Field Studies of Synthetic Food-Based Attractants for Detecting Invasive Fruit Flies (Diptera: Tephritidae)

doi:10.21203/rs.3.rs-3694604/v1

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Field Studies of Synthetic Food-Based Attractants for Detecting Invasive Fruit Flies (Diptera: Tephritidae)

https://doi.org/10.21203/rs.3.rs-3694604/v1

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A number of true fruit fly species (Diptera: Tephritidae) threaten the production and international trade of many commercially important fruit and vegetable crops. Many fruit fly-free regions operate continuous trapping programs for the detection of these invasive pests. Food baits are an important component of detection trapping as they are general attractants that are neither sex- nor species-specific. A torula yeast-borax solution has been widely used as a food bait, but it has a relatively short field longevity and is generally replaced every 1–2 weeks. Dry synthetic food-based attractants, consisting of ammonium acetate, putrescine, and trimethylamine, have been developed and appear effective for several months in the field. Initially, the three components were presented in individual sachets within a trap, but to ease handling ‘all-in-one’ dispensers have been developed that contain all three components. While a logistical improvement, there are few data that directly compare captures between the standard torula yeast-borax solution and these combination dispensers. The present paper presents the results of several field experiments assessing the relative effectiveness of three ‘all-in-one’ dispensers of synthetic food-based attractants in trapping three major pest species of tephritid fruit flies in Hawaii. Food cone and BioLure Unipak dispensers were significantly less attractive than the torula yeast-borax mixture for all target species, while captures of the Mediterranean fruit fly were similar in traps baited with TMA TRI Difusor sachets or the torula yeast-borax solution.

Trapping

Detection

Food baits

Tephritidae

Hawaii

Tephritid fruit flies (Diptera: Tephritidae) are serious pests of many commercially important fruits and vegetables (White and Elson-Harris 1992; Dias et al. 2018). Consequently, southern states in the USA with large horticultural production, notably California, Florida, and Texas, operate large-scale trapping networks to monitor incursions of fruit fly pests (USDA 2015). These detection programs rely heavily on traps baited with male-specific attractants, termed male lures. While male lures are powerful attractants, several factors limit their effectiveness. As the name implies, they are sex-specific and attract only males. In addition, male lures are taxonomically specific, and a particular lure attracts only males of species in the same genus or closely related genera (Tan et al. 2014). Finally, males of many tephritid species do not respond to any male lure, consequently male lures are effective for only a subset of economically important tephritid species (Drew and Hooper 1981; Royer 2015).

Owing to these limitations, detection programs usually include traps baited with food-based attractants. Food baits do not suffer the limitations noted for male lures, as they are neither sex- nor taxon-specific (Epsky et al. 2014). A commonly used food bait, and one described as the standard food attractant in tephritid trapping programs worldwide, is torula yeast (Heath et al. 1995). Torula yeast is presented in an aqueous solution, often containing propylene glycol to reduce evaporation and decomposition of trapped insects (Thomas 2008), that contains dissolved pellets of enzymatic hydrolyzed yeast with borax included to reduce decomposition of the bait as well as captured insects (Thomas 2008; Epsky et al. 2014). The torula yeast-borax slurry (TYB hereafter) acts both as the attractant and catch mechanism as the attracted flies drown in the liquid (Thomas et al. 2001).

While recognized as a useful attractant, TYB is considered to have several shortcomings, namely variability in the chemical composition of the pellets (Epsky et al. 2014), a relatively short period of effectiveness in the field, with replacement requirement required every 1–2 weeks (Calkins et al. 1984; FAO/IAEA 2018; but see Torres-Quezada et al. 2021), and capture of large numbers of non-target organisms (Heath et al. 1995; Thomas 2003; but see Leblanc et al. 2010). As a result, the use of dry food-based synthetic attractants has been investigated, with focus on formulations of three compounds, ammonium acetate, putrescine, and trimethylamine, or two compounds, ammonium acetate and putrescine only without trimethylamine (Heath et al. 1995, 1997; Epsky et al. 1999, 2011; Broughton and de Lima 2002). Initially, these synthetic baits (commercially available as BioLure [Suterra LLC, Bend, OR, USA], Epsky et al. 2010) were dispensed individually from sachets placed within the trap (Epsky et al. 2014). However, the placement of multiple packets was considered cumbersome (Jang et al. 2007; Holler et al. 2009), and dispensers were developed that contained all components in a single device. These dispensers are either sachets similar in construction to the individual packets (e.g., BioLure Unipak [Suterra LLC, Bend, OR, USA] and Trypak [Sanidad Agricola Econex, Santomera, Spain]) or cone-shaped devices (Scentry Biologicals Inc., Billings, MT, USA). For both individual and ‘all-in-one’ dispensers, data suggest that the synthetic food baits are attractive for 4–12 weeks (Epsky et al. 1999; Katsoyannos et al. 1999; Miranda et al. 2001; Martinez et al. 2007; Navarro-Llopis et al. 2008).

A number of studies have directly compared fly captures in traps baited with individual, synthetic food-bait dispensers versus traps baited with standard TYB or other liquid protein (e.g., NuLure). These have generally, but not always (Heath et al. 1995; Conway and Forrester 2007; Leblanc et al. 2010), shown that captures were significantly greater for the synthetic food baits (Heath et al. 1997; Epsky et al. 1999, 2011; Katsoyannos et al. 1999; Miranda et al. 2001; Martinez et al. 2007). In contrast, relatively few studies (Jang et al. 2007; Shelly et al. 2020, 2022; Vázquez et al. 2022) have compared the efficacy of ‘all-in-one’ synthetic food-based dispensers to liquid protein lures despite increasing use of these combination baits in detection programs (e.g., food cones are now used in Florida and Texas surveillance trapping, A. Fox and G. Gracia, respectively, pers. comm.) or mass-trapping efforts (e.g., BioLure Unipak and Tripack in Tunisian citrus orchards, Boulahia Kheder et al. 2012; Hafsi et al. 2015). Moreover, with respect to detection trapping, the data regarding the relative efficacy of synthetic food-based dispensers and liquid protein baits have been inconsistent.

The present study describes several field experiments designed to provide additional data regarding the effectiveness of dispensers containing ≥ 2 synthetic food attractants relative to TYB. As described below, the multicomponent dispensers tested included Biolure Unipaks (Suterra), food cones (Scentry), and Difusors (Susbin SA, Mendoza, Argentina), and the target species included the Mediterranean fruit fly (medfly), Ceratitis capitata (Wiedemann), the oriental fruit fly, Bactrocera dorsalis (Hendel), and the melon fly, Zeugodacus cucurbitae (Coquillett), all of which are important agricultural pests (White and Elson-Harris 1992). Inclusion of the latter two species is of particular interest, as the great majority of studies on tephritid fruit fly food baits have been conducted on C. capitata and various Anastrepha spp.

Experiment 1: Comparison of torula yeast borax, three-component food cones, and BioLure Unipak sachets.

Study site. Trapping was conducted in a coffee field (Coffea arabica L.; area 65 ha, elevation 90 m) approximately 10 km southeast of Haleiwa, Oahu, Hawaii, USA. Plants were 2–4 m tall and were grown in parallel rows spaced 2–3 m apart. Within a row, trunks of the individual plants were separated by 1–2 m, but foliage was generally contiguous between neighboring plants. Trapping was conducted during August - September 2022, with C. capitata and B. dorsalis captured in sufficient numbers for statistical analysis. Average daily minimum and maximum temperatures over this interval were 20.1^oC and 29.2^oC, respectively (Wheeler Army Airfield, Wahiawa, HI, approximately 10 km from the site).

Food baits. Following standard protocol, TYB solution was prepared by dissolving one TYB pellet (5 g; Scentry Biologicals Inc., Billings, MT, USA) per 100 mL of a water/antifreeze solution (90:10 v:v; SPLASH RV and Marine Antifreeze [14% propylene glycol], SPLASH Products Inc., St. Paul, MN, USA). TYB was prepared anew for each trapping period and served as a standard against which the other baits were compared (see below). In the field, 300 mL of the solution were placed in individual Multilure traps (Better World Manufacturing Inc., Fresno, CA, USA), which are two-piece, plastic McPhail-like traps (FAO/IAEA 2018). The top portion is clear, while the bottom is bright yellow and holds the liquid food bait. The bottom of the trap has a central, open invagination through which insects enter; the liquid reservoir acts as the killing mechanism. A wire hanger at the top of the trap is used to suspend the trap from tree branches.

Both the food cones (Scentry Biologicals Inc., Billings, MT, USA) and BioLure Unipak sachets (Suterra LLC, Bend, OR, USA; hereafter Unipaks) were comprised of ammonium acetate, putrescine, and trimethylamine, but the amounts differed between the baits. The amounts of ammonium acetate, putrescine, and trimethylamine in the food cones were 5.0, 0.55, and 1.5 g, respectively, compared to 6.1, 0.04, and 2.5 g, respectively, in the Unipaks. Both baits were deployed in Multilure traps. Food cones (height 5 cm, base diameter 2 cm) were placed in a capped, slitted well built into the top of the trap. The Unipak sachets were plastic packets (9.5 cm squares) with a circular opening on one side to allow release of the odor. A Unipak was suspended from a metal hook affixed to the top portion of the trap. Thus, both the food cones and Unipaks were suspended in the upper part of the trap above the bottom reservoir. For traps baited with food cones or Unipaks, we placed 300 mL of the water/antifreeze solution (90:10 volumetric proportions as above) in the bottom reservoir.

Unlike the TYB bait, which as noted above was prepared fresh for each trapping period, the food cones and Unipaks were fresh for the initial sampling period but then aged for use in the subsequent sampling periods. To weather these baits, Multilure traps containing food cones or Unipaks (but without liquid in the bottom of the trap) were hung about 2 m above ground in a covered area adjacent to the USDA laboratory in Aiea, Oahu, Hawaii, under similar environmental conditions as the trapping site.

Trap deployment and processing. Trapping was conducted at 0 weeks (all baits fresh) and after the food cones and Unipaks were weathered for 2, 4, and 6 weeks. Ten traps were used for each of the three treatments (i.e., 30 total traps), with one trap/treatment placed in each of 10 plant rows. Within a row, neighboring traps were separated by 10–12 m, and trap-bearing rows were spaced 12–15 m apart. Traps were placed at the same sites over all sampling periods, with treatment positions within rows randomized for each sampling period. Traps were deployed between 9:00 am and 10:00 am and operated for 2–3 days. When a trap was collected, the liquid was poured through a sieve to retain the catch, and samples were returned to the laboratory to identify and count the flies.

Experiment 2: Comparison of TYB and TMA TRI Difusor Lures

Study site. Trapping was conducted in the same coffee field described above during October - November 2022 with C. capitata and B. dorsalis again captured in sufficient numbers for statistical analysis. Average daily minimum and maximum temperatures over this interval were 19.3^oC and 27.4^oC, respectively (Wheeler Army Airfield, Wahiawa, HI).

Food baits. Two food baits, which were presented in Multilure traps, were compared in this experiment – TYB solution and TMA TRI Difusor sachets (Susbin SA, Mendoza, Argentina; hereafter 3C Difusor lures). The 3C Difusor lures contained the same three components as the food cones and Unipaks but in different quantities, namely 7.7 g ammonium acetate, 0.01 g putrescine, and 2.8 g trimethylamine. Like the Unipaks, the 3C Difusors were plastic sachets (10 by 6 cm) with an opening on one side to allow release of the odor and were suspended by a hook from the top of the Multilure trap. As in the previous experiment, the TYB was prepared fresh for each trapping period, while the 3C Difusor sachets were weathered over the course of the study following the above protocol.

Trap deployment and processing. Trapping was conducted at 0 weeks (all baits fresh) and after 3C Difusor lures were weathered for 2, 4, and 6 weeks. Twelve traps were used for each treatment (i.e., 24 total traps), with one trap of each treatment placed in 12 different plant rows. Traps operated for 2–3 days, and trap placement and processing followed the same protocol as Experiment 1.

Experiment 3: Comparison of TYB, food cones, and 3C Difusor Lures

Study site. Trapping was conducted in the same coffee field described above during February - May 2023. Average daily minimum and maximum temperatures over this interval were 18.1^oC and 27.0^oC, respectively (Wheeler Army Airfield, Wahiawa, HI).

Food baits. Three food baits, which were presented in Multilure traps, were compared in this experiment – TYB solution, food cones, and 3C Difusor sachets. As in the previous experiments, the TYB was prepared fresh for each trapping period, while the food cones and 3C Difusor lures were weathered over the course of the study following the above protocol.

Released insects. Unlike the previous experiments, this experiment utilized released insects obtained from a mass-rearing facility. Non-irradiated pupae of C. capitata were obtained from the California Department of Food and Agriculture facility in Waimanalo, HI. Approximately 10,000 pupae of each sex were placed in PARC boxes (1 box per sex) in the USDA-PPQ-S&T fruit fly laboratory, Aiea, HI. Upon adult emergence, slabs of a sugar and protein hydrolysate mixture (3:1 v:v) were placed on the lid’s screened central portion along with water-soaked sponges. Food was replenished as needed, and the sponges were rehydrated daily. Pupae were procured and placed in the PARC boxes 3–4 days before emergence, and adults were released 4–5 days after emergence. Holding conditions were 25-27^oC, 50%-80% rh, and a 12:12 L:D photoperiod under artificial and natural light.

Trap deployment and insect release. Trapping was conducted at 0 weeks (all baits fresh) and after food cones and 3C Difusor lures were weathered for 2, 4, 6, 8, 12, and 16 weeks. Preliminary sampling with the male lure trimedlure indicated that the wild population of C. capitata was very small (ripe fruits were absent both before and during the experiment). The flies were released from a central point, and traps were placed equidistantly along the circumference of a circle of 25 m radius (adjacent traps were approximately 7 m apart). Traps were placed in repeating sequences around the circle (3 baits x 8 traps per bait = 24 total traps), with the positions of the baits advanced one site between successive trapping periods to minimize potential position effects. Traps were deployed immediately before insect release between 9 am and 9.30 am and were collected 2 days later.

To release flies, the two PARC boxes were placed on the ground several meters apart near the center of the circular plot. Females were released 15–20 min before males. For both sexes, the box lid was removed, and the insects left the box on their own volition. After 20–30 min, the boxes were tapped gently to induce flight in the remaining flies. On four occasions, we collected dead flies from the boxes and counted them at the laboratory. On average, 352.5 males (range: 249–548) and 295.4 females (range: 155–477) were found dead in individual boxes, representing approximately 3% mortality for each sex.

Experiment 4: Comparison of TYB and two component (2C) and 3C Difusor Lures

Study site. Trapping was conducted during June-August 2023 at the edge of second-growth forest (170 m elevation) approximately 10 km south of Hilo on Hawaii Island (Big Island), Hawaii, USA with B. dorsalis and Z. cucurbitae captured in sufficient numbers for statistical analysis. Host fruits (mainly papaya, Carica papaya L., and guava, Psidium guajava L.) were abundant in nearby fields. Average daily minimum and maximum temperatures over this interval were 18.3^oC and 26.2^oC, respectively (NOAA, Keaau, HI, approximately 6 km from the site).

Food baits. Three food baits, which were presented in Multilure traps, were compared in this experiment – TYB solution and two component (2C) and 3C Difusor lures. The 2C Difusor lures contained 9.7 g of ammonium acetate and 0.03 g of putrescine, but no trimethylamine. As in the previous experiments, the TYB was prepared fresh for each trapping period, while the food cones and Difusor lures were weathered over the course of the study following the above protocol.

Trap deployment. Trapping was conducted at 0 weeks (all baits fresh) and after 2C and 3C Difusor lures were weathered for 3, 6, 9, and 12 weeks. Traps were placed in repeating sequences along the forest edge (3 baits x 12 traps per bait = 36 total traps), with 10 m separating adjacent traps. Traps were deployed between 7.30–8.30 hrs and collected 1 day later. The positions of the baits were advanced one site between successive trapping periods to minimize potential position effects.

Statistical analyses

For each experiment and each species, we first compared sex ratios of captured flies among traps containing different food baits. For Experiments 1 and 2, data from individual traps were included only if they contained ≥ 10 individuals, while for Experiments 3 and 4, traps were included only if they contained ≥ 20 individuals. Sex ratios (number of females/ total captures) observed in individual traps were then compared among treatments, using data from all sampling periods, with the Mann-Whitney test (test statistic T) for pair wise comparisons or the Kruskal-Wallis test (test statistic H) for cases with > 2 groups. If sex ratio varied significantly among different food baits, capture data were analyzed separately for females and males. Also, if significant variation was detected with the Kruskal-Wallis test, Dunn’s multiple comparison test (P = 0.05) was used to identify differences among the bait types (Daniel 1990). If between-treatment variation was not significant, capture data for females and males were pooled for each food bait.

For all experiments (except Experiment 3), the numbers of captures in individual traps (expressed as flies per trap per day or FTD) were analyzed using generalized linear models (GLMs), with bait and week as independent variables. For Experiment 3, GLM was run using data from the 2-day post-release trapping period. In all cases, data were non-normal, and a Poisson distribution was chosen with the log link. The significance of the independent variables was tested using a likelihood ratio chi-square, with df = 2 for food bait for Experiments 1, 3, and 4 and df = 1 for food bait for Experiment 2. For week, df = 3 for Experiments 1 and 2, df = 6 for Experiment 3, and df = 4 for Experiment 4. The nonparametric Wilcoxon rank sum test was used to identify significant differences in pairwise comparisons of the different food treatments, using the normal approximation (test statistic Z) for significance testing. As noted below, week had a significant effect on captures in all experiments, which likely reflected (i) natural variation in the size of wild populations and/or (ii) variable environmental conditions, particularly wind speed, that affected the ability of flies to orient toward and locate traps. Because the potential impact of these two factors were not monitored, analysis focused on identifying differences among bait treatments. GLMs were performed with JMP 14 software (SAS Institute, Cary, NC, US).

Experiment 1: Comparison of TYB, food cones, and Unipaks

For medfly, sex ratios did not vary significantly among treatments (H = 5.6, df = 2, P = 0.06, N = 31, 12, and 17 for TYB, food cones, and Unipaks, respectively, consequently the sexes were pooled for analysis. Captures were female-biased for all baits, with females comprising an average of 72% − 86% across the different food baits. For the oriental fruit fly, sex ratios were female-biased as well but varied significantly among the treatments. On average, females comprised 80% of the captures in traps baited with TYB (N = 39) compared to only 63% for traps baited with food cones (N = 24; T = 451.5, P < 0.001; no Unipak-baited traps captured ≥ 10 oriental fruit flies).

For C. capitata, both week (ꭓ² = 28.4, P < 0.001) and bait (ꭓ² = 105.0, P < 0.001) had significant effects on captures (Fig. 1). The interaction was significant as well (ꭓ² = 18.1, P < 0.01). Traps baited with TYB captured significantly more flies than traps baited with food cones (Z = 5.9, P < 0.001) or Unipaks (Z = 5.3, P < 0.001). Captures did not differ significantly between food cones and Unipaks (Z = 0.6, P = 0.56).

For B. dorsalis females, both week (ꭓ² = 15.0, P < 0.01) and bait (ꭓ² = 894.1, P < 0.001) had significant effects on captures (Fig. 2). The interaction was significant as well (ꭓ² = 28.6, P < 0.001). Traps baited with TYB captured significantly more females than traps baited with food cones (Z = 7.4, P < 0.001) or Unipaks (Z = 7.7, P < 0.001), and captures were significantly higher for food cones than Unipaks (Z = 6.1, P < 0.001). For B. dorsalis males, bait (ꭓ² = 174.1, P < 0.001) had a significant effect on captures, but week (ꭓ² = 5.9, P = 0.11) did not (Fig. 2). As with females, traps baited with TYB captured significantly more males than traps baited with food cones (Z = 3.9, P < 0.001) or Unipaks (Z = 7.3, P < 0.001), and captures were significantly higher for food cones than Unipaks (Z = 5.8, P < 0.001).

Experiment 2: Comparison of TYB and 3C Difusor Lures

For medfly, sex ratios did not vary significantly among treatments (T = 235.0, P = 0.88, N = 18 and 14 for TYB and 3C Difusor lure, respectively), consequently the sexes were pooled for analysis. Captures were female-biased for both baits, with females comprising an average of 70% and 69% of the catch in TYB- and 3C Difusor lure-baited traps, respectively. For the oriental fruit fly, sex ratios were female-biased as well but varied significantly between TYB and 3C Difusors. On average, females comprised 82% of the captures in traps baited with TYB (N = 29) compared to 71% for traps baited with the 3C Difusor lures (N = 15; T = 214.0, P = 0.002).

For C. capitata, week (ꭓ² = 99.4, P < 0.001) had a significant effect on captures, but bait did not (ꭓ² = 0.3, P = 0.56; Fig. 3). The interaction was not significant (ꭓ² = 2.3, P = 0.51).

For B. dorsalis females, both week (ꭓ² = 74.5, P < 0.001) and bait (ꭓ² = 73.6, P < 0.001) had significant effects on captures (Fig. 4). The interaction was significant as well (ꭓ² = 43.8, P < 0.001). Traps baited with TYB captured significantly more females than traps baited with the 3C Difusor lure (Z = 4.1, P < 0.001). For B. dorsalis males, both week (ꭓ² = 8.7, P < 0.03) and bait (ꭓ² = 17.3, P < 0.001) had significant effects on captures (Fig. 4). The interaction was significant as well (ꭓ² = 31.4, P < 0.001). Traps baited with TYB captured significantly more males than traps baited with 3C Difusor lure (Z = 2.9, P = 0.003).

Experiment 3: Comparison of TYB, food cones, and 3C Difusor lures

This experiment utilized released medflies, and all analyses refer to this species. Sex ratios were female-biased for all food baits, but there was significant variation among them (H = 41.8, df = 2, P < 0.001). On average, females comprised 81% of the total captures for TYB (N = 50), 55% for food cones (N = 32), and 62% for 3C Difusor lures (N = 48). Sex ratios for TYB were significantly greater than those for food cones or 3C Difusor lures, while no difference was found between these latter treatments (Dunn’s test, P > 0.05).

For females, both week (ꭓ² = 1645.4, P < 0.001) and bait (ꭓ² = 593.3, P < 0.001) had significant effects on captures (Fig. 5). The interaction was significant as well (ꭓ² = 506.8, P < 0.001). Traps baited with TYB captured significantly more females than traps baited with food cones (Z = 4.8, P < 0.001) but similar numbers to traps baited with 3C Difusor lures (Z = 1.8, P = 0.06). The 3C Difusor lures also attracted significantly more females than food cones (Z = 3.0, P < 0.01). For males, both week (ꭓ² = 1823.7, P < 0.001) and bait (ꭓ² = 137.4, P < 0.001) had significant effects on captures (Fig. 5). The interaction was significant as well (ꭓ² = 1003.4, P < 0.001). Traps baited with 3C Difusors captured significantly more males than traps baited with TYB (Z = 3.1, P = 0.002) or food cones (Z = 2.3, P = 0.03). Male captures did not differ significantly between TYB and food cones (Z = 0.5, P = 0.58).

Experiment 4: Comparison of TYB and 2C and 3C Difusor lures

For the oriental fruit fly, captures were < 20 individuals for all traps with 2C or 3C Difusor lures, and comparisons among treatments were conducted using total captures (sexes combined). Over all traps and sampling periods, sex ratios were female-biased for all treatments: 73% for TYB, 83% for 2C Difusors and 81% for 3C Difusors. For the melon fly, sex ratios were female-biased as well but varied significantly among treatments (H = 12.7, P < 0.01). Sex ratio for TYB traps (74%, N = 57) was significantly greater than that observed for 2C Difusor lures (66%, N = 57) but similar to that observed for 3C Difusors (71%, N = 46). Sex ratio did differ significantly between 2C and 3C Difusor lures. between TYB and 3C Difusors (Dunn’s test, P = 0.05).

For C. dorsalis, both week (ꭓ² = 277.5, P < 0.001) and bait (ꭓ² = 1350.2, P < 0.001) had significant effects on captures (Fig. 6). The interaction was significant as well (ꭓ² = 54.6, P < 0.01). Traps baited with TYB captured significantly more flies than traps baited with 2C (Z = 7.9, P < 0.001) or 3C Difusor lures (Z = 8.3, P < 0.001). Captures did not differ significantly between 2C and 3C Difusors (Z = 1.3, P = 0.19).

For Z. cucurbitae females, both week (ꭓ² = 1280.8, P < 0.001) and bait (ꭓ² = 665.2, P < 0.001) had significant effects on captures (Fig. 7). The interaction was significant as well (ꭓ² = 51.9, P < 0.001). Traps baited with TYB captured significantly more females than traps baited with 2C (Z = 3.7, P < 0.001) or 3C (Z = 6.2, P < 0.001), and captures were significantly higher for 2C than 3C Difusors (Z = 3.3, P < 0.001). For Z. cucurbitae males, both week (ꭓ² = 107.4, P < 0.001) and bait (ꭓ² = 5.9, P < 0.001) had significant effects on captures (Fig. 7). The interaction was significant as well (ꭓ² = 49.7, P < 0.001). Traps with TYB captured significantly more males than traps baited with 2C (ꭓ² = 2.1, P = 0.03) or 3C (ꭓ² = 5.5, P < 0.001) Difusor lures, and captures were significantly higher for 2C than 3C Difusors (Z = 4.2, P < 0.001).

The present study generated several key findings regarding the efficacy of multicomponent synthetic food-based attractants relative to the standard TYB bait. First, the Unipaks were significantly less effective than TYB for capturing either C. capitata or B. dorsalis (Experiment 1). To our knowledge, no prior data exist for any Bactrocera species, but Holler et al. (2009) reported no difference in captures of C. capitata and Anastrepha suspensa (Loew) between Unipaks and individual sachets of the different components. As several previous studies (e.g., Heath et al. 1997; Epsky et al. 1999; Miranda et al. 2001; Martinez et al. 2007) found that the BioLure individual packets were as effective as TYB, it was expected that the BioLure Unipak would be at least as attractive as TYB. Moreover, BioLure Unipaks have been used in mass-trapping programs in Europe and North Africa (Boulahia Kheder et al. 2012; Navarro-Llopis et al. 2013; Ben Chaaban et al. 2018) and appear effective in reducing medfly populations over periods of 2–4 months. Why the Unipaks performed poorly in this study and for C. capitata, in particular, is not known.

Second, food cones were less effective than TYB in capturing females of C. capitata females (Experiments 1 and 3) or females and males of B. dorsalis (Experiment 1). TYB-baited traps captured more C. capitata males than food cone-baited traps in Experiment 1, while captures of male medflies were similar for these two baits in Experiment 3. These results are consistent with recent studies (Shelly et al. 2020, 2022, 2023) conducted in Hawaii, showing that food cones are generally inferior attractants relative to TYB for C. capitata, B. dorsalis, or Z. cucurbitae. Similarly, Vázquez et al. (2022), working in Florida, found that TYB-baited traps captured more A. suspensa of both sexes than food cone-baited traps. In contrast, Jang et al. (2007), also working in Florida, found no difference in captures between TYB- or food cone-baited traps for C. capitata or A. suspensa. However, these authors used mass-reared, released flies exclusively, and for C. capitata only males were released (from the genetic sexing strain used in the Florida Preventative Release Program, Jang et al. 2007). Thus, it is possible that the use of mass-reared as opposed to wild flies and/or the release protocol (specifically, the location of release sites vis-à-vis trap positions) may account for the differences noted between Jang et al. (2007) and the aforementioned studies.

Finally, compared to TYB, the 3C Difusor lures were found to be equally effective in capturing C. capitata (Experiment 2 and 3) but less effective in capturing B. dorsalis (Experiment 2 and 4) or Z. cucurbitae (Experiment 4). To our knowledge, only two published studies have evaluated the effectiveness of 3C Difusor lures. Navarro-Llopis et al. (2008) did not include TYB in their set of tested food baits but found that 3C Difusors were as effective as other synthetic food baits in attracting C. capitata over a 6-week period in a Spanish citrus grove. Delgado et al. (2022) worked in three orchards over two seasons in Uruguay and observed that medfly captures with 3C Difusor lures exceeded captures with TYB in all instances except one. This study also reported no difference in captures of Anastrepha fraterculus (Wiedemann) in traps baited with 2C Difusor lures and TYB.

In conclusion, the data provided here indicate that, with respect to C. capitata, the 3C Difusor performed as well as TYB, while the Unipaks and food cones were significantly less attractive than TYB. With respect to B. dorsalis and Z. cucurbitae, none of the synthetic baits tested was as effective as TYB. Thus, among the baits studied here, TYB was most effective in attracting all three of the target species. Despite its wide usage, the relative attractiveness of individual TYB volatiles, and the likely synergy or antagonism among them, are not well known, a task made difficult by the complexity of the full TYB aroma. Buttery et al. (1983), for example, identified 43 volatile chemicals derived from PIB-7, a corn-based protein bait. Ammonium is one release product known to modulate tephritid fruit fly attraction to food baits (Bateman and Morton 1981; Mazor et al. 1987), but its importance appears to vary with the presence and/or amount of other protein-derived odors (Piñero et al. 2020; Lasa and Williams 2021a,b). In attempting to improve the potency of protein-based food baits for tephritids, a productive approach (and one used for the spotted wing Drosophila, D. suzukii (Matsumura); Cha et al. 2014) may involve assessing the attractiveness of constituent volatiles, both in isolation and in combination, and then producing a synthetic blend based on an identified subset of attractive compounds.

Acknowledgements

We are gratefulto the Dole Corporation and Island Princess Mac Nut Inc. for allowing access to their properties on Oahu and the Big Island, respectively, and to Abbie Fox and Guadalupe Gracia for providing information on the use of food cones in detection programs.

Author contributions Todd Shelly designed the experiments, collected and analyzed the data, and prepared the manuscript. Thomas Fezza collected and analyzed the data.

Funding No funding was received to conduct this study.

Conflict of interest The authors declare that they have no conflict of interest.

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Field Studies of Synthetic Food-Based Attractants for Detecting Invasive Fruit Flies (Diptera: Tephritidae)

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Abstract

Figures

Introduction

Materials and methods

Experiment 2: Comparison of TYB and TMA TRI Difusor Lures

Experiment 3: Comparison of TYB, food cones, and 3C Difusor Lures

Experiment 4: Comparison of TYB and two component (2C) and 3C Difusor Lures

Statistical analyses

Results

Experiment 1: Comparison of TYB, food cones, and Unipaks

Experiment 2: Comparison of TYB and 3C Difusor Lures

Experiment 3: Comparison of TYB, food cones, and 3C Difusor lures

Experiment 4: Comparison of TYB and 2C and 3C Difusor lures

Discussion

Declarations

References

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Version 1