated traps. This regression provided evidence of a monotonically increase in proportion flies, but in a decreasing rate of increase (F(1,4) = 7.402, P = 0.053, r2 = 0.59). Fig. 1. Open in new tabDownload slide Drosophila suzukii captures in elevated traps (1.2 m above ground) compared with wild blueberry canopy-level (<0.25 m above ground) traps along wild blueberry field edges, male (A), female (B), and total fly captures (C). Error bars are SE. Fig. 1. Open in new tabDownload slide Drosophila suzukii captures in elevated traps (1.2 m above ground) compared with wild blueberry canopy-level (<0.25 m above ground) traps along wild blueberry field edges, male (A), female (B), and total fly captures (C). Error bars are SE. Trap Location (Field Edge vs Field Interior) Significantly more adult D. suzukii were caught in traps placed along wild blueberry field edges at the canopy level of shrubs and trees (1.2 m above ground) compared with traps placed at the canopy level of wild blueberry plants in the interior of the blueberry field. This was true for males (χ2(1) = 15.996, P < 0.0001), females (χ2(1) = 36.498, P < 0.0001), and total combined sexes (χ2(1) = 45.184, P < 0.0001). In addition, for males, females, and combined sexes, there was a significant interaction between week and trap height (P < 0.05). This interaction suggests that as the growing season progressed, a higher proportion of flies were caught in the field edge than in the blueberry field (Fig. 2). Inspection of the negative binomial maximum likelihood estimates of the coefficients for the week × field × field location interaction showed that they were all (n = 26) positive, but of differing degrees. This supports the pattern of increasing proportion of flies caught at the field edge relative to the field interior as the season progressed. Overall, by the end of the growing season, edge traps caught an average of 56.24 ± 11.77 cumulative flies, whereas interior blueberry field traps caught an average of 1.08 ± 0.48 cumulative flies. Fig. 2. Open in new tabDownload slide Drosophila suzukii captures in traps along wild blueberry field edges (1.2 m above ground) compared with wild blueberry canopy-level (<0.25 m above ground) traps in the interior of wild blueberry fields, male (A), female (B), and total fly captures (C). Error bars are SE. Fig. 2. Open in new tabDownload slide Drosophila suzukii captures in traps along wild blueberry field edges (1.2 m above ground) compared with wild blueberry canopy-level (<0.25 m above ground) traps in the interior of wild blueberry fields, male (A), female (B), and total fly captures (C). Error bars are SE. Oviposition Site and Activity Period A significantly higher proportion of D. suzukii larvae were found in nonshaded fruit collected from the top of a stem compared with shaded fruit collected from the bottom half of a stem. Fruits collected from the top of 7 of 10 stems were found to be infested; infested fruit was found on the bottom of only 2 of 10 stems. The mean number of larvae per berry was 0.10 ± 0.03 (top) and 0.02 ± 0.01 (bottom). Despite the low number of larvae, there was a significant difference (approximately 5×) in the mean number of D. suzukii per berry between fruit collected from the top and bottom of stems (F(1,18) = 4.815, P = 0.042). There was a significant difference in larval infestation among the oviposition time periods. Most D. suzukii oviposition activity occurred during the day; there was no significant difference among the three daylight periods (0800–1200, 1200–1600, and 1600–2000 h); however, all three were significantly higher than the evening (2000–0800 h) period (F(3,9) = 9.572, P = 0.004; Fig. 3). However, when a trend analysis was performed (single degree of freedom contrast), a linearly decreasing trend in larval infestation is supported with the highest in the morning decreasing throughout the day and then being minimal throughout the evening (F(1,8) = 22.104, P = 0.002; Fig. 3). Fig. 3. Open in new tabDownload slide Larval infestation of wild blueberry fruit reflecting oviposition activity at different times of the day. Error bars are SE. Fig. 3. Open in new tabDownload slide Larval infestation of wild blueberry fruit reflecting oviposition activity at different times of the day. Error bars are SE. Colonization and Within-Field Movement Post-pesticide Colonization of a Wild Blueberry Field Adult D. suzukii moved into the field very quickly following the application of Delegate (Fig. 4). Three traps captured D. suzukii 1 d after application (2.5% of all traps), and 4 d after application, 38.0% of all traps had captured flies. The area treated with insecticide was 2.4 ha. The trapped area was in one corner of the treated area of 0.4 ha (61 × 61 m). Therefore, if most trap captures resulted from flies moving into the treated area from outside the 2.4 ha field, it appears that colonization can occur at a geometric rate (χ2(1) = 11.204, P = 0.008), of approximately 5.5 ± 1.8 flies per day on a linear basis (Fig. 4). Distance moved into the field was 36.6 m on day 1 and 61 m (the far edge of the grid) by the second day after the insecticide application. The number of flies captured during the experiment was not enough to provide statistical power for a two-dimensional spatial analysis of fly colonization over time. However, by the end of the experiment, a spatial pattern of fly abundance declining toward the field interior was observed (P < 0.05). Fig. 4. Open in new tabDownload slide Colonization of a wild blueberry field by Drosophila suzukii after an insecticide application, total flies captured in field, and flies captured per trap on each day post-application. Error bars are SE and calculated from flies per trap data. Regression line is based on Poisson regression (P = 0.008). Fig. 4. Open in new tabDownload slide Colonization of a wild blueberry field by Drosophila suzukii after an insecticide application, total flies captured in field, and flies captured per trap on each day post-application. Error bars are SE and calculated from flies per trap data. Regression line is based on Poisson regression (P = 0.008). Colonization of Wild Blueberry Fields In experiment 1 (trial 1), we captured significantly more non-marked flies than marked flies (χ2(1) = 12.056, P = 0.0005). We found that fly dispersal dropped off significantly as one moved into the pruned field (χ2(1) = 13.164, P = 0.0003); we found no evidence of a difference between non-marked and marked fly dispersal distance (χ2(1) = 0.787, P = 0.375). We also found no effect of transect (χ2(4) = 2.846, P = 0.584). In the 2014 prune trial, the capture rate for flies released along field edges was 2.18–5.76 (trial 1), 2.18 (trial 2), and 3.24% (trial 3). Released flies traveled maximum distances per day of 121.92 m (trial 1), 136.3 m (trial 2), and 62.8 m (trial 3). An analysis of the three trials in the 2014 prune field in Winterport showed that capture of released fluorescent marked flies varied by trial (χ2(2) = 43.071, P < 0.0001) and marginally for transect within trial (χ2(4) = 7.810, P = 0.098). The distance that released flies were captured at varied by trial (χ2(2) = 18.352, P = 0.0001). Overall, fewer flies were caught in traps further from the field edge (χ2(1) = 15.276, P < 0.0001, slope = −0.048 ± 0.012). Figure 5 depicts the distance that flies penetrated into the two fields per day, and the exponential decay curve represents the average dispersal pattern per day during the 2014 study. Fig. 5. Open in new tabDownload slide Dispersal distances in trials conducted in 2014. Trials 1–3 were performed in a pruned field. Exponential curve fit to mean of all data (Y = 10.410 × X−0.485, r2 = 0.940, P = 0.002). Error bars are SE. Fig. 5. Open in new tabDownload slide Dispersal distances in trials conducted in 2014. Trials 1–3 were performed in a pruned field. Exponential curve fit to mean of all data (Y = 10.410 × X−0.485, r2 = 0.940, P = 0.002). Error bars are SE. In experiment 2, capture rates of released flies were 1.7–2% in fruit-bearing fields. We found that male and female captures were not significantly different (χ2(1) = 3.395, P = 0.065), although there was a trend toward more females captured than males (30 vs 17). There was also no significant sex × trap capture distance interaction (χ2(1) = 1.777, P = 0.183), suggesting that there was no difference in the distance each sex dispersed over the experiment. The trap capture distance was significant (χ2(1) = 9.125, P = 0.003). The coefficient for the distance term was −0.081 ± 0.027, suggesting a decrease in trap capture as one moves farther from the point of release. The maximum traveled distance per day reflected by trap capture was approximately 120 m, whereas the average distance was 7.9, 26.3, and 10.5 m per day, for each of the three trials, respectively. Figure 6 illustrates the dispersal per day within the wild blueberry fruit-bearing fields for both years. A decay curve was fit to all the data in both years to estimate an average per day dispersal rate. Fig. 6. Open in new tabDownload slide Number of total flies (male + female) captured at each trap distance in a 2014 fruit-bearing field; male, female, and total flies captured in a 2015 fruit-bearing field; and the mean number of flies captured in both years. Exponential fit to total fly capture distances in both 2014 and 2015 (Y = 0.019 + 7.438 × e(-0.139 × X), r2 = 0.993, P < 0.0001). Error bars are standard errors. Fig. 6. Open in new tabDownload slide Number of total flies (male + female) captured at each trap distance in a 2014 fruit-bearing field; male, female, and total flies captured in a 2015 fruit-bearing field; and the mean number of flies captured in both years. Exponential fit to total fly capture distances in both 2014 and 2015 (Y = 0.019 + 7.438 × e(-0.139 × X), r2 = 0.993, P < 0.0001). Error bars are standard errors. Experiment 3, similar to experiment 2, was conducted in fruit-bearing fields. In total, 13,467 flies were marked and released at an approximate 50:50 sex ratio. The average percentage of flies that survived the marking and dispersed on release was 69.88 ± 3.02% (SE). The sex ratio of those flies that died or were unresponsive during release was 54.48 ± 3.68%. Only one female fly was captured in trial 1, and so the analysis of dispersal was only conducted on trials 2–4. The average trap capture rate based on the flies that survived marking and dispersed was 2.86 ± 0.23% or 189 flies summed across trials 2–4. We found no overall difference in trap captures among the three trials (χ2(2) = 3.685, P = 0.158). The capture rate for flies released within the field was 2.44–3.62%. Flies across trials traveled 7.95–26.32 m per day on average. There was a difference in the capture of males compared with females, but this varied by trial (χ2(2) = 6.557, P = 0.038). There was no difference in distance of trap capture between sexes (sex × distance interaction (χ2(1) = 0.513, P = 0.474). The distance that flies were captured from the release point varied by trial (χ2(2) = 14.084, P = 0.0009). Overall, the distance that flies were trapped from their release point decreased (χ2(1) = 6.080, P = 0.009, slope of distance term = −0.037 ± 0.0143). Figure 7 shows a frequency distribution of the distance moved per day of flies captured in traps over the three trials (estimated by dividing the distance trapped from the release point by the number of days post-release). It can be seen that the majority of flies move less than 20 m per day within a wild blueberry field. Fig. 7. Open in new tabDownload slide Frequency distribution of fly movement distances per day in a 2016 fruit-bearing field. Geometric curve fit to the data (Y = 82.102 × X−0.934, r2 = 0.907, P = 0.003). Fig. 7. Open in new tabDownload slide Frequency distribution of fly movement distances per day in a 2016 fruit-bearing field. Geometric curve fit to the data (Y = 82.102 × X−0.934, r2 = 0.907, P = 0.003). Discussion To improve IPM practices in wild blueberry, we studied optimal trapping methods, reproductive parameters such as diurnal activity and location, and movement within the landscape. When studying optimal trapping methods, we found that trap height above the crop canopy did affect trap capture of adult D. suzukii. Significantly more adult flies were captured in traps 1.2 m above the ground than at the top of the wild blueberry plant canopy. We have no data that describes why this might be the case; however, Drummond et al. (1984) found that the apple maggot fly was captured in higher frequencies when foliage was removed in the direct adjacent vicinity of the trap. This suggests that traps that are more visually apparent capture more flies. Trap visibility might also be a mechanism that determines trap efficiency and thus capture. Fruit volatiles can be very attractive to D. suzukii (Abraham et al. 2015, Keesey et al. 2015). Competition with fruit volatiles emanating from the crop could also be a mechanism that determines trap attraction and thus efficiency. In addition, the physical properties of a volatile bait might make it heavier than air and under certain environmental conditions cause it to sink. Thus, traps closer to the ground may have less olfactory apparency. We do need to be cautious in our overall conclusion derived from our trap height study. Because we did not assess trap height in both the field edge and the field interior, our conclusion of a higher trap capture efficiency in the elevated traps can only be made as it refers to the field edge. This limitation may not be consequential to pest management because growers deploy traps along the field edge. This is because during the previous year, there is no fruit within the field and so D. suzukii adults only colonize fields from the outside. Another aspect of trap location that we found to be significant in wild blueberry was field interior versus edge captures. We found that elevated traps deployed along the field edge consistently caught more flies compared to traps at the crop canopy in the field interior. Although we did not test capture rates in all elevated traps in the edge and the interior, other studies have shown that more D. suzukii are found along field edges compared with interiors, especially during the early fruit ripening stage (Cahenzli et al. 2018). A study in raspberries determined that D. suzukii initially forage on crop perimeters and recommended placing monitoring traps in these areas for early detection (Rice et al. 2017a). Field edges in wild blueberry may act as refugia during hot and dry times of the day, as D. suzukii reproductive success is linked to mild temperatures and humid microclimates (Diepenbrock and Burrack 2017, Evans et al. 2017). To determine optimal trap placement, we have used the information presented in this paper on captures as they relate to trap height, field edge, and field crop status (pruned vs fruit-bearing), so that growers can monitor D. suzukii in Maine wild blueberry efficiently (Drummond et al. 2017). We found that in Maine wild blueberry, activity of flies, based on oviposition and resulting larval infestation of fruit, is diurnal with peak activity in the mornings. Flies are apparently still active in early to mid-afternoon with less activity occurring in the late afternoon to dusk. Hamby et al. (2016) found that D. suzukii in California had a bimodal pattern in the summer, early morning and at dusk, and in the winter was unimodal in activity during the warmest period of the day. This suggests that adult activity varies by temperature stress and they are capable of much plasticity depending on the invaded geographic region. Lin et al. (2014) in Florida found that copulation tended to peak in the morning, as did Revadi et al. (2015) in Europe. However, Lin et al. (2014) found that oviposition occurred at dusk and into the evening (2000–2400 h) but that feeding occurred mostly in the photo-phase periods in the day. Again, these findings suggest that diurnal activity and behavioral responses may depend on abiotic stress conditions. Local patterns of activity of D. suzukii flies may have implications for management (Hamby et al. 2013). Use of nonpersistent insecticides such as pyrethrum (Blackith 1952) or spinosyns (Dripps et al. 2011) might be targeted in Maine wild blueberry in the morning for best control when flies are most actively foraging. Despite wild blueberry being a short shrub (25–40 cm), there is still a vertical architecture to berry dispersion. Flowers are formed from the upper tip of the upright stems to within 2–3 cm of ground level on the bottom of stems. Thus, wild blueberries are typically found on the top of the canopy with almost no foliage shading them to the bottom of the canopy where they are heavily shaded by dense foliage. We investigated this natural fruit dispersion pattern and the response of ovipositing female D. suzukii. We found, based on larval presence in fruit, that 10 times the density of larval infestation is found in fruit at the top of stems compared with fruit at the bottom of stems. This suggests that D. suzukii oviposition behavior is one of skimming along the top of the wild blueberry canopy laying eggs in the fruit located in an area unobstructed by foliage. We did not find any published studies in other fruit crop systems that suggested a similar behavior resulting in a spatial distribution of infested fruit within the shrub or tree canopy. This may have implications in management. If female D. suzukii restrict themselves to the top surface of the canopy, then it implies that penetration of the canopy with an insecticide spray is not as critical as with some pests such as the blueberry spanworm, Itame argillacearia (Packard) (Lepidoptera: Geometridae), that feed within the plant canopy. Many wild blueberry growers in Maine use misting airblast sprayers that provide insecticide coverage 25–30 m out from the tractor-mounted sprayer (Drummond 2003, Collins and Drummond 2004). These sprays tend not to penetrate the canopy, but instead cover the top of the canopy with a dense layer of droplets of fine size. Our research suggests that these sprayers are adequate for management of the D. suzukii. Mark, release, capture studies were conducted between 2014 and 2016 in both pruned and fruit-bearing fields. Our first trial in 2014 suggests that there is no deleterious effect on measuring dispersal with the method of dusting D. suzukii adults with fluorescent dyes; therefore, the release of marked flies can provide a realistic dispersal rate of D. suzukii moving across wild blueberry fields. It is not always possible to test this assumption in these types of studies. We were able to take advantage of conducting a release in a pruned field where, as we have already shown, D. suzukii densities are usually very low. In addition, we were able to release both marked and non-marked flies before any naturally occurring flies could be detected in the field with a high density of traps deployed prior to the release. Several studies have tested the effect of externally applied fluorescent markers, although many have not (Hagler and Jackson 2001). Verhulst et al. (2013) found no effect of using fluorescent markers on mosquitoes, and Dominiak et al. (2010) found no impairment of the flight capability of marked Queensland fruit flies. Wild blueberry fields are unique in their physical topological structure for conducting mark, release, and capture studies. The fields have no crop rows (solid matt of contiguous wild blueberry plants), and so channeling of flies down rows compared with across rows is not a complication in analysis. In addition, the low stature in growth habit of the plant and the apparent behavior of flies skimming across the top of the canopy, as discussed previously, provides a near two-dimensional surface for measuring dispersal. There are other crops that share this attribute such as cranberry, where previously damaged fruits are occasionally attacked by D. suzukii (Steffan et al. 2013), and alfalfa and turf grass, but these crops are not attacked by this pest (Asplen et al. 2015). We need to be cautious in our conclusions because capture rates of released flies were only 2.2–5.7%. The 2014 (experiment 1) release in a nonfruit-bearing pruned field is relevant to the biology of D. suzukii in Maine wild blueberry because almost half of the production acreage in Maine, in any given year, is in the pruned stage (ca. 9,500 ha; NASS 2016). Pruned field borders may serve as overwintering habitat for D. suzukii adults because the fields were fruiting prior to the winter season. In addition, pruned fields are probably traversed when flies search for abundant fruit in crop fields in the summer. Our capture rates combined with the number of released flies do not allow us to estimate directly the number of flies and the distance flown by long-distance dispersing flies. Long-distance dispersal across pruned fields undoubtedly occurs in the wild blueberry ecosystem, as has been reported in other crops ecosystems and across larger geographic landscapes (Cini et al. 2014, Wang et al. 2016). Our decay model depicted in Fig. 5, on extrapolation, suggests that a small proportion of flies can be expected to disperse over a large pruned field (1–2 km). However, on average, our study suggests that within a few days, flies will readily disperse between 0.1 and 30 m in a pruned field, with an average being approximately 5 m. In trials where we released a 50:50 sex ratio we found no evidence to conclude that a difference exists between male and female dispersal distance when considering a short-term measurement period (1–5 d). However, because of the low capture rates that characterized our studies and the limited release quantities of 1,000–2,000 individuals per trial, we lacked statistical power to definitively conclude that there is not a sex difference in dispersal. It could be that over longer periods of measurement, any differential in survival among sexes would result in differences in maximum dispersal between sexes (Diepenbrock et al. 2016). Movement within a crop or fruit-bearing field did not appear to differ from the pattern of dispersal that we saw in a pruned field. We were not able to evaluate this difference directly using a statistical test because the three experiments that focused on dispersal in both pruned and fruit-bearing fields were conducted in different years and locations. Looking at the individual decay rates in dispersal distance from a release point between experiment 1 (pruned field) and experiments 2 and 3 (fruit-bearing field) suggest that distances were similar, between 0.1 and 30 m and an average distance dispersed of between 5 and 10 m. The average distance per day moved by flies in a fruit-bearing field (Fig. 7) is 5.1 m per day. The magnitude of the dispersal rates in wild blueberry supports the potential for field perimeter-based insecticide applications as demonstrated in Florida (Liburd and Iglesias 2013) and used in wild blueberry for blueberry maggot fly, Rhagoletis mendax Curran (Diptera: Tephritidae) (Collins and Drummond 2004). However, depending on the fly population level along a field edge, even a low likelihood of dispersing long distances into the interior of a field may result in fruit infestation by D. suzukii. The immediate colonization by D. suzukii adults of a wild blueberry field sprayed the day previous to our observations suggests that average short distance dispersal rates only represent mean distances and do not capture the potential for rapid infestation of fields, especially if fly dispersal of a small insect like D. suzukii is greatly aided by wind. In conclusion, we found that in the cool summer climate where Maine wild blueberry is grown, D. suzukii appear to be most active in the morning and that they lay eggs mostly in blueberries at the top of the plant canopy. Flies are more abundant in fruit-bearing fields compared with pruned fields, based on trap capture of adults, and that they tend to be most abundant along field edges compared with the interior of fruit-bearing. Traps appear to be most efficient in capturing flies about 1 m above the crop canopy along the field edge than within the crop canopy. Our mark, release, capture experiments suggest that dispersal rates are not different between sexes. We also conclude that dispersal distance on average is at fairly low rates (0.1–30 m) per day and that there appears to be little difference in the dispersal pattern through pruned fields with no fruit and fruit-bearing fields. Whether the propensity of field edges to maintain high population abundance of flies and the low dispersal rates in fruit-bearing fields will make it possible to employ perimeter treatments remains to be seen, but we suggest that a high risk may be associated with this strategy. We hope this new information on optimal trapping methods, reproduction parameters, and movement into and within fields will improve IPM practices in Maine wild blueberry. Acknowledgments This article was greatly improved by the valuable comments and suggestions by the editor and two anonymous reviewers. .We thank EleshaYoung, Hillary Peterson, Nicholas Peterson, Josh Stubbs, and Chris McMannus for helping to conduct the laboratory and field research for this study. We also thank the Maine wild blueberry growers who allowed us to conduct research in their fields. This research was supported by the USDA Specialty Crop Block Grant Program (award CT01A-2013-1023*1659) received from the Maine Department of Agriculture, Conservation, and Forestry, and the USDA National Institute for Food and Agriculture through the Specialty Crop Research Initiative (award 2015-51181-24252). This is Maine Agricultural and Forestry Experiment Station publication number 3642 References Cited Abraham , J. , A. Zhang , S. Angeli , S. Abubeker , C. Michel , Y. Feng , and C. Rodriguez-Saona . 2015 . Behavioral and antennal responses of Drosophila suzukii (Diptera: Drosophilidae) to volatiles from fruit extracts . Environ. Entomol . 44 : 356 – 367 . Google Scholar Crossref Search ADS PubMed WorldCat Alnajjar , G. , J. Collins , and F. A. Drummond . 2017 . Behavioral and preventative management of Drosophila suzukii Matsumura (Diptera: Drosophila) in Maine wild blueberry (Vaccinium angustifolium Aiton) through attract and kill trapping and insect exclusion-netting . Int. J. Entomol. Nematol . 3 : 51 – 61 . WorldCat Alnajjar , G. , F. A. Drummond , and E. Groden . 2018 . Laboratory and field susceptibility of Drosophila suzukii Matsumura (Diptera: Drosophilidae) to entomopathogenic fungal mycoses. J. Agric. Urban Entomol . 33 : 111 – 132 . Google Scholar Crossref Search ADS WorldCat Asplen , M. K. , G. Anfora , A. Biondi , D. S. Choi , D. Chu , K. M. Daane , P. Gibert , A. P. Gutierrez , K. A. Hoelmer , W. D. Hutchison , et al. 2015 . Invasion biology of spotted wing drosophila (Drosophila suzukii): a global perspective and future priorities . J. Pest Sci . 88 : 469 – 494 . Google Scholar Crossref Search ADS WorldCat Atallah , J. , L. Teixeira , R. Salazar , G. Zaragoza , and A. Kopp . 2014 . The making of a pest: the evolution of a fruit-penetrating ovipositor in Drosophila suzukii and related species . Proc. R. Soc. B Biol. Sci . 281 : 9 . Google Scholar Crossref Search ADS WorldCat Bajcz , A. W. , and F. A. Drummond . 2017 . Bearing fruit: flower removal reveals the trade-offs associated with high reproductive effort for wild blueberry . Oecologia 185 : 13 – 26 . Google Scholar Crossref Search ADS PubMed WorldCat Ballman , E. S. , and F. A. Drummond . 2018 . Infestation of wild fruit by Drosophila suzukii surrounding Maine wild blueberry fields . J. Agric. Urban Entomol . 33 : 61 – 70 . Google Scholar Crossref Search ADS WorldCat Ballman , E. S. , J. A. Collins , and F. A. Drummond . 2017 . Predation on Drosophila suzukii (Diptera: Drosophilidae) pupae in Maine wild blueberry fields . J. Econ. Entomol . 110 : 2308 – 2317 . Google Scholar Crossref Search ADS PubMed WorldCat Bellamy , D. E. , M. S. Sisterson , and S. S. Walse . 2013 . Quantifying host potentials: indexing postharvest fresh fruits for spotted wing drosophila, Drosophila suzukii. PLoS One 8 : e61227 . Google Scholar Crossref Search ADS PubMed WorldCat Blackith , R. E . 1952 . Stability of contact insecticides. I—ultra-violet photolysis of the pyrethrins . J. Sci. Food Agric . 3 : 219 – 224 . Google Scholar Crossref Search ADS WorldCat Burrack , H. J. , M. Asplen , L. Bahder , J. Collins , F. A. Drummond , C. Guédot , R. Isaacs , D. Johnson , A. Blanton , J. C. Lee , et al. 2015 . Multistate comparison of attractants for monitoring Drosophila suzukii (Diptera: Drosophilidae) in blueberries and caneberries . Environ. Entomol . 44 : 704 – 712 . Google Scholar Crossref Search ADS PubMed WorldCat Cahenzli , F. , I. Bühlmann , C. Daniel , and J. Fahrentrapp . 2018 . The distance between forests and crops affects the abundance of Drosophila suzukii during fruit ripening, but not during harvest . Environ. Entomol . 47 : 1274 – 1279 . Google Scholar Crossref Search ADS PubMed WorldCat Chabert , S. , R. Allemand , M. Poyet , P. Eslin , and P. Gibert . 2012 . Ability of European parasitoids (Hymenoptera) to control a new invasive Asiatic pest, Drosophila suzukii . Biol. Control 63 : 40 – 47 . Google Scholar Crossref Search ADS WorldCat Chiasson , G. , and J. Argall . 2010 . Growth and development of lowbush blueberry . New Brunswick Department of Agriculture and Rural Development . Factsheet A.2.0. Google Preview WorldCat COPAC Cini , A. , C. Ioriatti , and G. Anfora . 2012 . A review of the invasion of Drosophila suzukii in Europe and a draft research agenda for integrated pest management . Bull. Insectol . 65 : 149 – 160 . WorldCat Cini , A. , G. Anfora , L. A. Escudero-Colomar , A. Grassi , U. Santosuosso , G. Seljak , and A. Papini . 2014 . Tracking the invasion of the alien fruit pest Drosophila suzukii in Europe . J. Pest Sci . 87 : 559 – 566 . Google Scholar Crossref Search ADS WorldCat Collins , J. A. , and F. A. Drummond . 2004 . Field-edge based management tactics for blueberry maggot in lowbush blueberry . Small Fruits Rev . 3 : 283 – 293 . Google Scholar Crossref Search ADS WorldCat Cupers , G. W. , P. G. Mulder , and T. A. Royer . 2000 . Implementation of ecologically-based IPM, pp. 171 – 204 . In J. E. Rechcigl and N. A. Rechcigl (eds.), Insect pest management . CABI International , Oxfordshire, United Kingdom . Google Preview WorldCat COPAC Deprá , M. , J. L. Poppe , H. J. Schmitz , D. C. De Toni , and V. L. S. Valente . 2014 . The first records of the invasive pest Drosophila suzukii in the South American continent . J. Pest Sci . 87 : 379 – 383 . Google Scholar Crossref Search ADS WorldCat Diepenbrock , L. M. , and H. J. Burrack . 2017 . Variation of within-crop microhabitat use by Drosophila suzukii (Diptera: Drosophilidae) in blackberry . J. Appl. Entomol . 141 : 1 – 7 . Google Scholar Crossref Search ADS WorldCat Diepenbrock , L. M. , K. A. Swoboda-Bhattarai , and H. J. Burrack . 2016 . Ovipositional preference, fidelity, and fitness of Drosophila suzukii in a co-occurring crop and non-crop host system . J. Pest Sci . 89 : 761 – 769 . Google Scholar Crossref Search ADS WorldCat Dominiak , B. C. , S. Sundaralingam , L. Jiang , A. J. Jessup , and I. M. Barchia . 2010 . Impact of marker dye on adult eclosion and flight ability of mass produced Queensland fruit fly Bactrocera tryoni (Froggatt) (Diptera: Tephritidae) . Aust. J. Entomol . 49 : 166 – 169 . Google Scholar Crossref Search ADS WorldCat Dreves , A. J. , and G. A. Langellotto-Rhodaback . 2011 . Protecting garden fruits from spotted wing drosophila . Oregon State University Extension Fact Sheet EM 9026 . http://mkwc.org/files/4513/8907/1042/Drosophila-Oregon-State.pdf (accessed 8 March 2019 ). Dripps , J. E. , R. E. Boucher , A. Chloridis , C. B. Cleveland , C. V. DeAmicis , L. E. Gomez , D. L. Paroonagian , L. A. Pavan , T. C. Sparks , and G. B. Watson . 2011 . The spinosyns insecticides, pp. 163 – 212 . In O. Lopez , J. Fernandez , and J. G. Bolanos (eds.), Trends in insect control . Royal Society of Chemistry , Cambridge, United Kingdom . Google Preview WorldCat COPAC Drummond , F. A . 2003 . Perimeter treatment with Imidan for control of the blueberry maggot, Rhagoletis mendax, pp. 121 – 135 . In Proceedings of the 9th International Symposium on Fruit Flies Biology . B. Sabater-Munoz , T. Vera , R. Pereira , (eds). Bangkok, Thailand , May 2014, 447 pp. ISBN: 978-616-358-207-2 Google Preview WorldCat COPAC Drummond , F. A. , E. Groden , and R. J. Prokopy . 1984 . Comparative efficacy and optimal positioning of traps for monitoring apple maggot flies (Diptera: Tephritidae) . Environ. Entomol . 13 : 232 – 235 . Google Scholar Crossref Search ADS WorldCat Drummond , F.A. , J. Collins , and E. Ballman . 2018 . Spotted wing Drosophila: Pest biology and IPM recommendations for wild blueberries . Univ. Maine Coop. Ext . Fact Sheet 210, 6 pp. https://extension.umaine.edu/blueberries/factsheets/insects/210-spotted-wing-drosophila/ (accessed 8 March 2019 ). WorldCat Drummond , F. A. , E. Ballman , J. Collins and D. Yarborough . 2017 . Spotted wing drosophila: pest biology and IPM recommendations for wild blueberry . University of Maine Cooperative Extension Factsheet 210. University of Maine , Orono, ME , 7 pp. Google Preview WorldCat COPAC Drummond , F.A. , J.A. , Collins , G. Al-Najjar , and J. Christensen . 2019 . Itty-bitty traps for monitoring spotted wing Drosophila (Drosophila suzukii Matsumura), does size matter? In Proceedings of the North American Blueberry Research and Extension Workers Conference . August 12–15, 2018, Orono, ME . 9 pp. University of Maine Digital Commons . https://digitalcommons.library.umaine.edu/cgi/viewcontent.cgi?article=1075&context=nabrew2018 (accessed 8 March 2019 ). Google Preview WorldCat COPAC Evans , R. K. , M. D. Toews , and A. A. Sial . 2017 . Diel periodicity of Drosophila suzukii (Diptera: Drosophilidae) under field conditions . PLoS One 12 : 20 . WorldCat Fernandez-Cornejo , J. , and S. Jans . 1999 . Pest Management in U.S. agriculture . Resource Economics Division, Economic Research Service, U.S. Department of Agriculture , Washington, DC . Agricultural Handbook No. 717. Google Preview WorldCat COPAC Firth , D . 1993 . Bias reduction of maximum likelihood estimates . Biometrika 80 : 27 – 38 . Google Scholar Crossref Search ADS WorldCat Gerdeman , B. S. , L. K. Tanigoshi , and G. Hollis Spitler . 2011 . Spotted wing drosophila (SWD) monitoring, identifying, and fruit sampling . Washington State University Extension Fact Sheet FS049E . http://cru.cahe.wsu.edu/CEPublications/FS049E/FS049E.pdf (accessed 8 March 2019 ). Hagler , J. R. , and C. G. Jackson . 2001 . Methods for marking insects: current techniques and future prospects . Annu. Rev. Entomol . 46 : 511 – 543 . Google Scholar Crossref Search ADS PubMed WorldCat Hall , D. B . 2000 . Zero-inflated Poisson and binomial regression with random effects: a case study . Biometrics 56 : 1030 – 1039 . Google Scholar Crossref Search ADS PubMed WorldCat Hamby , K. A. , R. S. Kwok , F. G. Zalom , and J. C. Chiu . 2013 . Integrating circadian activity and gene expression profiles to predict chronotoxicity of Drosophila suzukii response to insecticides . PLoS One 8 : e68472 . Google Scholar Crossref Search ADS PubMed WorldCat Hamby , K. A. , D. E. Bellamy , J. C. Chiu , J. C. Lee , V. M. Walton , N. G. Wiman , R. M. York , and A. Biondi . 2016 . Biotic and abiotic factors impacting development, behavior, phenology, and reproductive biology of Drosophila suzukii. J. Pest Sci . 89 : 605 – 619 . Google Scholar Crossref Search ADS WorldCat Hampton , E. , C. Koski , O. Barsoian , H. Faubert , R. S. Cowles , and S. R. Alm . 2014 . Use of early ripening cultivars to avoid infestation and mass trapping to manage Drosophila suzukii (Diptera: Drosophilidae) in Vaccinium corymbosum (Ericales: Ericaceae) . J. Econ. Entomol . 107 : 1849 – 1857 . Google Scholar Crossref Search ADS PubMed WorldCat Hauser , M . 2011 . A historic account of the invasion of Drosophila suzukii (Matsumura) (Diptera: Drosophilidae) in the continental United States, with remarks on their identification . Pest Manag. Sci . 67 : 1352 – 1357 . Google Scholar Crossref Search ADS PubMed WorldCat Jones , M. S. , H. Vanhanen , R. Peltola , and F. A. Drummond . 2014 . A global review of arthropod-mediated ecosystem-services in Vaccinium berry agroecosystems . Terr. Arthro. Rev . 7 : 41 – 78 . Google Scholar Crossref Search ADS WorldCat Karageorgi , M. , L. B. Bräcker , S. Lebreton , C. Minervino , M. Cavey , K. P. Siju , I. C. Grunwald Kadow , N. Gompel , and B. Prud’homme . 2017 . Evolution of multiple sensory systems drives novel egg-laying behavior in the fruit pest Drosophila suzukii . Curr. Biol . 27 : 847 – 853 . Google Scholar Crossref Search ADS PubMed WorldCat Karuppuchamy , S. V. , and S. Venugopal . 2016 . Integrated pest management, pp. 651 – 684 . In Omkar (ed.), Ecofriendly pest management for food security . Elsevier Inc. , San Diego, CA . 762 pp. ISBN: 9780128032657. Google Preview WorldCat COPAC Keesey , I. W. , M. Knaden , and B. S. Hansson . 2015 . Olfactory specialization in Drosophila suzukii supports an ecological shift in host preference from rotten to fresh fruit . J. Chem. Ecol . 41 : 121 – 128 . Google Scholar Crossref Search ADS PubMed WorldCat Kinjo , H. , Y. Kunimi , T. Ban , and M. Nakai . 2012 . Oviposition efficacy of Drosophila suzukii (Diptera: Drosophilidae) on different cultivars of blueberry . J. Econ. Entomol . 106 : 1767 – 1771 . Google Scholar Crossref Search ADS WorldCat Kirkpatrick , D. M. , P. S. McGhee , L. J. Gut , and J. R. Miller . 2017 . Improving monitoring tools for spotted wing drosophila, Drosophila suzukii . Entomol. Exp. Appl . 164 : 87 – 93 . Google Scholar Crossref Search ADS WorldCat Kirkpatrick , D. M. , L. J. Gut , and J. R. Miller . 2018 . Estimating monitoring trap plume reach and trapping area for Drosophila suzukii (Diptera: Drosophilidae) in Michigan tart cherry . J. Econ. Entomol . 111 : 1285 – 1289 . Google Scholar Crossref Search ADS PubMed WorldCat Klick , J. , W. Q. Yang , V. M. Walton , D. T. Dalton , J. R. Hagler , A. J. Dreves , J. C. Lee , and D. J. Bruck . 2016 . Distribution and activity of Drosophila suzukii in cultivated raspberry and surrounding vegetation . J. Appl. Entomol . 140 : 37 – 46 . Google Scholar Crossref Search ADS WorldCat Knoll , V. , T. Ellenbroek , J. Romeis , and J. Collatz . 2017 . Seasonal and regional presence of hymenopteran parasitoids of Drosophila in Switzerland and their ability to parasitize the invasive Drosophila suzukii. Sci. Rep . 7 : 11 . Google Scholar Crossref Search ADS PubMed WorldCat Leach , H. , J. Moses , E. Hanson , P. Fanning , and R. Isaacs . 2018 . Rapid harvest schedules and fruit removal as non-chemical approaches for managing spotted wing drosophila . J. Pest Sci . 91 : 219 – 226 . Google Scholar Crossref Search ADS WorldCat Lee , J. C. , D. J. Bruck , H. Curry , D. Edwards , D. R. Haviland , R. A. Van Steenwyk , and B. M. Yorgey . 2011 . The susceptibility of small fruits and cherries to the spotted-wing drosophila, Drosophila suzukii . Pest Manag. Sci . 67 : 1358 – 1367 . Google Scholar Crossref Search ADS PubMed WorldCat Lee , J. C. , H. J. Burrack , L. D. Barrantes , E. H. Beers , A. J. Dreves , K. A. Hamby , D. R. Haviland , R. Isaacs , T. A. Richardson , P. W. Shearer , C. A. Stanley , D. B. Walsh , V. M. Walton , F. G. Zalom , and D. J. Bruck . 2012 . Evaluation of monitoring traps for Drosophila suzukii (Diptera: Drosophilidae) in North America . J. Econ. Entomol . 105 : 1350 – 1357 . Google Scholar Crossref Search ADS PubMed WorldCat Lee , J. C. , P. W. Shearer , L. D. Barrantes , E. H. Beers , H. J. Burrack , D. T. Dalton , A. J. Dreves , L. J. Gut , K. A. Hamby , D. R. Haviland , et al. 2013 . Trap designs for monitoring Drosophila suzukii (Diptera: Drosophilidae) . Environ. Entomol . 42 : 1348 – 1355 . Google Scholar Crossref Search ADS PubMed WorldCat Lee , J. C. , A. J. Dreves , A. M. Cave , S. Kawai , R. Isaacs , J. C. Miller , S. Van Timmeren , and D. J. Bruck . 2015 . Infestation of wild and ornamental noncrop fruits by Drosophila suzukii (Diptera: Drosophilidae) . Ann. Entomol. Soc. Am . 108 : 117 – 129 . Google Scholar Crossref Search ADS WorldCat Liburd , O. E. , and L. E. Iglesias . 2013 . Spotted wing drosophila: pest management recommendations for Florida blueberries . University of Florida , Gainsville, FL . Google Preview WorldCat COPAC Lin , Q. C. , Y. F. Zhai , C. G. Zhou , L. L. Li , Q. Y. Zhuang , X. Y. Zhang , F. G. Zalom , and Y. Yu . 2014 . Behavioral rhythms of Drosophila suzukii and Drosophila melanogaster . Fla. Entomol . 97 : 1424 – 1433 . Google Scholar Crossref Search ADS WorldCat Little , C. M. , T. W. Chapman , D. L. Moreau , and N. K. Hillier . 2017 . Susceptibility of selected boreal fruits and berries to the invasive pest Drosophila suzukii (Diptera: Drosophilidae) . Pest Manag. Sci . 73 : 160 – 166 . Google Scholar Crossref Search ADS PubMed WorldCat Miller , B. , G. Anfora , M. Buffington , K. M. Daane , D. T. Dalton , K. M. Hoelmer , M. V. R. Stacconi , A. Grassi , C. Ioriatti , A. Loni , J. C. Miller , M. Ouantar , X. G. Wang , N. G. Wiman , and V. M. Walton . 2015 . Seasonal occurrence of resident parasitoids associated with Drosophila suzukii in two small fruit production regions of Italy and the USA . Bull. Insectol . 68 : 255 – 263 . WorldCat (NASS) National Agricultural Statistics Service . 2016 . New England Agricultural Statistics 2015 . USDA National Agricultural Statistics Service, New England Field Office , Concord, NH . Google Preview WorldCat COPAC Pedigo , K. P. , S. H. Hutchins , and L. G. Higley . 1986 . Economic injury levels in theory and practice . Ann. Rev. Entomol . 31 : 341 – 368 . Google Scholar Crossref Search ADS WorldCat Poyet , M. , V. Le Roux , P. Gibert , A. Meirland , G. Prevost , P. Eslin , and O. Chabrerie . 2015 . The wide potential trophic niche of the Asiatic fruit fly Drosophila suzukii: the key of its invasion success in temperate Europe? PLoS One 10 : 26 . Google Scholar Crossref Search ADS WorldCat Qu , H. , and F. A. Drummond . 2018 . Simulation-based modeling of wild blueberry pollination . Comput. Electron. Agric . 144 : 94 – 101 . Google Scholar Crossref Search ADS WorldCat Renkema , J. M. , R. Buitenhuis , and R. H. Hallett . 2014 . Optimizing trap design and trapping protocols for Drosophila suzukii (Diptera: Drosophilidae) . J. Econ. Entomol . 107 : 2107 – 2118 . Google Scholar Crossref Search ADS PubMed WorldCat Renkema , J. M. , L. E. Iglesias , P. Bonneau , and O. E. Liburd . 2018 . Trapping system comparisons for and factors affecting populations of Drosophila suzukii and Zaprionus indianus in winter-grown strawberry . Pest Manag. Sci . 74 : 2076 – 2088 . Google Scholar Crossref Search ADS WorldCat Revadi , S. , S. Lebreton , P. Witzgall , G. Anfora , T. Dekker , and P. G. Becher . 2015 . Sexual behavior of Drosophila suzukii . Insects 6 : 183 – 196 . Google Scholar Crossref Search ADS PubMed WorldCat Rice , K. B. , S. K. Jones , W. Morrison , and T. C. Leskey . 2017a . Spotted wing drosophila prefer low hanging fruit: insights into foraging behavior and management strategies . J. Insect Behav . 30 : 645 – 661 . Google Scholar Crossref Search ADS WorldCat Rice , K. B. , B. D. Short , and T. C. Leskey . 2017b . Development of an attract-and-kill strategy for Drosophila suzukii (Diptera: Drosophilidae): evaluation of Attracticidal Spheres Under Laboratory and Field Conditions . J. Econ. Entomol . 110 : 535 – 542 . Google Scholar Crossref Search ADS WorldCat SAS Institute . 2017 . JMP® Version 14 . SAS Institute Inc. , Cary, NC , 1989 – 2007 . Google Preview WorldCat COPAC Shapiro , S. S. , and M. B. Wilk . 1965 . An analysis of variance test for normality (complete samples) . Biometrika 52 : 591 – 611 . Google Scholar Crossref Search ADS WorldCat Spears , L. R. , C. Cannon , D. G. Alston , R. S. Davis , C. Stanley-Stahr , and R. A. Ramirez . 2017 . Spotted wing drosophila (Drosophila suzukii) . Utah State University Extension Fact Sheet ENT-187-17 . https://digitalcommons.usu.edu/extension_curall/1787 (accessed 9 March 2019 ). Stacconi , M. V. R. , A. Panel , N. Baser , C. Ioriatti , T. Pantezzi , and G. Anfora . 2017 . Comparative life history traits of indigenous Italian parasitoids of Drosophila suzukii and their effectiveness at different temperatures . Biol. Control 112 : 20 – 27 . Google Scholar Crossref Search ADS WorldCat Steffan , S. A. , J. C. Lee , M. E. Singleton , A. Vilaire , D. B. Walsh , L. S. Lavine , and K. Patten . 2013 . Susceptibility of cranberries to Drosophila suzukii (Diptera: Drosophilidae) . J. Econ. Entomol . 106 : 2424 – 2427 . Google Scholar Crossref Search ADS PubMed WorldCat Stockton , D. G. , A. Wallingford , D. Rendon , P. Fanning , C. K. Green , L. Diepenbrock , E. Ballman , V. Walton , R. Isaacs , H. Leach , A. A. Sial , F. Drummond , H. Burrack , and G. M. Loeb . 2019 . Interactions Between Biotic and Abiotic Factors Affect Survival in Overwintering Drosophila suzukii (Diptera: Drosophilidae) . Environ. Entomol . doi:. WorldCat Crossref Tochen , S. , D. T. Dalton , N. Wiman , C. Hamm , P. W. Shearer , and V. M. Walton . 2014 . Temperature-related development and population parameters for Drosophila suzukii (Diptera: Drosophilidae) on cherry and blueberry . Environ. Entomol . 43 : 501 – 510 . Google Scholar Crossref Search ADS PubMed WorldCat Van den Bosch , R. , and V. M. Stern . 1962 . The integration of chemical and biological control of arthropod pests . Annu. Rev. Entomol . 7 : 367 – 386 . Google Scholar Crossref Search ADS PubMed WorldCat Van Steenwyk , R. A. and M. P. Bolda . 2015 . Spotted wing drosophila: devastating effects on cherry and berry pest management . Acta Hortic . 1105 , 11 – 18 doi: 10.17660/Acta Hortic.2015.1105.2 Google Scholar Crossref Search ADS WorldCat Verhulst , N. O. , J. A. Loonen , and W. Takken . 2013 . Advances in methods for colour marking of mosquitoes . Parasit. Vectors 6 : 200 . Google Scholar Crossref Search ADS PubMed WorldCat Wallingford , A. K. , D. H. Cha , and G. M. Loeb . 2018 . Evaluating a push-pull strategy for management of Drosophila suzukii Matsumura in red raspberry . Pest Manag. Sci . 74 : 120 – 125 . Google Scholar Crossref Search ADS PubMed WorldCat Walton , V.M. , H.J. Burrack , D.T. Dalton , R. Isaacs , N. Wiman , and C. Ioriatti . 2016 . Past, present and future of Drosophila suzukii: distribution, impact and management in United States berry fruits . Acta Hortic . 1117 : 87 – 94 . doi:10.17660/Acta Hortic.2016.1117.16 Google Scholar Crossref Search ADS WorldCat Wang , X. G. , T. J. Stewart , A. Biondi , B. A. Chavez , C. Ingels , J. Caprile , J. A. Grant , V. M. Walton , and K. M. Daane . 2016 . Population dynamics and ecology of Drosophila suzukii in Central California . J. Pest Sci . 89 : 701 – 712 . Google Scholar Crossref Search ADS WorldCat Woltz , J. M. , and J. C. Lee . 2017 . Pupation behavior and larval and pupal biocontrol of Drosophila suzukii in the field . Biol. Control 110 : 62 – 69 . Google Scholar Crossref Search ADS WorldCat Woltz , J. M. , K. M. Donahue , D. J. Bruck , and J. C. Lee . 2015 . Efficacy of commercially available predators, nematodes and fungal entomopathogens for augmentative control of Drosophila suzukii . J. Appl. Entomol . 139 : 759 – 770 . Google Scholar Crossref Search ADS WorldCat Yarborough , D. E . 2009 . Wild blueberry culture in Maine . University of Maine Cooperative Extension Fact Sheet No. 220. University of Maine , Orono, ME . Google Preview WorldCat COPAC Yarborough , D. , F. Drummond , S. Annis , and J. D’Appollonio . 2017 . Maine wild blueberry systems analysis . Acta Hort . 1180 : 151 – 160 . Google Scholar Crossref Search ADS WorldCat Zhu , C. J. , J. Li , H. Wang , M. Zhang , and H. Y. Hu . 2017 . Demographic potential of the pupal parasitoid Trichopria drosophilae (Hymenoptera: Diapriidae) reared on Drosophila suzukii (Diptera: Drosophilidae) . J. Asia-Pac. Entomol . 20 : 747 – 751 . Google Scholar Crossref Search ADS WorldCat © The Author(s) 2019. Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/open_access/funder_policies/chorus/standard_publication_model)
TI - Spotted-Wing Drosophila (Diptera: Drosophilidae) Adult Movement, Activity, and Oviposition Behavior in Maine Wild Blueberry (Vaccinium angustifolium; Ericales: Ericaceae)
JF - Journal of Economic Entomology
DO - 10.1093/jee/toz059
DA - 2019-08-03
UR - https://www.deepdyve.com/lp/oxford-university-press/spotted-wing-drosophila-diptera-drosophilidae-adult-movement-activity-kHLpf147Nf
SP - 1623
VL - 112
IS - 4
DP - DeepDyve
ER -