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Captures of Pest Fruit Flies (Diptera: Tephritidae) and Nontarget Insects in BioLure and Torula Yeast Traps in Hawaii LUC LEBLANC,1,2 ROGER I. VARGAS,3



Environ. Entomol. 39(5): 1626Ð1630 (2010); DOI: 10.1603/EN10090

ABSTRACT MultiLure traps were deployed in a Hawaiian orchard to compare the attraction of economically important fruit ßies and nontarget insects to the three-component BioLure and torula yeast food lures. Either water or a 20% propylene glycol solution was used to dissolve the torula yeast or as capture ßuid in BioLure traps. Torula yeast in water was more attractive than BioLure for male and female Bactrocera cucurbitae (Coquillett) and Bactrocera dorsalis (Hendel) and as attractive for Ceratitis capitata (Wiedemann), and the addition of propylene glycol signiÞcantly inhibited the attractiveness of torula yeast. The known synergistic effect of propylene glycol with BioLure, resulting in increased captures of Anastrepha ßies, was not observed with Bactrocera. Nontarget Drosophilidae, Neriidae, Phoridae, Calliphoridae, Sarcophagidae, and Muscidae were more strongly attracted to BioLure, and both lures collected Chloropidae equally. As with fruit ßies, propylene glycol in torula yeast signiÞcantly decreased nontarget captures. The results therefore suggest that torula yeast in water is a more effective attractant than BioLure for pest Bactrocera while minimizing nontarget captures. KEY WORDS nontarget, torula yeast, BioLure, Bactrocera, Ceratitis

Food lures have long been used in traps to monitor pest fruit ßies (Tephritidae), based on female protein requirement for egg maturation. Torula yeast pellets (Lopez-D. et al. 1971) have been widely used in traps, at times diluted in a propylene glycol (PPG) solution to prevent sample desiccation (Thomas and Robacker 2006), to monitor Bactrocera ßy populations during the Area-Wide Fruit Fly Management Program in Hawaii (Vargas et al. 2008). More recently, a synthetic dry food lure was developed for use primarily against the Mediterranean fruit ßy, Ceratitis capitata (Wiedemann), and Anastrepha ßies. This BioLure consists of three chemicals (ammonium acetate, trimethylamine hydrochloride, and putrescine) incorporated in slow-release membranes attached to the inside wall of a McPhail-type trap (Epsky et al. 1999). The three-component version is marketed for C. capitata, whereas a two-component version, excluding trimethylamine hydrochloride, is used to monitor Anastrepha spp. Target ßies entering the trap are captured on a sticky card or drowned in liquid. The addition of PPG in the capture liquid helps preserve fruit ßies for identiÞcation and dissection (Thomas et al. 2001, Martinez et al. 2007), and was 1 Department of Plant and Environmental Protection Sciences, University of Hawaii, 3050 Maile Way, Room 310, Honolulu, HI 96822. 2 Corresponding author: Department of Plant and Environmental Protection Sciences, University of Hawaii, 3050 Maile Way, Room 310, Honolulu, HI 96822-2271 (e-mail: [email protected]). 3 United States PaciÞc Basin Agricultural Research Center, United States Department of AgricultureÐAgricultural Research Service, P.O. Box 4459, Hilo, HI 96720.

determined to act synergistically with BioLure, increasing captures of Anastrepha ludens (Loew) and Anastrepha suspensa (Loew) (Thomas et al. 2001, Thomas 2008, Hall et al. 2005, Robacker and Czokajlo 2006). Although BioLure is now widely used to monitor Anastrepha spp and even control C. capitata through mass trapping (McQuate et al. 2005, NavarroLopis et al. 2008), little is known on its effectiveness at attracting Bactrocera fruit ßies. The undesirable attraction of nontarget insects to food lures has been documented in some detail in literature (Hardy 1952, Steyskal 1977, Neuenschwander et al. 1981, Asquith and Messing 1992, Katsoyannos et al. 1999, Thomas 2003, Conway and Forrester 2007, Martinez et al. 2007, Leblanc et al. 2010). Captures were consistently dominated by scavenger ßies, and also Lepidoptera in one study (Martinez et al. 2007), but the undesirable attraction of beneÞcial Chrysopidae (Neuenschwander et al. 1981, Thomas 2003, Martinez et al. 2007, Conway and Forrester 2007) and Tachinidae (Thomas 2003, Leblanc et al. 2010) was also reported. In Hawaii, BioLure traps captured large numbers of nontarget endemic Drosophilidae and Calliphoridae when traps were set in native forest (Leblanc et al. 2010). The objectives of our investigation were to compare attraction of Bactrocera and Ceratitis fruit ßies and the dominant nontarget insect families to BioLure and torula yeast in a Hawaiian orchard environment, and to determine whether the addition of PPG to food lure traps results in increased fruit ßy or nontarget attraction.

0046-225X/10/1626Ð1630$04.00/0 䉷 2010 Entomological Society of America

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Traps and Lures. MultiLure traps (Better World Manufacturing, Fresno, CA) were used for all treatments. The plastic trap consists of a transparent cover that interlocks with an opaque yellow base, allowing insect entry through a bottom opening and functioning as a collecting vessel for captured insects. Two different food lures were used. The Þrst was BioLure (Suterra LLC, Bend, OR) fruit ßy food lure, with the three sticky component membranes attached to the inner surface of the trap cover. Depending on the experiment, 200 ml of either water or a 20% aqueous solution of PPG (Sierra Antifreeze, Old World Industries, Northbrook, IL) was used in the bottom recipient to retain the trapped insects. The second lure treatment was prepared by dissolving two 5-g torula yeast pellets (2.25 g of torula yeast and 2.75 g of borax; ERA International, Freeport, NY), in 200 ml of either water or 20% PPG. Traps were hung on trees, 1.5Ð2 m above the ground, using 15-gauge aluminum tie wire, and at least 10 m apart to avoid interference among traps. Design. Forty-eight traps were deployed in the orange section of an unsprayed 5-ha citrus orchard (⬇200 tangerine and 1,000 orange trees) on Oahu Island (21⬚22⬘31”N, 158⬚02⬘44”W, 55 m elevation). Traps were arranged in a randomized block design, with eight rows (blocks) of six traps, with traps every third tree and every third row in the orchard. In each block, there were two BioLure traps, with water or 20% PPG; two traps with torula yeast, dissolved in water or 20% PPG; and two unbaited controls, with water or 20% PPG. Trap position within each block was randomly assigned. To prevent the frequent escape of fruit ßies after entering traps (Diaz-Fleischer et al. 2009), a small 12 ⫻ 12-mm strip with 10% dichlorvos (Vaportape II, Hercon Environmental, Emingsville, PA) was inserted in the lure receptacle built in the trap cover. Traps were emptied every 3Ð 4 d, with a total of seven collections over 24 d, in January 2010. After each collection, the water in the BioLure trap and all the torula yeast solutions were replaced, and all traps were shifted along blocks by one position. Sample Processing and Data Analysis. Collected insects were counted, sexed, and identiÞed to species. All counts were converted to number of insects per trap per day, subjected to the log(n⫹1) transformation to stabilize variance, and analyzed using analysis of variance (ANOVA; two-way), with the minimum variance unbiased quadratic estimation (PROC MIXED MIVQUE0, SAS Institute 2004). MIVQUE0 provides reliable estimates of parameters for data with a nonnormal distribution, large numbers of zero values, and unequal variances. In the mixed model, lure, preservative, and their interaction were treated as Þxed factors and block as a random factor. Capture data from the separate collections of each trap were used as replicate data for individual traps in the statistical analyses. Data were analyzed by individual species for the pest Tephritidae, and by family for all nontarget families represented by at least 200


specimens. Least square means estimates for each lure-preservative treatment were compared using TukeyÕs honest signiÞcant difference test. Means and standard errors are presented in their original, untransformed form. Pinned voucher specimens of all species were deposited at the University of Hawaii Insect Museum (Manoa, HI) and the Bernice P. Bishop Museum (Honolulu, HI).

Results and Discussion The traps collected all four Hawaiian pest tephritids (C. capitata, Bactrocera dorsalis [Hendel], Bactrocera cucurbitae [Coquillett], and Bactrocera latifrons [Hendel]) (38.4% of all captures). For both Bactrocera species, torula yeast in water consistently collected more ßies than BioLure traps, which attracted equal numbers of ßies, regardless of the presence or absence of PPG (Fig. 1). There was, however, a signiÞcant interaction between bait and preservative liquid for torula yeast, which sharply reduced captures when dissolved in PPG. Although C. capitata was captured in small numbers, torula yeast in water was as effective as either BioLure traps, and so few ßies were collected in torula yeast with PPG that captures were not statistically different from the unbaited controls (Fig. 1). The literature has repeatedly shown that BioLure is more attractive to C. capitata, at least at higher population densities, than either aqueous solutions of various protein hydrolysates (Gazit et al. 1998, Epsky et al. 1999, Katsoyannos et al. 1999, Cohen and Yuval 2000, Broughton and De Lima 2002) or torula yeast (Heath et al. 1997, Martinez et al. 2007). There was not a synergistic reaction between BioLure and PPG for the target ßies captured in our traps. Contrastingly, the addition of PPG to torula yeast drastically reduced captures for all species, possibly because the pH value of the baits may have increased, potentially exerting a negative inßuence in ßy captures (Heath et al. 2009). A similar 2-fold reduction was reported with A. suspensa captures in traps with torula yeast and 10% PPG (Hall et al. 2005), whereas Thomas and Robacker (2006) collected as many A. ludens in torula yeast, with or without PPG. Therefore, previous use of PPG in traps baited with torula yeast in Hawaii may have resulted in an underestimation of the ßy population densities. Both lures attracted a broad diversity of nonnative nontarget arthropods, covering 65 species, in 56 genera, 40 families, and 12 orders, dominated (⬎97%) by Diptera, mainly the Neriidae (61.9%, one species): Telostylinus lineolatus (Wiedemann), Chloropidae (24.1%, nine species), Phoridae (5.1%, three species), and Drosophilidae (3.1%, six species). Species in these and the other most consistently captured families (Lonchaeidae, Calliphoridae, Sarcophagidae, and Muscidae) are scavengers at the larval stage. The same species or families were also the dominant nontargets in other studies with detailed nontarget listings (Steyskal 1977, Asquith and Messing 1992, Thomas 2003, Leblanc et al. 2010), and are strongly attracted to



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Fig. 1. Captures (mean ⫾ SEM per trap per day) of pest fruit ßies (B. cucurbitae, B. dorsalis, and C. capitata) in traps baited with three-component BioLure or torula yeast, with water or 20% PPG as liquid preservative. Values in each species-sex with the same letter are not signiÞcantly different at the P ⫽ 0.05 level, ANOVA, PROC MIXED MIVQUE0 (SAS Institute 2004). Numerator and denominator degrees of freedom for F values are 2,323 for lure effect, 1,323 for preservative effect, and 2,323 for their interaction, and F values are displayed in that order for each species-sex. P ⬍ 0.0001 for all effects, unless otherwise indicated. B. cucurbitae: females, F ⫽ 344.41, 16.09, 33.06, and males, F ⫽ 255.06, 16.27, 12.95; B. dorsalis: females, F ⫽ 177.63, 30.31, 32.40, and males, F ⫽ 83.48, 8.59 (P ⫽ 0.0036), 15.82; C. capitata: females, F ⫽ 54.29, 4.41 (P ⫽ 0.0365), 6.24 (P ⫽ 0.0022), and males, F ⫽ 27.22, 0.63 (P ⫽ 0.4265), 3.70 (P ⫽ 0.0258).

decaying fruit ßies that accumulate inside male lure traps (Uchida et al. 2007, Leblanc et al. 2009). Overall nontarget captures in BioLure were significantly higher than in torula yeast, and not affected by the presence (39.97 ⫾ 6.77) or absence (40.53 ⫾ 6.40) of PPG in the capture ßuid (Fig. 2). In contrast, there was a signiÞcant difference in captures in torula yeast traps with water (16.22 ⫾ 1.59) versus those with PPG (8.08 ⫾ 0.82). In all groups except for the Chloropidae, BioLure collected at least as many individuals as torula yeast in water, whereas torula yeast in PPG collected

as few nontargets as the unbaited controls. Whereas the Neriidae were consistently strongly attracted to BioLure, with and without PPG, there were marked differences for the other groups, with drosophilids and calyptrate ßies more numerous in traps with water alone, and more Phoridae captured in traps with PPG. Torula yeast in water collected as many Chloropidae as BioLure with PPG, and fewer, but equal numbers were trapped in either torula yeast with PPG or BioLure with water. Unbaited control traps, with or without PPG, did not attract nontargets (0.88 ⫾ 0.10 per

Fig. 2. Captures (mean ⫾ SEM per trap per day) of nontarget insects in traps baited with three-component BioLure or torula yeast, with water or 20% PPG as liquid preservative. Values in each species-sex with the same letter are not signiÞcantly different at the P ⫽ 0.05 level, ANOVA, PROC MIXED MIVQUE0 (SAS Institute 2004). Numerator and denominator degrees of freedom for F values are 2,323 for lure effect, 1,323 for preservative effect, and 2,323 for their interaction, and F values are displayed in that order for each family. P ⬍ 0.0001 for all effects, unless otherwise indicated. Drosophilidae (introduced): F ⫽ 54.49, 20.73, 14.89; Chloropidae: F ⫽ 314.00, 1.51 (P ⫽ 0.2204), 17.50; T. lineolatus: F ⫽ 435.54, 29.75, 26.56; Phoridae: F ⫽ 29.83, 1.88 (P ⫽ 0.1707), 17.55; calyptrate Diptera: F ⫽ 30.12, 10.44 (P ⫽ 0.0014), 2.62 (P ⫽ 0.0747).

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trap per day). Although there was no consistent evidence of synergy between PPG and BioLure for nontargets or fruit ßies in our study, PPG should still be included in wet BioLure traps, because captured insects quickly start decaying in water-based traps after 5 d, accelerating nontarget attraction (L. L., unpublished observations). In contrast with our results in this study, previous studies indicated that aqueous solutions of torula yeast collected more nontarget ßies (Heath et al. 1995, Thomas 2003, Martinez et al. 2007) and Hymenoptera (Martinez et al. 2007), but fewer Lepidoptera (Martinez et al. 2007) and Chrysopidae (Thomas 2003, Conway and Forrester 2007, Martinez et al. 2007) than BioLure. The only exception was the equal capture of nontarget ßies in BioLure and torula yeast, incidentally both with 10% PPG, reported by Conway and Forrester (2007). The factors bearing on attraction for nontarget taxa require further study to determine whether there are strong regional and taxonomic biases in the speciÞcity of BioLure or torula yeast. The implication of our results and the strong endemic nontarget attraction to BioLure in Hawaii (Leblanc et al. 2010), however, is of primary concern for the conservation of rare Hawaiian insects. BeneÞcial predators, parasitoids, and pollinators were not collected in our study, but the possibility of lacewing (Neuroptera) and tachinid (Diptera) attraction to BioLure cannot be overlooked in a large-scale control context. Our results suggest that no single food attractant used in one trap works efÞciently for both Ceratitis and Bactrocera in Hawaii. However, the attraction of Bactrocera ßies to various combinations of the BioLure components is worth further investigation, because the three-component lure, strongly attractive to C. capitata, may not be as attractive as a twocomponent combination, as was documented with A. ludens (Heath et al. 2004), and the omission of putrescine still results in strong attraction of C. capitata (Leblanc et al. 2010). More comparative trapping should also be considered at higher Bactrocera densities.

Acknowledgments We are grateful to Alec Sou (Aloun Farms) for access to his citrus orchard. Mark G. Wright and Jaime C. Pinero (University of Hawaii, Manoa Campus) have provided advice on data analysis and improvement of the manuscript, and Ming-Yi Chou (UH Manoa) assisted in setting up the traps and preliminary sample sorting. This work was supported by United States Department of AgricultureÐAgricultural Research Service through a SpeciÞc Cooperative Agreement with University of HawaiiÕs College of Tropical Agriculture and Human Resources (0500-00044-016-07) titled “Study of Attraction of Nontarget Organisms to Fruit Fly Female Attractants and Male Lures in Hawaii,” and United States Department of Agriculture Cooperative State Research, Education and Extension Project HAW00942-H, administered by College of Tropical Agriculture and Human Resources.


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