Introduction

Western cherry fruit fly, Rhagoletis indifferens Curran (Diptera: Tephritidae), is an economically important quarantine pest of sweet cherry, Prunus avium L. (L.), as well as a pest of tart cherry, P. cerasus L., in western North America (Frick et al. 1954). There is zero tolerance for larvae in fresh market sweet and canned tart cherries due to strict consumer standards (State of Washington Department of Agriculture, Permanent Order No. 1099, effective 30 September 1968) (Smith and Kupferman 2003). Since about 2005 (Yee and Chapman 2005; Warner 2008), the fly has been managed in Washington [which produces 55% of fresh market cherries in the U.S. (Smith and Kupferman 2003)] and other cherry-producing areas using mostly spinosad bait sprays (GF-120® NF Naturalyte®, Dow AgroSciences, Indianapolis, IN) rather than cover sprays. Spinosad bait is applied weekly, or reapplied after rainfall, to kill flies before they are able to lay eggs in fruit, which first occurs when flies are ~7 days old (Frick et al. 1954). Commercial cherry orchards are generally free of infestations, and larval finds in commercial cherries have become rare in recent years. Nevertheless, sprays are applied to orchards as insurance. Growers like using spinosad bait because it is easy to apply, relatively inexpensive, efficacious, and organic.

Spotted wing drosophila, Drosophila suzukii Matsumura, was first detected in the U.S. in California in 2008 and is potentially a major pest of cherry (Caprile et al. 2010) that could be a threat to orchards at the same time as R. indifferens. It was first discovered in eastern Washington in June 2010 (Beers et al. 2010) and in northern Utah in August 2010 (Stanley-Vorel et al. 2010). In Utah, adults were caught in a tart cherry orchard post-harvest where many fruits were still on the trees (D.G.A., personal observation). Drosophila suzukii is a major concern for cherry growers because it attacks whole intact cherries, whereas most Drosophila species attack only damaged and over-ripe fruit (Caprile et al. 2010). Unlike R. indifferens, D. suzukii apparently is not controlled using low volume spinosad bait sprays (Van Steenwyk 2011). Current data suggest that D. suzukii is a late season pest (Beers et al. 2011), so spinosad bait could still be used against R. indifferens early in the cherry season. However, near harvest or in cooler environments with late-season cherry varieties, alternative materials to spinosad bait may be needed to protect fruit from D. suzukii infestations. Neonicotinoid insecticides that are effective against R. indifferens apparently are also relatively ineffective against D. suzukii (Van Steenwyk 2011).

Insecticides for control of both D. suzukii and R. indifferens need to be identified quickly to prevent economic losses while integrated pest management (IPM) strategies for cherries are revised. In early tests of 28 available insecticides (Oregon State University 2010), three were identified as being potentially effective against D. suzukii: malathion (an organophosphate), zeta-cypermethrin (a pyrethroid), and spinetoram (a spinosyn) (Walsh et al. 2010; Tanigoshi et al. 2010; Van Steenwyk 2011). These materials are also registered for use against R. indifferens (Dow AgroSciences 2009; FMC Corp. 2009; Micro Flo Company 2011), but how well they protect fruit against reproductively mature flies is not known. Many insecticides can be used to kill R. indifferens during the first week to 10 days after fly emergence, including malathion (Zwick et al. 1970). However, once females are reproductively mature, rapid mortality is likely required to prevent egg-laying. Insecticides such as spinosad and neonicotinoids cannot kill all flies fast enough to prevent egg-laying in cherries even after insecticides are ingested in bait (Yee 2010).

Cover sprays or contact with residues of malathion, zeta-cypermethrin, and spinetoram may vary in their effects on killing flies quickly, and thus preventing egg laying. Based on effects of these or related materials on other insects (e.g., Rothwell et al. 1998; Braham et al. 2007; Dripps et al. 2008; Aheer et al. 2009; Conway and Forrester 2011) and their different mechanisms of action (Brown 2006), it can be predicted that the three insecticides cause different rates of mortality and thus possess differential potential to prevent oviposition of R. indifferens. Materials that cause quick mortality would be expected to reduce oviposition more than slower-acting materials, even if differences are only a few hours.

The main objectives of this study were to determine behavioral responses, rate of mortality, and oviposition of reproductively mature female R. indifferens exposed to malathion, zeta-cypermethrin, and spinetoram. The hypothesis that none of the insecticides is repellent and that adults are equally likely to contact surfaces treated with them was tested. The hypothesis that zeta-cypermethrin is more effective at reducing oviposition than malathion and spinetoram because of its faster knockdown ability was also tested. Effects of both residual and direct spray contact were assessed. Based on the results, scenarios for effective field control using materials targeted against both D. suzukii and R. indifferens are presented.

Materials and methods

Source and maintenance of flies

Rhagoletis indifferens flies used in studies originated as eggs or larvae in sweet cherries collected from the field in Richland and Kennewick, Benton County, Washington, in June 2010. Cherries were placed on hardware cloth suspended above soil in plastic tubs. Puparia were stored in moist soil inside 0.473-l plastic cups (11.6-cm diameter and 7.5-cm high) held at 3–4°C for 6–7 months. Puparia were transferred to 26–27°C and a 16 h:8 h L:D photoperiod for adult emergence. Flies were maintained inside 1.9-l containers (10.2-cm diameter and 16.2-cm high) with food (dry 20% yeast extract and 80% sucrose) and water upon emergence. Thirty males and 30 females were held inside each container to allow mating. In all experiments, 12- to 20-day-old females were used because these represented reproductively mature flies that were capable of laying eggs. Flies were not exposed to cherries before any experiment.

Insecticides

Malathion [Malathion, 50% a.i. by weight (515 g a.i./l), Spectrum Group, St. Louis, MO] (EPA Reg. No. 46515-19-8845), zeta-cypermethrin [Mustang Max™ EC, 9.6% a.i. by weight (96 g a.i./l), FMC Corp., West Point, GA] (EPA Reg No. 279-3327), and spinetoram (spinosyn J) (Delegate™ WG, 25% spinetoram, Dow AgroSciences, Indianapolis, IN) (EPA Reg. No. 62719-541) were tested. Deionized water was used as the control. In the first experiment, a control and high label rates of each of the three insecticides were tested. In the second, third, and fourth experiments, a control and low and high rate of each of the three insecticides were tested. The low and high rates were determined by the manufacturers and stated on the specimen labels. The low rate of malathion was 0.236 l/935 l/ha (118 g a.i./ha); the high rate was 0.473 l/935 l/ha (236 g a.i./ha). The low rate of zeta-cypermethrin was 0.038 l/935 l/ha (3.6 g a.i./ha); the high rate was 0.118 l/935 l/ha (11.3 g a.i./ha). The low rate of spinetoram was 127.6 g/935 l/ha (31.9 g a.i./ha); the high rate was 198.4 g/935 l/ha (49.6 g a.i./ha). All insecticides were mixed in deionized water.

Behavioral responses of flies to dried residues on cherries

To determine if the different insecticide residues on fruit repelled flies from landing on them or affected the flies’ behaviors in other ways, observations were conducted of individual flies exposed to a single control or treated cherry. Cherries used in all experiments were variety “Bing,” 2.5–2.7 cm in diameter, and were obtained from Chile in January 2011 and stored at 1.6°C for 1–4 weeks until testing. Cherries were rinsed with tap water, dried, and held at 20–22°C for 2 h before being treated with insecticides. Cherries were dipped for 2–3 s in water or high rates of insecticide solution, and then left to dry for 20 h at 20–22°C. A single female fly was introduced into an inverted 296-ml clear plastic cup (7.8-cm diameter tapering to 5.1- and 10.0-cm high) on a sheet of white paper. The cup had ten 1.05 mm holes on top for ventilation. A single control or treated cherry was then placed underneath the cup, and the fly observed continuously for 2 h. Timings of first and subsequent landings on the cherry were recorded, as was feeding (grazing), stinging or oviposition behavior, and paralysis or mortality. One landing was defined as continuous occupation of the cherry, including stinging events. A separate landing occurred when the fly left the cherry but then came back. Observations were made at 20–21°C under bright fluorescent light. Cherries were collected at the end of observations. Cherries were stored in 70% ethanol and eggs beneath the skin were later counted under a microscope. Flies were left in the cups, provided with food and water, and then held at 26–27°C and 16 h:8 h L:D for 24 h to assess mortality. A fly was considered dead if it could not walk straight when it was probed, even if its legs twitched or it tried to walk. Thirty-six flies were tested for the control and each insecticide treatment (six flies per day over 6 days).

Effects of dried residues on cherries on mortality and oviposition

This experiment determined mortality and oviposition of flies that were exposed to dried insecticide residues on cherries. Individual cherries were dipped into low or high rates of insecticide solutions for 2–3 s and allowed to dry as in the previous experiment. Ten control or insecticide-treated cherries were placed on an 11.8-cm diameter and 1.0-cm high plastic lid, and the lid was placed on the bottom of a 1.9-l container (same type used to hold flies before testing) with food and water at 16 h:8 h L:D, 26–27°C, and 30–45% RH. Then, 15 flies were introduced into each control or treatment container. Fly mortality was recorded at 2, 4, 6, and 24 h after exposure to insecticide-treated cherries. Numbers of dead flies were recorded at each time interval. Cherries were examined for eggs as in the behavior study. Flies were left in containers for an additional 24 h to make certain they were dead. There were five replicates of the control and each treatment (one complete set of the control and all treatments run on a single day).

Effects of contact with dried residues followed by exposure to dried residues on cherries on mortality and oviposition

This experiment determined mortality and oviposition of flies that walked on dried insecticide residues before being exposed to dried residues on cherries. This exposure simulates flies walking on treated leaves and stems before moving to fruits. Two ml of insecticide solution was applied into a 11.5-cm diameter and 4.3-cm high clear plastic container using a Potter Precision Laboratory Spray Tower (Burkhard Manufacturing Co Ltd. Rickmansworth Herts, England) (Potter 1952) so that uniform spray coverage was obtained. The tower had a spray cone width of 11.7 cm at the bottom, a nozzle with an orifice diameter of 0.65 mm, and delivered solutions at 1.8 kg/cm2 (10 psi) into the container. The container had a hole on its side to introduce flies. The container was placed on a circular platform 8.89 cm beneath the bottom of the spray cone. The platform of the spray tower automatically rose 5.08 cm toward the spray cone during spraying, resulting in a space of 3.81 cm between it and the container. Because the container was 4.3-cm high and 11.5-cm wide and the cone was 11.7-cm wide, the container moved up 0.49 cm into the bottom of the spray cone. This left only a 0.2-cm wide gap between the cone and container and caused most of the spray to back up into the cone, resulting in less spray coverage than if there were more space between the cone bottom and container (see below). The lid for the container was 11.8 cm in diameter and 1.0-cm high, and the bottom of it was also sprayed so that when containers were sealed, flies inside had continuous contact with residues. Ten cherries were placed on an 11.8-cm diameter and 1.0-cm high lid and sprayed with 2 ml of water or insecticide solution. The distance between the bottom of the spray cone and lid was 3.81 cm. After 24 h, the cherries were placed in a 1.9-l test container. Fifteen unsprayed flies were introduced into the container with dried insecticide residues for 20–25 min at 26–27°C. Flies from each container were then released inside a 30 cm3 screen cage, recaptured within 5 min, and introduced into a 1.9-l container with treated cherries. Mortality and oviposition were followed as in the second experiment. There were five replicates of the control and each treatment.

To document spray coverage (dried residues, 2 ml spray), three yellow Teejet® water and oil sensitive papers (each 26 mm × 76 mm) (Spraying Systems Co.®, Wheaton, IL) were placed inside an 11.5-cm diameter and 4.3-cm high container and on an 11.8-cm diameter and 1.0-cm high lid beneath the spray tower and sprayed with 2 ml of water (which should result in the same patterns as using the insecticide solutions). All spots within one 0.25 cm2 area on each of the three papers were counted. Twenty representative spots on the papers were measured as an indication of spray droplet size. Discrete spots or splotches were measured at their widest diameters, avoiding drops that bled into each other.

Effects of direct sprays and exposure to insecticide-treated cherries on mortality and oviposition

This experiment determined mortality and oviposition of flies that were directly sprayed with insecticide, and then exposed to cherries with fresh insecticide. Fifteen flies were held inside each 0.473-l paper container with food and water the day before insecticide exposure. On test day, flies were chilled at 0.6–1.7°C for 20–30 min to immobilize them. While flies were being chilled, water or insecticide was applied onto 10 cherries placed on a 11.8-cm diameter and 1.0-cm high plastic lid using the spray tower as previously described. Two separate tests were performed, one with 1 ml of spray and the other with 2 ml (both on flies and cherries). The cherries on the lid were placed onto the bottom of a 1.9-l test container immediately after being sprayed. The immobilized flies were then removed from chilling and placed onto a 9.0-cm wide and 1.6-cm high plastic dish and sprayed with water or insecticide using the spray tower. The bottom of the spray cone was 3.81 cm above the dish with flies. The flies were transferred into the test container with cherries. Mortality and oviposition data were gathered as in the previous two experiments. There were five replicates of the control and each treatment. Water-sensitive papers placed on 11.8-cm diameter and 1.0-cm high lids were used to document spray coverage from the 1 and 2 ml sprays. As when cherries and flies were directly sprayed, the distance between the spray cone and bottom of lids was 3.81 cm.

Statistics

None of the data gathered in this study was normally distributed and/or had equal variances despite data transformations (arcsine-square-root for percent mortality and square root for egg counts), so non-parametric statistics were employed. For the behavior experiment, time to first landing, number of landings, duration on cherries, min per landing, and number of eggs per cherry were analyzed using Kruskal–Wallis tests, generating T statistics, followed by multiple comparisons tests (Conover 1980, pp. 229–232). Percent landing, percent feeding, percent of flies landing on cherries, that oviposited, that stung fruit, and that died were analyzed using tests of more than two proportions, followed by a Tukey type multiple comparison procedure (Zar 1999, pp. 562–565). For the second to fourth experiments, mortality data for each time exposure (2, 4, 6, and 24 h) and oviposition by 24 h data were analyzed using Kruskal–Wallis tests. In tables, means are presented in parentheses to make data easier to understand, but analyses were conducted on ranks.

Results

Behavioral responses of flies to dried residues on cherries

The percent of flies landing and time to first landing on control and malathion-, zeta-cypermethrin-, and spinetoram-treated cherries did not differ (Table 1). However, the number of landings on cherries treated with zeta-cypermethrin was higher than on other cherries. Flies spent less time on cherries treated with malathion and zeta-cypermethrin than control or spinetoram-treated cherries, on which they were relatively inactive. Flies spent the least amount of time per landing on cherries treated with zeta-cypermethrin (Table 1). Percent of flies that fed on untreated cherry surfaces and surfaces of cherries treated with each of the three insecticides did not differ, but variance was high. Resting and grooming behaviors were observed in all flies. Grooming was not consistently recorded, but at least 12.5, 38.9, 64.3, and 27.3% of flies that landed on control, malathion-, zeta-cypermethrin-, and spinetoram-treated cherries, respectively, groomed their legs, wings, and/or heads.

Table 1 Behavioral responses of R. indifferens females to dried residues on cherries during 2-h observation periods at 20–21°C
Full size table

Oviposition and mortality responses of females that landed on cherries are shown in Table 2. Of flies that landed on fruits, the percentage that laid eggs in control fruit and insecticide-treated fruit did not differ. The percentages of flies that stung fruit were higher in malathion and zeta-cypermethrin treatments than in the spinetoram treatment, although they did not differ from the control. The percent of flies that stung fruit and laid eggs did not differ in the control and malathion and zeta-cypermethrin treatments. Only two flies in the spinetoram treatment stung fruit and laid eggs (not included in the analysis). The number of eggs laid per cherry did not differ among treatments (there were many zero data) (Table 2). The percent of flies that was paralyzed or dead within 2 h was higher in malathion and zeta-cypermethrin treatments than in the control and spinetoram treatment. Percent mortality at 24 h of flies that landed on malathion-, zeta-cypermethrin-, and spinetoram-treated cherries did not differ, but they were higher than in the control (Table 2).

Table 2 Oviposition and mortality responses of R. indifferens females that landed on dried residues on cherries duirng 2-h observation periods at 20–21°C
Full size table

Effects of dried residues on cherries on mortality and oviposition

Percent fly mortality 2 h post-exposure was highest in the high zeta-cypermethrin treatment (Table 3). At 4 and 6 h, mortalities in low and high zeta-cypermethrin treatments and low and high malathion treatments did not differ, and were higher than those in the two spinetoram treatments. By 24 h, however, all materials caused >90% mortality and did not differ (Table 3). None of the insecticide treatments prevented oviposition, but low and high rates of zeta-cypermethrin reduced oviposition the most, followed by the high and low rates of malathion, and then the high and low rates of spinetoram (Table 3).

Table 3 Effects of dried residues on cherries (dipped in solutions) on mortality and oviposition in R. indifferens females at 26–27°C
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Effects of contact with dried residues followed by exposure to dried residues on cherries on mortality and oviposition

Percent fly mortality 2 h post-exposure was higher in low and high zeta-cypermethrin than in all other treatments (Table 4). At 4 h, mortalities in low and high zeta-cypermethrin treatments were still highest, followed by high malathion and low and high spinetoram treatments, which did not differ. At 6 h, mortality was highest in the high zeta-cypermethrin treatment, followed by the low zeta-cypermethrin treatment; the high spinetoram treatment caused higher mortality than both malathion treatments. By 24 h, mortalities in the high zeta-cypermethrin and low and high spinetoram treatments were 100% and greater than in all other treatments. Results with the low malathion treatment did not differ from the control at any time (Table 4).

Table 4 Effects of contact with dried residues (2 ml spray) followed by exposure to dried residues on cherries (2 ml spray) on mortality and oviposition in R. indifferens females at 26–27°C
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Low and high zeta-cypermethrin treatments prevented all oviposition. Low and high spinetoram treatments did not differ and were the next most effective at reducing oviposition, followed by the high malathion treatment. The number of eggs in the low malathion treatment did not differ from that in the control (Table 4). The mean number of water droplets from the 2 ml spray (dried residues) on water sensitive papers in the 11.5-cm diameter and 4.3-cm high containers was 1,109 ± 47/cm2, with a mean droplet diameter of 0.351 ± 0.044 mm (range, 0.078–0.893 mm). Coverage on papers on the bottom of the lids of containers was 100% (papers were entirely blue), as there were no distinct droplets surrounded by uncovered paper.

Effects of direct sprays and exposure to insecticide-treated cherries on mortality and oviposition

Using 1 ml of spray, the percent mortality 2 h post-exposure was highest in the high zeta-cypermethrin treatment, followed by the low zeta-cypermethrin treatment, and then the high malathion treatment (Table 5). At 4 h, mortalities in low and high zeta-cypermethrin treatments were highest and did not differ, and mortality was greater in the high malathion treatment than in low and high spinetoram treatments. At 6 h, a similar trend was seen, except by this time, results with the high malathion and high spinetoram treatments did not differ. By 24 h, however, mortalities in the high zeta-cypermethrin and both spinetoram treatments were 100% and greater than in the malathion treatments (Table 5). At all times, the low malathion treatment caused the lowest mortality of the insecticide treatments (Table 5). Low and high zeta-cypermethrin treatments prevented all oviposition. Numbers of eggs in the high malathion and low and high spinetoram treatments did not differ. The number of eggs in the low malathion treatment did not differ from that in the control (Table 5). The mean number of water droplets from the 1 ml spray was 739 ± 104/cm2, with a mean droplet diameter of 0.240 ± 0.024 mm (range, 0.097–0.495 mm).

Table 5 Effects of direct sprays (1 ml) and exposure to insecticide-treated cherries (1 ml) on mortality and oviposition in R. indifferens females at 26–27°C
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Using 2 ml of spray, the percent mortality 2 h post-exposure was highest in low and high zeta-cypermethrin treatments (Table 6), with the high malathion treatment having an effect and both spinetoram treatments showing no effect compared with the control. At 4 h, the pattern was similar, except the spinetoram treatments began to show effects. At 6 h, low and high zeta-cypermethrin and high malathion treatments caused 98–100% mortality, more than other treatments. By 24 h, however, mortality in all insecticide treatments except the low malathion treatment was 97 or 100%. As in the two previous tests, the low malathion treatment caused the lowest mortality of all insecticides (Table 6). Also, as in those tests, low and high zeta-cypermethrin treatments prevented all oviposition. The number of eggs in the high malathion treatment was lower than in the low and high spinetoram treatments. The high spinetoram treatment had fewer eggs than the low spinetoram treatment, which had fewer than the low malathion treatment (Table 6). In this test, the droplet density could not be determined because the 2 ml spray resulted in near 100% coverage and almost all droplets bled into one another, causing the papers to be nearly entirely blue. Of the relatively few darker blue droplets that stood out against lighter blue or yellow areas, the mean diameter was 0.580 ± 0.038 mm (range, 0.214–0.854 mm).

Table 6 Effects of direct sprays (2 ml) and exposure to insecticide-treated cherries (2 ml) on mortality and oviposition in R. indifferens females at 26–27°C
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Discussion

The differences in mortality and oviposition in R. indifferens observed in this study were likely caused by the differences in modes of action of the materials. Malathion is a cholinesterase inhibitor (Spencer and O’Brien 1957), whereas zeta-cypermethrin acts on the sodium channel modulator of the nervous system (Soderlund et al. 2002; Brown 2006; Anonymous 2011). Zeta-cypermethrin has quick knockdown ability typical of pyrethroids (Briggs et al. 1974). Spinetoram is a newer, semi-synthetic spinosyn insecticide (Dripps et al. 2008) whose mechanism of action is presumably similar to that of spinosad, which acts as a nicotinic acetylcholine receptor agonist (mimic) and affects the GABA receptor function (Brown 2006; Dow AgroSciences 2011).

Despite the insecticides’ different modes of action, behavioral responses of R. indifferens females indicated that the propensity to land on dried residues of the three insecticides on cherry fruits did not differ at 20–21°C. This suggests that the flies were unable to detect the different residues or that if they did, they did not avoid them, resulting in equal likelihood of flies contacting residues of the three insecticides tested. These results are similar to those for neonicotinoid insecticides (Yee 2008). In other insects, however, including house flies, mosquitoes, stinkbugs, and psyllids, there is evidence for repellency or avoidance behavior toward some insecticides (Brown and Pal 1971; Burden 1975; Moore 1977; Pluthero and Singh 1984; Gharalari et al. 2009; Kamminga et al. 2009). In R. indifferens, females actually spent the most time on spinetoram-treated and control cherries. Flies also had the most frequent landing bouts on zeta-cypermethrin-treated cherries, possibly because flies were poisoned and irritated (Pluthero and Singh 1984) by the dried residues, resulting in more erratic and frequent movement in the relatively confined space inside cups. Dried spinetoram residues acted more slowly than malathion and zeta-cypermethrin, evidenced by less movement by flies exposed to the spinetoram-treated cherries. However, flies were not deterred from feeding on dried residues of any of the insecticides, so that mortality caused by a combination of tarsal contact and ingestion is equally likely for all three.

During the 2-h behavioral observations, none of the dried insecticide residues immediately knocked flies down, unlike when flies were sprayed with fresh zeta-cypermethrin (fourth experiment) or when materials such as acetamiprid or imidacloprid were ingested with bait (Barry and Polavarapu 2005; Yee 2010). This allowed flies to sting fruit and in many cases to oviposit. The percent of females that stung fruit in the spinetoram treatment was low, suggesting that the material arrested the flies during the 2-h exposures at 20–21°C. The lack of a one to one correspondence between stinging and oviposition suggests flies evaluated the cherries for suitable places to oviposit regardless of insecticide presence. Malathion and zeta-cypermethrin acted more quickly than spinetoram, but all insecticides caused similar mortality after 24 h (82–89%), suggesting that exposure of <2 h to treated cherries at 20–21°C does not result in lethal doses for all three materials.

In the second to fourth experiments, zeta-cypermethrin always killed flies the fastest, as indicated by mortalities at 2-h post exposure, and always caused flies to lay the fewest eggs, suggesting that speed of mortality was related to and almost certainly the cause of low oviposition levels (Yee 2010). Results with these three insecticides suggest a material has to kill about 78% of reproductively mature flies within 2 h to prevent oviposition. Low and high rates of zeta-cypermethrin and of malathion killed 76–81% of flies by 6 h (second experiment), but this was too late to prevent oviposition (Table 3). Thus, mortalities after 6 h do not provide accurate information about the efficacy of a material against reproductively mature flies.

Although it was clear that zeta-cypermethrin was the most effective material tested at causing mortality within 2 h and preventing oviposition, the degree of protection it afforded depended on how the flies were exposed to it. Zeta-cypermethrin did not completely prevent oviposition when untreated flies were presented with cherries dipped in insecticide. This suggests either that there was surface area of cherries not covered with dried residues or that, as the results suggest, flies need to contact dried zeta-cypermethrin residues for up to 20–25 min before contacting residues again on cherries in order for flies to be killed quickly enough to prevent oviposition. Direct sprays also killed flies the quickest, consistent with studies in other insects comparing topical versus residual toxicities (Marçon et al. 1997; Boiteau and Noronha 2007; Dagli and Bahsi 2009), affording 100% protection of cherries. The 2 ml sprays resulted in higher earlier mortality than 1 ml sprays, presumably because of greater, more uniform, insecticide dosages. Topical applications seem to result in less variability in mortality than residual contact (Marçon et al. 1997).

Similarly, the relative effects of malathion and spinetoram on mortality and oviposition were affected by how the flies were exposed to the two materials. The high rate of malathion was more effective than spinetoram at reducing oviposition when flies contacted dried residues on cherries that had been dipped in insecticide (first and second experiments) or were directly sprayed at a high volume (2 ml) (fourth experiment). The rate of malathion obtained by dipping cherries in solution in the second experiment probably was higher than that achieved by direct spray with 1 ml in the fourth experiment, based on mortalities, but this was not true of spinetoram or zeta-cypermethrin, perhaps reflecting adhesion differences among insecticides. Malathion may need to be applied at high concentrations and/or high volume to kill a large percentage of flies. Malathion applied to 1- to 24-h-old R. indifferens using an atomizer was not very effective compared with other insecticides applied the same way (Frick 1957). In tsetse flies, several insecticides (e.g., dieldrin and isobenzan) were more potent as topical than as residual deposit applications, but malathion seemed to be more active as residues when flies were exposed to them for only 1 min (Busvine et al. 1967).

Spinetoram was more effective than malathion in causing adult mortality and reducing oviposition when flies walked for 20–30 min on dried residues, and then contacted dried residues on cherries applied using the spray tower at 2 ml (third experiment). Apparently this method of exposure resulted in higher lethal doses of spinetoram than malathion for R. indifferens. However, at 1 ml spray, there was no difference in reducing oviposition between the high dosage rates of spinetoram and malathion (fourth experiment), suggesting both materials at a low spray volume are relatively ineffective.

It is not possible to precisely determine the spray volume that would cover an individual fly in the field, but there would clearly be variability. At 935 l spray/ha, 6.1 m × 6.1 m tree spacing and 269 trees/ha, one tree would receive about 3.5 l of spray, depending on tree size, canopy area, spray drift, and how much spray ends up in between tree rows. Where the flies are located within trees would affect how thoroughly they are covered. Field tests can be conducted to determine the volume needed to achieve the 1,109 (2 ml spray) and 739 spray droplets/cm2 coverage (1 ml spray), as well as the 100% coverage seen in this study using the spray tower so that fly mortality in the field can be predicted.

Early data are unclear as to whether there are differences between the susceptibility of R. indifferens and D. suzukii to the three insecticides, in particular to their speed of kill. Residues of malathion caused higher mortality in D. suzukii than residues of zeta-cypermethrin and spinetoram after 24 h (Oregon State University 2010). However, direct sprays of malathion, zeta-cypermethrin, and spinetoram at the high field rate in 468 l spray/ha caused 100% mortality at 24 h, even though timings of earlier mortality were not reported (Oregon State University 2010).

Based on results presented here, the best scenarios for effective field control of R. indifferens in the framework of D. suzukii control involve spraying zeta-cypermethrin on cherry trees near harvest when D. suzukii is most likely to occur in the orchard. Unless sprays for D. suzukii are to be applied anyway, it is first necessary to assess the risk of mature R. indifferens entering orchards, which could be based on the presence of unmanaged, infested cherry trees 171 m away, one cited dispersal distance (Jones and Wallace 1955). Ideally, if there was a risk for reproductively mature R. indifferens in the orchard, high volume cover sprays would be applied to prevent oviposition. Residues remaining on leaves and cherries may also be sufficient to kill R. indifferens early enough to prevent oviposition if flies first land on leaves and walk on residues for about 20 min before landing on fruits. Mature females that enter orchards and land immediately on treated cherries are the greatest risk for laying eggs before being killed. The likelihood of this scenario is unclear because leaves account for such a large surface area of cherry trees and R. indifferens females spend a large amount of their midday hours on leaves (Yee 2002). However, to fully implement an IPM program, data on the effects of insecticide residues on D. suzukii mortality (in addition to what has been done, Oregon State University 2010) and their effects on mortality of both R. indifferens and D. suzukii at the same time under field conditions are needed.

Use of malathion, zeta-cypermethrin, and spinetoram may all have advantages and disadvantages. As consistently shown in this study, zeta-cypermethrin is most effective at protecting cherries and is the material of choice, but it and other pyrethroids have been reported to cause flare-ups of spider mites during warm summer months due to toxicity to natural enemies (Wong and Chapman 1979; Holland 1991; Smith and Kupferman 2003). However, one study showed that zeta-cypermethrin had low toxicity as a leaf residue to the beneficial insects Aphytis and Orius (Michaud and Grant 2003). Of the three insecticides, zeta-cypermethrin has the longest pre-harvest interval (PHI) at 14 days. Malathion can reduce densities of natural predators (e.g., Cohen et al. 1987; Knutson et al. 2011) and has been reported to injure fruit and foliage of “Rainier” cherries (Washington State University 2011), but it has the shortest PHI at 3 days. No injury to cherry foliage caused by zeta-cypermethrin and spinetoram has been reported. Spinetoram has a PHI of 7 days. Spinetoram is safer for bumblebees than spinosad (Besard et al. 2011), which is also toxic to aphid parasitoids (Wang et al. 2005).

The current study did not determine the long-term residual activity of any insecticide against R. indifferens. However, in laboratory trials in Oregon against D. suzukii, diazinon and malathion had the longest residual activity against D. suzukii, and zeta-cypermethrin had the longest residual efficacy of any pyrethroid tested. In these same trials, spinetoram had residual activity comparable to zeta-cypermethrin (Oregon State University 2010; Walsh et al. 2010). Residual toxicities of malathion (Mohammad and AliNiazee 1989) and spinetoram (Yee et al. 2007) against apple maggot, Rhagoletis pomonella (Walsh), on apple leaves was <1 week.

In summary, the results suggest zeta-cypermethrin is the most effective of the three materials tested at protecting cherries against oviposition by R. indifferens because of its fast-acting toxicity and could be used in an integrated control program for it and D. suzukii, although any disadvantages of using it need to be taken into account. Direct spray of zeta-cypermethrin on R. indifferens flies may be the most effective control method, but prolonged fly contact with dried residues also may be effective. Studies that directly compare relative insecticide efficacies against R. indifferens and D. suzukii in the field are needed before IPM strategies for cherries are revised.