Specialized Pheromone and Lure Application Technology as an Alternative Male Annihilation Technique to Manage Bactrocera tryoni (Diptera: Tephritidae)

Transcription

1 Horticultural Entomology Journal of Economic Entomology, 109(3), 2016, doi: /jee/tow023 Advance Access Publication Date: 27 March 2016 Research article Specialized Pheromone and Lure Application Technology as an Alternative Male Annihilation Technique to Manage Bactrocera tryoni (Diptera: Tephritidae) O. L. Reynolds, 1,2 T. Osborne, 3 P. Crisp, 4 and I. M. Barchia 3 1 Graham Centre for Agricultural Innovation (New South Wales Department of Primary Industries and Charles Sturt University), Elizabeth Macarthur Agricultural Institute, Private Bag 4008, Narellan, New South Wales 2567, Australia (olivia.reynolds@ dpi.nsw.gov.au), 2 Corresponding author, olivia.reynolds@dpi.nsw.gov.au, 3 NSW Department of Primary Industries, Elizabeth Macarthur Agricultural Institute, Private Bag 4008, Narellan, New South Wales 2567, Australia (terry.osborne@trade. nsw.gov.au; idris.barchia@dpi.nsw.gov.au), and 4 South Australian Government, South Australian Research and Development Institute, GPO Box 397, Adelaide, South Australia 5001, Australia (peter.crisp@sa.gov.au) Received 6 November 2015; Accepted 27 January 2016 Abstract The results of this study suggest that a novel male annihilation technique (specialized pheromone and lure application technology [SPLAT] incorporating cue-lure [CL] plus spinosad) is as effective as industry standard male annihilation controls, and is worth exploring further to manage Bactrocera tryoni (Froggatt) populations. Three lures were evaluated in a contact and feeding bioassay and a cage attractancy trial: 1) SPLAT-CL þ spinosad; 2) SPLAT-CL without spinosad; and 3) wick-cl þ malathion. In a field attraction trial, lures (1) and (3) were evaluated with a third treatment, caneite blocks-cl þ malathion. Lures were weathered for 0, 1, 2, 4, or 8 wk, with an additional weathering treatment of 12 wk included in the field trial. In the contact and feeding bioassay, lures with SPLAT-CL þ spinosad were >97% effective at 48 h for up to 2 wk weathering; however, wicks-cl þ malathion killed B. tryoni within 2 h of exposure under all weathering periods. In the cage attractancy trial, SPLAT-CL þ spinosad was as effective as, or performed better than, wicks-cl þ malathion under all weathering treatments. The field study trap catches were similar for SPLAT-CL þ spinosad and blocks-cl þ malathion, and both had higher trap catches than wicks-cl þ malathion at all weathering periods, except week 12. Overall, SPLAT-CL þ spinosad compared favorably with current standard techniques for male annihilation and warrants further research. SPLAT-CL þ spinosad may be a reduced-risk alternative for wicks-cl þ malathion or blocks-cl þ malathion for B. tryoni and other CL-responding fruit flies, such as Bactrocera cucurbitae Coquillett, because it contains a reduced-risk insecticide that poses a lower risk to humans and the environment and does not require labor-intensive handling and placement. Key words: specialized pheromone and lure application technology, male annihilation technique, malathion, spinosad, Queensland fruit fly Fruit flies (Diptera: Tephritidae) constitute some of the world s most significant pests of horticulture (Sutherst et al. 2000). The Queensland fruit fly, Bactrocera tryoni (Froggatt), is the most significant biosecurity threat to national and international market access for horticultural commodities produced in eastern and south-eastern Australia (Plant Health Australia [PHA] 2008). The polyphagous nature of this pest, recorded on >240 plant species from 49 families (White and Elson-Harris 1992, Hancock et al. 2000), its climatic adaptability, and the expansion of its cultivated host range have, among other factors, enabled its spread throughout northern and eastern Australia. Economic losses owing to B. tryoni were estimated at AU$28.5 million annually in 2000, rising to an estimated AU$100 million in lost production if the population is uncontrolled (Sutherst et al. 2000). In the early 1900s, the notion of managing fruit flies by targeting males was proposed (Froggatt 1909). This concept of male annihilation is based upon reducing the number of males available for mating in the population, thereby reducing the number of mated females and breaking the life cycle. The male annihilation technique (MAT) is a form of attract and kill, whereby an attractant lure is included in some form of matrix, which also includes a toxicant. Without an attractant or lure, effective management of tephritids is difficult. In the late 1950s, Willison [unpublished data, as cited by Bateman (1966)] found that males of B. tryoni were attracted to a VC The Authors Published by Oxford University Press on behalf of Entomological Society of America. All rights reserved. For Permissions, please journals.permissions@oup.com 1254

2 Journal of Economic Entomology, 2016, Vol. 109, No compound that he synthesized, 4-(p-hydroxypheny1) butan-2-one (Bateman 1966), now commonly referred to as cue-lure (CL). In Australia, male annihilation successfully employs CL to control mature male B. tryoni (Dominiak et al. 2003, Lloyd et al. 2010, Dominiak and Nichol 2012). Male flies are typically attracted to and locate a lure, impregnated with an insecticide, through upwind anemotaxis (Hee and Tan 1998, Meats and Hartland 1999), feed, and then die. Male annihilation is a very effective form of pest management and has been used worldwide to manage tephritids (see Vargas et al. 2014a for a review). In an integrated pest management (IPM) system, male annihilation is typically used in conjunction with protein bait sprays and crop sanitation (Vargas et al. 2014a). Historically, organophosphate insecticides including malathion, fipronil, and naled have been the toxicant used with male annihilation, but, more recently, there has been a move toward reduced-risk insecticides (Vargas et al. 2014a), so less toxic and more userfriendly alternative attract and kill male lure devices containing the reduced-risk insecticide, spinosad, are currently being researched and developed. Spinosad, which comes from the soil bacterium Saccharopolyspora spinosa Mertz and Yao, works mainly via ingestion, but also via contact. Spinosad is more environmentally sustainable than the products currently used, because it is considered to pose less risk to mammals, birds, fish, and natural enemies, and is active at low application rates against many economically important pest insects (DowElanco 1994, Stark 2004). Further, traditional blocks used in B tryoni management are caneite blocks, which must be soaked in a lure or toxicant mix, and then attached to trees individually. There is an increased health risk with the handling of organophosphate insecticides by operators and their subsequent use in residential and other environmentally sensitive areas. Individual placement of blocks is also labor intensive. Consequently, a sprayable attract and kill (i.e., male annihilation) formulation consisting of a waxy dispenser, called specialized pheromone and lure application technology (SPLAT; ISCA Tech., Riverside, CA), in combination with the reduced-risk insecticide spinosad and either methyl eugenol (ME) or CL was first tested against fruit flies (Vargas et al. 2008a). The SPLAT formulation of biologically inert materials is used to control the release of semiochemicals, with or without pesticides, while protecting these components from environmental degradation. SPLAT-MAT is a highly adaptable product that is both amorphous and flowable (Stelinski 2007), and can be applied via a range of options, including a high-powered spray gun, regular spray equipment on a quad bike or tractor, or aerial release (Vargas et al. 2008a), with unmanned devices an untested alternative. This ease of delivery may reduce labor costs, speed up delivery, and eliminate the need to establish, replenish, and retrieve devices including lure- and toxicant-impregnated blocks and wicks (Vargas et al. 2009, 2010; Hsu and Tan 2010). Efficacy of SPLAT formulations are thought to be enhanced as several hundred point sources per hectare can be achieved via spray application, compared with the physical placement of MATs at recommended rates for male annihilation (Hsu 2010). In Hawaii, SPLAT and CL or ME suppresses fruit flies for up to 12 wk (Vargas et al. 2008a, 2009, 2010; Gomez et al. 2015). The few published studies demonstrating the efficacy of SPLAT- MAT against fruit flies have largely focused on the melon fly, Bactrocera cucurbitae Coquillett, and Oriental fruit fly, Bactrocera dorsalis Hendel, in Hawaii (Vargas et al. 2008a, 2009, 2010, 2014b; Gomez 2015), B. dorsalis in Taiwan (Hsu and Tan 2010), and the peach fruit fly, Bactrocera zonata, in Pakistan (Gomez et al. 2015). Only a single study has included B. tryoni (and B. dorsalis), and it was in Tahiti (Leblanc et al. 2011). It showed that SPLAT- MAT-CL-baited trap captures of B. tryoni, compared favorably with other standard lure formulations (Leblanc et al. 2011). As this paper will show, SPLAT-CL þ spinosad compared favorably with standard male annihilation controls in Australia and is worth exploring further to suppress B. tryoni populations. Materials and Methods Insects Bactrocera tryoni pupae were obtained from a low stress colony at Central Coast Primary Industries Centre, NSWDPI, North Loop Road, Ourimbah, reared in a controlled environment room (i.e., C, % relative humidity [RH], and a photoperiod of 14:10 [L:D] h, with a simulated dawn and dusk as the lights ramped up and down at the beginning and end of the light phase). At Elizabeth Macarthur Agricultural Institute (EMAI), Menangle, NSW, Australia, pupae were placed in 50 mm-diameter plastic Petri dishes, under moistened vermiculite (1:4; water:vermiculite) on the base of cubical mesh holding cages (30 cm 3 ; Bugdorm, Taiwan) under standard conditions in a controlled environment room (i.e., C, % RH, and a photoperiod of 16:8 [L:D] h). Emerged adult flies were provided with sugar (sucrose) cubes as a source of carbohydrate and a 30 mm-diameter plastic Petri dish containing yeast hydrolysate enzymatic (MP Biomedical, Auburn, OH; 60% protein) as a source of protein and water ad libitum. Adult male flies were allowed to mate and were tested when aged 7 10 d, at which time they have normally reached sexual maturity and are responsive to CL. Male annihilation is based upon this concept that the flies will be attracted, feed, and die. Weathering of Cue-Lure Treatments Three male annihilation CL treatments were evaluated in a laboratory feeding bioassay and a cage attraction trial: 1) SPLAT-5%CL þ spinosad (hereafter referred to as SPLAT-CL þ spinosad ; 2% active ingredient [a.i.]); 2) SPLAT-CL without spinosad (control); 3) wicks with CL þ malathion (hereafter referred to as wicks-cl þ malathion ; 57% a.i.; 0.5 ml per wick maldison [malathion], 1.0 ml per wick 4-(p-Acetoxyphenyl) butan-2-one; Bugs for Bugs, Mundubberra, Qld, Australia), an industry standard currently used in Australia. SPLAT (blank; ISCA Tech.) was mixed with CL (Bugs for Bugs) þ spinosad (Success 2 Naturalyte Insect Control; Dow AgroSciences, Frenchs Forest, NSW, Australia), and CL to achieve the required amount for treatments 1 and 2, respectively. The SPLAT-CL treatment without spinosad was evaluated to determine whether continuous exposure to CL for a maximum period of 48 h would be lethal to males. In a field attraction trial, treatments (1) and (3) above were evaluated with a third treatment, MAT caneite blocks (hereafter referred to as blocks-cl þ malathion ; 50 by 50 by 12 mm 3 impregnated with 2 ml maldison þ 2 ml CL per block), a New South Wales (NSW) government standard used across NSW, Australia. Approximately 0.02 g (Contact and feeding toxicity bioassay see below), 1 g (Cage attraction trial see below), and 2 g (Field trial) of each SPLAT treatment was placed onto the surface of wooden ice-cream sampler sticks (1.7 by 9.5 cm 2 ; Stsellsok [A1 Packaging] Merrylands, NSW, Australia). For wicks-cl þ malathion, 0.02 g was used in the laboratory bioassay, whereas the whole wick was suspended in cages and Lynfield traps for the cage attraction and field attraction trials, respectively. For blocks-cl þ malathion, the whole block was suspended in Lynfield traps. TherequiredamountofeachSPLATtreatmentwasappliedtothe surface of each stick using a spatula, and weighed using a balance, to

3 1256 Journal of Economic Entomology, 2016, Vol. 109, No. 3 two decimal places. A small hole was drilled in the nontreated end of each stick. Wooden sticks, wicks-cl þ malathion, and blocks-cl þ malathion were hung on a weathering line suspended between Lilly Pilly, Syzygium smithii (Poir.), trees in partially shaded locations and exposed to sunlight, wind, and rain at EMAI. For each trial, three treatments were tested for each of five aging periods (0, 1, 2, 4, and 8 wk), with the exception of the field trial, which included an additional 12-wk weathered treatment. At the prescribed intervals, each stick or wick or block was utilized in the relevant trial (see below). The climatic data for the weathering of the lure or toxicant for each trial are shown in Table 1. Trial Protocol Contact and Feeding Toxicity Bioassay (Trial 1) A laboratory contact or feeding bioassay was used to determine the relative toxicity of the three differentially aged CL formulations described earlier, under standard conditions, using laboratory-reared F14 15 generation males. The method was modified from that of Vargas et al. (2009). Individual males were introduced into an experimental mesh cage (30 cm 3 ) containing a particular treatment, gently placed onto the test material, and allowed to feed or come in contact with the lure for 1 min 30 s to 5 min. Only those feeding or in contact with the lure for >1 min 30 s were included in the analyses. After feeding or contact, each male was introduced into individual 500-ml plastic cups containing a cube of agar-based adult diet containing sugar and yeast hydrolysate and covered with fly proof mesh. Eight males were exposed in sequence to the same material; therefore, mortality after 2, 4, 24, and 48 h was calculated as a proportion (number of males dead/eight males that fed on or contacted a given treatment). For each of the five aging periods, there were five replicates of each of the three MAT CL treatments. Cage Attraction Trial (Trial 2) The relative toxicity of the three MAT CL treatments associated with a toxicant (spinosad or malathion) described earlier was quantified in by by 93-cm mesh cages (Bugdorm, Taiwan) deployed in a large covered open-sided field laboratory with plenty of airflow at the EMAI using laboratory-reared F15 generation male B. tryoni as described earlier. A blank treatment (untreated wooden stick) was also used to assess natural mortality. Cages were spaced at least 2 m apart. For each of the five weathered periods for each test period, a single wick or treated or untreated wooden stick was hung inside each of three mesh cages containing four sugar (sucrose) cubes as a source of carbohydrate and a 30-mm-diameter plastic Petri dish containing yeast hydrolysate enzymatic (as described above) and water ad libitum. Twenty-five laboratory-reared males were released per cage between 0900 and 1030 hours. After flies were released, an observer recorded the number of dead males at 4, 24, and 48 h after release. Four temporal replicates were carried out for each treatment age combination. In total, 300 males were tested for each aging period, 100 males for each treatment age period (i.e., 1,500 males total). The mean (6SE) trial temperature and RH were C and %, respectively. Field Attraction Trial (Trial 3) A field trial was conducted from 18 February to 1 April The relative toxicity of the three MAT CL treatments associated with a toxicant (spinosad or malathion), as described earlier, was quantified in a mixed fruit (pome, stone, and quince fruit) orchard located at EMAI, which had not been treated with any pesticide in over four yr. Twelve Lynfield traps were spaced 20 m apart with three traps in each of four rows. Each row held one of each MAT CL treatments, suspended in the trap in a random design. Traps were checked for B. tryoni after 7 d. The trial was temporally replicated six times. The mean (6 SE) trial temperature, RH, and rainfall were C, %, and mm, respectively. Statistical Analysis Contact and Feeding Bioassay and Cage Attraction Trial Data (proportion of B. tryoni mortality) were analyzed using a generalized linear mixed model (Schall 1991) to compare the effects of SPLAT and other pesticides at different weathering periods. As these treatment combinations were repeated at different times (different cohorts), these effects were assumed to be random in the model. A logit link was used to relate the observed values and the explanatory variables. All parameters were estimated using the residual maximum likelihood (REML) technique (Patterson and Thompson 1971). Because zero or 100 percent mortality inflates the weighting factor of logit transformed data, a small value (0.25 N 1 ) was added to zero proportion and subtracted from 100% (Bartlett 1947). Multiple comparison tests between treatments were made using the least significant difference (LSD) test at P < 0.05 on the logit scale. Table 1. Mean 6 SE minimum and maximum temperature and relative humidity, and cumulative rainfall for the weathering site at Menangle, Australia, for all trials Trial Weathering period (wk) Mean temp ( C) 6 SE Min and max temp ( C) Mean relative humidity (%) 6 SE Min and max relative humidity (%) Cumulative rainfall (mm)

4 Journal of Economic Entomology, 2016, Vol. 109, No Table 2. Mortality (logit (P) 6 SE and mean (%)) of male Queensland fruit fly, B. tryoni, allowed to feed or contact (1 min 30 s to 5 min) weathered SPLAT-CL þ spinosad, SPLAT-CL (no toxicant), or wick-cl þ malathion after 2, 4, 24, and 48 h Treatment Weathering period (wks) Logit (P) 6 SE and mean (%) mortality 2h 2h 4h 4h 24h 24h 48h 48h SPLAT-CL (no toxicant) f e e d f e e e e d d d f e d d f e d d SPLAT-CL þ spinosad b b b b c b b a c b b a d c c c f c c c Wick-CL þ malathion a a a a a a a a a a a a a a a a a a a a Treatment means were compared on the logit scale. Means within columns followed by the same letter were not significantly different using LSD, P ¼ Field Attraction Trial Number of insects (male B. tryoni) were analyzed using a generalized linear mixed model with errors assumed to follow a Poisson distribution (Schall 1991). A logarithmic link function was used to relate the figures for chemical and weathering duration fixed effects and replicate random effects. A REML method (Patterson and Thompson 1971) was used to estimate all parameters, and treatment mean differences were made on log scale at P < 0.05 significance level. Results Contact and Feeding Bioassay In the contact and feeding bioassay, wicks-cl þ malathion killed B. tryoni within 2 h of exposure in all weathering periods (Table 2). Overall, lures with SPLAT-CL (no toxicant) had little effect on B. tryoni on all occasions; however, lures with SPLAT-CL þ spinosad were most effective for up to 2 wk of weathering. Cage Attraction Trial In this study, the SPLAT-CL þ spinosad performed as well as the wicks-cl þ malathion across all weathering treatments, except week 1 when mortality was significantly higher for SPLAT-CL þ spinosad compared with the wicks-cl þ malathion (Table 3). SPLAT-CL (no toxicant) demonstrated less mortality than both treatments with a toxicant. A blank (wooden stick with no treatment) was included to determine natural mortality, which did not differ largely from the control (SPLAT-CL no toxicant), indicating that the SPLAT-CL by itself is not toxic to B. tryoni. Field Attraction Trial Blocks-CL þ malathion consistently reported the highest trap catches for all weathered and non-weathered periods, except week 12 (Table 4). SPLAT-CL þ spinosad trap catches compared favorably with blocks-cl þ malathion at 0, 1, 8, and 12 wk weathering, however, was lower than blocks-cl þ malathion for weeks 2 and 4. SPLAT-CL þ spinosad was comparable with wicks-cl þ malathion at all weathering periods, with the exception of week 8, when it performed better than wicks-cl þ malathion; however, at 12 wk, wicks-cl þ malathion performed better than both SPLAT-CL þ spinosad and blocks-cl þ malathion. SPLAT-CL þ spinosad and blocks-cl þ malathion decreased in efficacy by week 12 compared with their respective nonweathered lures by 75 and 79%, suggesting reduced persistence and attractiveness from this time. Conversely, at week 12, wicks-cl þ malathion showed a 1.5-fold increase in efficacy compared with the nonweathered lure, despite the previous weathered treatment (i.e., week 8) showing the lowest efficacy. Discussion This study demonstrates that male B. tryoni populations may be managed with the use of a novel male annihilation, SPLAT-CL þ spinosad, which retains its attraction and efficacy up to 12 wk. In contrast to other male annihilation options for B. tryoni, the benefits of this technology are the inclusion of a reduced-risk insecticide, spinosad, with reduced human health and environmental impacts, that does not require individual handling. As spinosad acts mainly via ingestion and can take 1 2 d for mortality to occur and male B. tryoni demonstrate strong feeding behavior toward CL males had to be coaxed from feeding on both the SPLAT-CL þ spinosad and SPLAT-CL in the laboratory bioassay it is reasonable to expect that longer feeding periods would lead to greater ingestion of not just the lure, but also the toxicant. Therefore, as flies were exposed to each treatment for a maximum of 5 min in the bioassay, it would be reasonable to assume that under field conditions, males would have access to the toxicant for a longer period. In both the cage attraction and field studies, SPLAT- CL þ spinosad generally performed at least analogous to, or better than, the wicks-cl þ malathion and blocks-cl þ malathion, under most weathering treatments. These results are consistent with our prediction that, when males are allowed to feed over a longer period on the lure and toxicant mix, they imbibed enough toxicant to induce comparable or increased mortality across all weathered treatments trialed. Similarly, when comparing feeding tests and a field cage study, mortality of B. dorsalis was <50% after feeding on

5 1258 Journal of Economic Entomology, 2016, Vol. 109, No. 3 Table 3. Mortality (logit (P) 6 SE and mean (%)) of male Queensland fruit fly, B. tryoni, exposed continuously to weathered SPLAT- CL þ spinosad, SPLAT-CL (no toxicant; control), wick-cl þ malathion, or nil treatment (blank) at 4, 24, and 48 h Treatment Weathering period (wk) Logit (P) 6 SE and mean (%) mortality 4h 4h 24h 24h 48h 48h No treatment (blank) d c de SPLAT-CL (no toxicant; control) d c d d c de d c e d c d d c de SPLAT-CL þ spinosad ab a ab a a a abc ab bc abc a abc abc ab bc Wick-CL þ malathion bc ab ab c b c abc ab abc abc ab bc abc ab bc Treatment means were compared on the logit scale. Means within columns followed by the same letter were not significantly different using LSD, P ¼ Table 4. Trap captures of wild male Queensland fruit fly, B. tryoni, in Lynfield traps baited with non-weathered and weathered CL treatments at Menangle, New South Wales, Australia, in 2015 Treatment Weathering period (wk) SPLAT-CL þ spinosad Mean (%) 9.10abA 4.47abBC 6.45bAB 6.29bAB 10.76aA 2.32bC Wick-CL þ malathion 5.46bAB 2.32bC 4.63bAB 3.31bBC 2.32bC 8.61aA Block-CL þ malathion 14.40aA 7.12aB 13.57aA 17.21aA 11.59aAB 2.98bC SPLAT-CL þ spinosad Logit (P) Wick-CL þ malathion Block-CL þ malathion Means within columns followed by the same lowercase letter and means within rows followed by the same upper case letters were not significantly different using LSD, P ¼ wk weathered SPLAT-ME þ spinosad, but mortality ranged from 73 97% when flies were exposed to the same material in a field cage (Vargas et al. 2009). The authors attributed the results to greater amounts of spinosad likely ingested by the flies in the cage tests, where flies had continual access to the treatments. Moreover, in a feeding study in Hawaii, melon fly, B. cucurbitae, fed on SPLAT-CL þ spinosad displayed reduced mortality compared with Min-U-Gel-CL with naled (used in eradication programs against this and other ME-responding tephritids) from about 2 wk, which was attributed to the reduced persistence of spinosad (Vargas et al. 2010). However, the treated flies were held for 24 h, with longer holding periods thought necessary (Vargas et al. 2010). In our study, we consistently observed increased B. tryoni mortality from 4 h through to 48 h for the SPLAT-CL þ spinosad within a weathering period. SPLAT-CL þ spinosad performed as well as, or better than, the industry standard MATs, against B. tryoni for most of the weathering periods in the attraction trials. Based on the encouraging results of this study, further evaluations of SPLAT-CL þ spinosad against B. tryoni in Australia are warranted. In recent studies, SPLAT and CL or ME compared favorably with other standard formulations used against B. tryoni (Leblanc et al. 2011), B. dorsalis (Vargas et al. 2008a, 2014b; Gomez et al. 2015), and B. cucurbitae (Vargas et al. 2008a) for up to 12 wk. Male annihilation against tephritids is best used together with other compatible technologies in an IPM, area-wide or AW-IPM approach. The Hawaii fruit fly AW-IPM program successfully managed four invasive species (Mediterranean fruit fly, Ceratitis capitata (Wiedemann); melon fly, B. cucurbitae; oriental fruit fly, B. dorsalis; and Solanum fruit fly, B. latifrons (Hendel)), which in addition to MAT included field sanitation, protein bait, sterile insect technique (SIT), and biological control (Vargas et al. 2008b). Similarly, compatible technologies for B. tryoni management include protein bait sprays, crop or host sanitation (Lloyd et al. 2010), SIT (Gurr and Kvedaras 2010; Reynolds et al. 2012, 2014), and parasitoids (Ero et al. 2011, Spinner et al. 2011, Harris et al. 2012, Zamek et al. 2013), the latter which, are still under development. Combinations of these techniques are used to eradicate B. tryoni outbreaks from the B. tryoni-free states of South Australia (Jackman et al. 1996, Perepelicia et al. 1997) and Western Australia (Fisher 1996). These techniques were also used to eradicate B. tryoni from the Fruit Fly Exclusion Zone in New South Wales and Victoria (Reynolds et al. 2012).

6 Journal of Economic Entomology, 2016, Vol. 109, No Overall, SPLAT-CL þ spinosad is a promising alternative for wicks-cl þ malathion and blocks-cl þ malathion to manage B. tryoni under Australian conditions, and may have application for other CL-responding pest fruit flies, including the invasive B. cucurbitae. Acknowledgments Thank you to Robert Brown, Craig Boys, and two anonymous reviewers, who provided useful comments on an earlier draft. We thank Antonita Jukiel for assistance with manuscript production. This project has been funded by Horticulture Innovation Australia Limited using summerfruit, mango, cherry, citrus, banana, and avocado industry levy and funds from the Australian Government. References Cited Bartlett, M Multivariate Analysis. Journal of the Royal Statistical Society, Series B. 9: Bateman, M. A., A. H. Friend, and F. Hampshire Population suppression in the Queensland fruit fly, Dacus (Strumeta) tryoni. I. The effects of male depletion in a semi-isolated population. Aus. J. Agric. Econ. 17: Dominiak, B., and I. H Nichol Chemical analysis of male annihilation blocks used in the control of Queensland fruit fly Bactrocera tryoni (Froggatt) in New South Wlaes. Plant Prot. Quart. 27: Dominiak, B. C., A. R. Gilmour, B. Kerruish, and D. Whitehead Detecting low populations of Queensland fruit fly Bactrocera tryoni (Froggatt) with McPhail and Lynfield traps. Gen. Appl. Ent. 32: DowElanco Spinosad technical guide: DowElanco, Indianapolis, IN. Ero, M. M., C. J. Neale, E. Hamacek, T. Peek, and A. R. Clarke Preference and performance of Diachasmimorpha kraussii (Fullaway) (Hymenoptera: Braconidae) on five commercial fruit species. J. Appl. Entomol. 135: Fisher, K Queensland fruit fly (Bactrocera tryoni): eradication from Western Australia, pp In B. A. MacPheron and G. J. Streck (eds.), Fruit Fly Pests. A World Assessment of Their Biology and Management. St. Lucie Press, FL. Froggatt, W. W Official report on fruit fly and other pests in various countries, NSW Department of Agriculture. Gomez, L. E., M. Lysandraou, R. Vargas, J. E. Dripps, X. Huang, M. R. Yadav, and N.K.B. Venkata SPLAT-MAT Spinosad ME: a new control strategy for Bactrocera species attacking mango. Acta Hort. 1066: Gurr, G. M., and O. L. Kvedaras Synergizing biological control: Scope for sterile insect technique, induced plant defences and cultural techniques to enhance natural enemy impact? Biol. Control 52: Hancock, D. L., E. L. Hamacek, A. C. Lloyd, and M. M. Elson-Harris The distribution and host plants of fruit flies (Diptera: Tephritidae) in Australia. Department of Primary Industries, Queensland, Australia, pp Harris, A. R., C. F. Pratt, A. J. Jessup, C. Banos, K. Lindhout, G. Gurr, and O. L. Reynolds Rearing the biological control agent Diachasmimorpha kraussii (Fullaway) (Hymenoptera: Braconidae) on irradiated larvae of the Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Proceedings of the 8th International Symposium on Fruit Flies of Economic Importance, Valencia, Spain 2010, pp Hee, A. K., and K. Tan Attraction of female and male Bactrocera papayae to conspecific males fed with methyl eugenol and attraction of females to male sex pheromone components. J. Chem. Ecol. 24: Hsu, J.-C., P.-F. Liu, M. Hertlein, R.F.L. Mau, and H.-T Feng Greenhouse and field evaluation of a new male annihilation technique (MAT) product, SPLAT-MAT Spinosad ME, for the control of Oriental fruit flies (Diptera: Tephritidae) in Taiwan. Form. Entomol. 30: Jackman, D. J, P. Bailey, B. Milton-Hine, N. Perepelicia, A. Jessup, and W. Brewer The integrated chemical and sterile insect technique to eradicate Queensland fruit fly at Glenside and Moana, Adelaide, South Australia. Primary Industries, South Australia, Australia, pp Leblanc, L., R. I. Vargas, B. Mackey, R. Putoa, and J. C. Pinero Evaluation of cue-lure and methyl eugenol solid lure and insecticide dispensers for fruit fly (Diptera: Tephritidae) monitoring and control in Tahiti. Fla. Entomol. 94: Lloyd, A. C., E. L. Hamacek, R. A. Kopittke, T. Peek, P. M. Wyatt, C. J. Neale, M. Eelkema, and H. Gu Area-wide management of fruit flies (Diptera: Tephritidae) in the Central Burnett district of Queensland, Australia. Crop Prot. 29: Meats, A., and C. L. Hartland Upwind anemotaxis in response to cuelure by the Queensland fruit fly, Bactrocera tryoni. Physiol. Entomol. 24: Patterson, H. D., and R. Thompson Recovery of inter-block information when block sizes are unequal. Biometrika 58: Perepelicia, N., K. Black, P. T. Bailey, M. A. Terras, L. Schinagl, and B. C. Dominiak The integrated chemical and sterile insect technique to eradicate Queensland fruit fly at Linden Park, Adelaide, South Australia. Primary Industries, South Australia, pp (PHA) Plant Health Australia Draft National Fruit Fly Strategy. Plant Health Australia, Canberra, Australia. Reynolds, O. L., C. J. Smallridge, V. G. Cockington, L. D. Penrose The effect of release method and trial site on recapture rates of adult sterile Queensland fruit fly, Bactrocera tryoni (Froggatt) (Diptera: Tephritidae). Aust. J. Entomol. 51: Reynolds, O. L., B. A. Orchard, S. Collins, and P. Taylor Yeast hydrolysate supplementation increases sterile Queensland fruit fly, Bactrocera tryoni (Froggatt) field longevity and abundance. Bull. Entomol. Res. 104: Schall, R Estimation in generalized linear models with random effects. Biometrika 78: Spinner, J. E., A. M. Cowling, G. M. Gurr, A. J. Jessup, and O. L. Reynolds Parasitoid fauna of Queensland fruit fly, Bactrocera tryoni Froggatt (Diptera: Tephritidae) in inland New South Wales, Australia and its potential for use in augmentative biological control. Aust. J. Entomol. 50: Stark, J. D., R. Vargas, and N. Miller Toxicity of spinosad in protein bait to three economically important tephritid fruit fly species (Diptera: Tephritidae) and their parasitoids (Hymenoptera: Braconidae). J. Econ. Entomol. 97: Stelinski, L. L., J. R. Miller, R. Ledebuhr, P. Siegert and L. J. Gut Season-long mating disruption of Grapholita molesta (Lepidoptera: Tortricidae) by one machine application of pheromone in wax drops (SPLAT-OFM). J. Pest Sci. 80: Sutherst, R. W., B. S. Collyer, and T. Yonow The vulnerability of Australian horticulture to the Queensland fruit fly, Bactrocera (Dacus) tryoni, under climate change. Aus. J. Agric. Res. 51: Vargas, R. I., J. D. Stark, M. Hertlein, A. M. Neto, R. Coler, and J. C. Pinero. 2008a. Evaluation of SPLAT with spinosad and methyl eugenol or cue-lure for attract-and-kill of oriental and melon fruit flies (Diptera: tephritidae) in Hawaii. J. Econ. Entomol. 101: Vargas, R. I., R.F.L. Mau, E. B. Jang, R. M. Faust, and L. Wong. 2008b. The Hawaii Fruit Fly Area-Wide Pest Management Program, pp In O.Koul,G.W.Cuperus,andN.C.Elliott(eds.),Areawide IPM: theory to implementation. CABI Books, London, United Kingdom. Vargas, R. I., J. C. Piñero, R.F.L. Mau, J. D. Stark, M. Hertlein, A. Mafra- Neto, R. Coler, and A. Getchell Attraction and mortality of oriental fruit flies to SPLAT-MAT-methyl eugenol with spinosad. Entomol. Exp. Appl. 131: Vargas, R. I., J. C. Pinero, E. B. Jang, R.F.L. Mau, J. D. Stark, L. Gomez, L. Stoltman and A. Mafra-Neto Response of Melon Fly (Diptera: Tephritidae) to weathered SPLAT-spinosad-cue-lure. J. Econ. Entomol. 103: Vargas, R. I., L. Leblanc, J. C. Pinero, and K. M. Hoffman. 2014a. Male annihilation, past, present, and future. In T. E. Shelly, N. Epsky, E. B. Jang, J.

7 1260 Journal of Economic Entomology, 2016, Vol. 109, No. 3 Reyes-Flores, and R. I Vargas (eds.), Trapping and the detection, control and regulation of tephritid fruit flies. Springer ScienceþBusiness Media Dordrecht, The Netherlands. Vargas, R. I., S. K. Souder, K. Hoffman, J. Mercogliano, T. R. Smith, J. Hammond, B. J. Davis, M. Brodie, and J. E. Dripps. 2014b. Attraction and mortality of Bactrocera dorsalis to STATICTM Spinosad ME weathered under operational conditions in California and Florida: a reduced-risk male annihilation treatment. J. Econ. Entomol. 107: White, I. M., and M. M Elson-Harris Fruit flies of economic significance: their identification and binomics. CAB International, Wallingford, United Kingdom. Zamek, A. L., O. L. Reynolds, S. Mansfield, J. L. Micallef, and G. M. Gurr Carbohydrate diet and reproductive performance of a fruit fly parasitoid, Diachasmimorpha tryoni. J. Insect Sci. 13: 74.