Abstract
insects Article Optimizing Trap Characteristics to Monitor the Lea ooted Bug Leptoglossus zonatus (Heteroptera: Coreidae) in Orchards 1 , 1 2 Houston Wilson * , Jessica J. Maccaro and Kent M. Daane Department of Entomology, University of California, Riverside, Riverside, CA 92521, USA; [email protected] Department of Environmental Science, Policy and Management, University of California, Berkeley, Berkeley, CA 94720-3114, USA; [email protected] * Correspondence: [email protected]; Tel.: +001-(559)-646-6519 Received: 6 May 2020; Accepted: 6 June 2020; Published: 9 June 2020 Abstract: The lea ooted bug, Leptoglossus zonatus (Heteroptera: Coreidae), has become a key pest of almonds, pistachios, and pomegranates in California. Adults and nymphs directly feed on nuts and fruits, which reduces crop yield and quality and can facilitate pathogen infections. Current monitoring strategies require growers to actively sample the tree canopy, with no economic thresholds being developed for this pest. To improve monitoring of L. zonatus, a three-year study was conducted to identify an optimal trap. A hanging cross-vane panel trap was identified as the best trap type in Year 1, and subsequent work in Years 1–3 focused on refining its use by modifying surface texture and color. Results indicated that coating trap surfaces with the lubricant fluon improved trap catching ability, and adults were most frequently recovered in yellow traps. A hanging cross-vane panel trap with these features could serve as the basis for the development of a new monitoring system for this pest in orchards, which could be improved further if semiochemical lures will be developed. Keywords: lea ooted bug; cross-vane panel trap; trap color; Leptoglossus 1. Introduction The genus Leptoglossus is neotropical in origin, with most species limited to Central and South America [1,2], where they are considered pests for a wide variety of crops [3–8]. In North America, the key economic species are L. clypealis, L. occidentalis, L. phyllopus, and L. zonatus. Leptoglossus occidentalis primarily attack coniferous trees [9,10], whereas the other three species have been recovered from a range of perennial crops that include tree nuts, citrus, peaches, and pomegranates [11–14]. The primary agricultural pest species in California are L. clypealis and L. zonatus, which are known to attack almonds, pistachios, and pomegranates when not feeding on a variety of weedy annual species [15]. Early reports first documented L. clypealis feeding on pistachio, which led to nut drop and epicarp lesion [16,17]. While historically L. clypealis has been the dominant species found on California tree nuts [18], recent surveys have noted a shift towards L. zonatus, which is now considered the primary species attacking these crops [15,19,20]. These species of Leptoglossus overwinter as adults in aggregations in sheltered areas, such as evergreen trees, shrubs, and residential structures, and in the spring disperse in search of food and reproduction sites [10,14,15,21]. In California, L. clypealis and L. zonatus complete three generations, but a fourth generation is possible if quality food sources and mild fall-winter temperatures are present [19]. While there are many plant species these lea ooted bugs will feed on, adults typically begin to attack almonds in April–May. As almond shells harden, adults (either from the overwintering or first summer generation) move over to pistachios in May–June, which are still vulnerable during Insects 2020, 11, 358; doi:10.3390/insects11060358 www.mdpi.com/journal/insects Insects 2020, 11, 358 2 of 9 this period. Similarly, as pistachio shells harden, the later summer generation(s) of adult lea ooted bug shift to pomegranates in August–September, and typically complete a generation while residing in this crop until late November, at which point adults move to overwintering aggregation sites. While the most extensive crop damage is due to adults, who have strong mouthparts and can disperse widely, feeding by developing nymphs can also have an impact on crop yield and quality. Current recommendations for monitoring lea ooted bugs include beat sampling the tree canopy, visually searching trees for adults, or assessing immature nuts for signs of feeding damage [15,21]. All of these approaches are very time and labor intensive, and no economic thresholds associated with any of these sampling methods exist. Furthermore, damaging populations of L. zonatus adults can be sporadic and tend to arrive rapidly, which makes them dicult to predict and/or detect in a timely manner. As such, use of chemical controls is typically based on presence/absence of Leptoglossus spp. and largely rely on pyrethroids, like bifenthrin and lambda-cyhalothrin. Design of an e ective trap and lure system for monitoring L. zonatus could improve sampling eciency and facilitate the development of economic thresholds. Here, as a first step towards developing this type of system, di erent trap types were screened for their ability to catch L. zonatus under field conditions, with parallel optimization of several trap parameters. 2. Materials and Methods A series of field studies were carried out over a three-year period in the San Joaquin Valley, California. In an initial study in Year 1, the ecacy of di erent trap types was compared, in order to identify the most promising one. The subsequent e orts in Years 1–3 focused on refining the use of the most ecient trap, by modifying trap color and surface coating. Working with unbaited traps required that all studies took place at sites with heavy infestations in the late summer and fall when L. zonatus populations are highest. 2.1. Trap Comparison Study Five trap types and three bait treatments were evaluated at three field sites that included an olive, pistachio, and pomegranate orchard, each heavily infested with L. zonatus. The olive orchard was 2.8 ha (7 ac), the pistachio orchard was 0.8 ha (2 ac), and the pomegranate orchard was arranged as a hedge that was 4.6 m (15 ft) wide by 419.4 m (1376 ft) long. Trap types included a black hanging cross-vane panel trap (Intercept Trap, Alpha Scents, West Linn, OR, USA), a 1.2 m (4 ft) tall black pyramid trap (Dead Inn, AgBio Inc., Denver, CO, USA), a 0.6 m (2 ft) tall black pyramid trap (Dead Inn, AgBio Inc., Denver, CO, USA), a 15.2 30.5 cm (6 12 in) clear sticky dual panel trap (Pherocon, Trécé Inc., Adair, OK, USA), and a green-white-yellow bucket trap (Multi-color UNI-Trap, Alpha Scents, West Linn, OR, USA). The collection buckets of the hanging cross-vane panel traps and bucket traps contained 443 mL (15 oz) of a killing solution, which consisted of 9.9 mL (2 tsp) biodegradable detergent diluted in 3.8 L (1 gal) of water. Trap baits included split pomegranate (50 g), almond meal (40 g) mixed with crude almond oil (10 g), and a no bait control. Baits were placed in 10.2 15.2 cm (4 6 in) organdy mesh bags. These bait bags were then suspended from the center of the hanging panel trap, placed inside the collection cup at the top of the pyramid traps, attached with a binder clip to the clear sticky trap, or suspended in the collection cup inside the bucket trap. In total there were 15 unique trap bait treatment combinations. At each of the three sites, a randomized complete block design was used with five replicates per site. Replicates were spaced 36.6 m, 18.3 m, and 10 m apart and within replicates the di erent trap/bait treatments were spaced 9.1 m, 5.2 m, and 33 m apart at the olive, pistachio, and pomegranate sites, respectively. Traps were set up and monitored weekly between 7 September–18 October in Year 1. Each week the baits and collecting solution were replaced and all adult Leptoglossus spp. were removed, sexed, and identified to species. Insects 2020, 11, 358 3 of 9 2.2. Surface Coating Study In a follow-up study, the use of fluon (Insect-a-Slip, BioQuip, Rancho Dominguez, CA, USA) was evaluated to improve recovery of Leptoglossus spp. in the black hanging cross-vane panel traps. There were five treatments that included a coating of undiluted fluon; dilutions of 50%, 25%, and 12.5% fluon; and a control trap with no fluon. In each fluon treatment, a single layer of solution was painted over all trap surfaces. No baits were used with any of the traps. Traps were evaluated using a randomized complete block design with five replicates at the pomegranate site described above. Traps were set up and monitored weekly from 13 November–4 December in Year 1. As before, each week, the collecting solution was replaced and all adult Leptoglossus spp. were removed, sexed, and identified to species. 2.3. Trap Color The e ect of the hanging cross-vane panel trap color was evaluated each fall in a heavily infested pomegranate orchard over a three-year period. Black traps were compared to red, yellow, green, blue, and white traps. Field studies utilized a randomized complete block design with five replicates. In Years 1–2, this study was located at the pomegranate site described above and took place during 4–18 December, in Year 1, and 22 August–20 November, in Year 2. In Year 3, the study took place 27 September–3 December in a 0.4 ha (1 ac) pomegranate orchard at the UC Kearney Agricultural Research and Extension Center, Parlier, California, USA. Replicates were spaced 10 m and 10.3 m apart and traps within replicates were spaced 3 m and 9.1 m apart, in Years 1–2 and 3, respectively. 2.4. Statistical Analysis Data on insect abundance from each trial were log (x + 1) transformed and analyzed with generalized linear mixed-models using the “glmer” function in the “lme4” package in the R statistical program (http://www.r-project.org/). Fixed e ects were evaluated through model comparison using chi-square tests via the “drop1” function. When a multilevel categorical variable was found to be significant, means were separated using post hoc Tukey contrasts (“glht” function in the “multcomp” package). Male and female L. zonatus were evaluated separately. For the trap/bait study, fixed e ects included “Trap Type” and “Bait,” with the random e ects “Replicate Block” nested within “Site” within “Sample Week.” Replicate Block was included as a random e ect, since each block contained multiple repeats of the di erent trap types and baits. An interaction term for “Trap Type Bait” was initially evaluated, but since it was found to be non-significant, the analysis presented here models these factors separately. The fluon study included fixed e ect “Fluon Dilution” and the random e ect “Sample Week.” Finally, the trap color study included fixed e ect “Trap Color,” with random e ects “Site” nested within “Sample Week” within “Year.” 3. Results Almost all the Leptoglossus spp. recovered in these trials were L. zonatus, with L. clypealis rarely encountered. As such, all of the data analyses focused on L. zonatus alone. Analysis of the trap and bait trial data (n = 400, total L. zonatus females = 103, males = 114) indicated that capture of L. zonatus 2 2 was influenced by trap type (males = 106.8, p < 0.001; females = 101.0, p < 0.001), but not by bait 2 2 (males = 0.2, p = 0.91; females = 0.2, p = 0.92). The hanging cross-vane panel trap captured the most L. zonatus adults (Figure 1). In the surface treatment trial (n = 75, total L. zonatus females = 277, males = 213), L. zonatus catch was increased substantially by coating trap surfaces with fluon (males 2 2 = 33.6, p < 0.001; females = 20.4, p < 0.001), even when highly diluted (Figure 2). Finally, data from the multi-year trap color experiment (n = 568, total L. zonatus females = 342, males = 201) indicated di erences in L. zonatus catch across the di erent trap colors (males = 40.6, p < 0.001; females = 70.0, p < 0.001). Yellow traps were the most attractive, followed by blue and green traps, while white and red traps were the least attractive (Figure 3). Insects 2020, 11, x FOR PEER REVIEW 4 of 9 Insects 2020, 11, 358 4 of 9 Insects 2020, 11, x FOR PEER REVIEW 4 of 9 1.2 Male Female 1.2 1 B Male Female 0.8 B b 0.8 0.6 B 0.6 B 0.4 0.4 0.2 A a A A A A 0.2 0 a A a Alm. Cont. Pom. Alm. Cont. Pom. Alm. Cont. Pom. Alm. Cont. Pom. Alm. Cont. Pom. A A A A Bucket Trap Hanging Panel Pyramid - Short Pyramid - Tall Clear Sticky Trap Alm. Cont. Pom. Alm. Cont. Pom. Alm. Cont. Pom. Alm. Cont. Pom. Alm. Cont. Pom. Bucket Trap Hanging Panel Pyramid - Short Pyramid - Tall Clear Sticky Trap Figure 1. The hanging cross-vane panel trap consistently captured the most L. zonatus, regardless of bait type. Columns of the same color without a common letter differ significantly. Alm. = almond Figure 1. The hanging cross-vane panel trap consistently captured the most L. zonatus, regardless of Figure 1. The hanging cross-vane panel trap consistently captured the most L. zonatus, regardless of meal bait, Cont. = no bait control, and Pom. = pomegranate bait; Bucket Trap = green-white-yellow bait type. Columns of the same color without a common letter di er significantly. Alm. = almond meal bait type. Columns of the same color without a common letter differ significantly. Alm. = almond bucket trap, Hanging Panel = black hanging cross-vane panel trap, Pyramid - Short = 0.6 m pyramid bait, Cont. = no bait control, and Pom. = pomegranate bait; Bucket Trap = green-white-yellow bucket meal bait, Cont. = no bait control, and Pom. = pomegranate bait; Bucket Trap = green-white-yellow trap, Pyramid - Tall = 1.2 m pyramid trap, and Clear Sticky Trap = clear sticky dual panel trap. trap, Hanging Panel = black hanging cross-vane panel trap, Pyramid - Short = 0.6 m pyramid trap, bucket trap, Hanging Panel = black hanging cross-vane panel trap, Pyramid - Short = 0.6 m pyramid Pyramid - Tall = 1.2 m pyramid trap, and Clear Sticky Trap = clear sticky dual panel trap. trap, Pyramid - Tall = 1.2 m pyramid trap, and Clear Sticky Trap = clear sticky dual panel trap. Male Female Male Female B bc B AB bc ab AB 2 b ab 0 a A 0% 12.5% 25% 50% 100% Control Fluon Concentration 0% 12.5% 25% 50% 100% Control Fluon Concentration Figure 2. The addition of fluon increased trap capture of L. zonatus. Columns of the same color without Figure 2. The addition of fluon increased trap capture of L. zonatus. Columns of the same color without a common letter di er significantly. a common letter differ significantly. Figure 2. The addition of fluon increased trap capture of L. zonatus. Columns of the same color without a common letter differ significantly. Adults /Trap /Week Adults /Trap /Week Adults /Trap /Week Adults /Trap /Week Insects 2020, 11, x FOR PEER REVIEW 5 of 9 Insects 2020, 11, 358 5 of 9 Male Female 1.5 C c BC bc AC 0.5 ab AB ab A ab Red White Black Green Blue Yellow Figure 3. Yellow traps captured the most L. zonatus, followed by blue and green traps. X-axis defines Figure 3. Yellow traps captured the most L. zonatus, followed by blue and green traps. X-axis defines the color of trap evaluated. Columns of the same color without a common letter di er significantly. the color of trap evaluated. Columns of the same color without a common letter differ significantly. 4. Discussion 4. Discussion This series of experiments demonstrated that an unbaited hanging cross-vane panel trap is attractive to L. zonatus, especially a yellow trap. Capture can be increased by coating trap surfaces This series of experiments demonstrated that an unbaited hanging cross-vane panel trap is with fluon to reduce insect ability to grip the trap surface. Inclusion of a split pomegranate or almond attractive to L. zonatus, especially a yellow trap. Capture can be increased by coating trap surfaces meal bait did not increase trap catch, indicating that these materials have low attractive ability on with fluon to reduce insect ability to grip the trap surface. Inclusion of a split pomegranate or almond this insect species, and that L. zonatus apparently are attracted to the hanging cross-vane panel trap meal bait did not increase trap catch, indicating that these materials have low attractive ability on this itself. Response of L. zonatus to a large dark object, such as this panel trap, is similar to observations insect species, and that L. zonatus apparently are attracted to the hanging cross-vane panel trap itself. by Panizzi [22], who reported that L. zonatus aggregated on unbaited plastic cylinder traps when the Response of L. zonatus to a large dark object, such as this panel trap, is similar to observations by cylinders were first introduced into corn fields. Panizzi [22], who reported that L. zonatus aggregated on unbaited plastic cylinder traps when the The cross-vane panel trap was initially developed to monitor Coleoptera in forests [23,24], as a cylinders were first introduced into corn fields. replacement or supplement for the multiple-funnel trap [25]. Subsequent work with the cross-vane The cross-vane panel trap was initially developed to monitor Coleoptera in forests [23,24], as a panel trap demonstrated its utility for trapping cerambycid and buprestid beetles [26–28]. Trapping replacement or supplement for the multiple-funnel trap [25]. Subsequent work with the cross-vane e panel cacy trap for beetle demonstrated species can its uti be lity further for trapping enhanced, cerambycid sometimes and mor buprest e than id ten-fold, beetles [26 by –28 coating ]. Trap trap ping surfaces with fluon or other lubricants [29–31]. Our results demonstrated analogous increases in efficacy for beetle species can be further enhanced, sometimes more than ten-fold, by coating trap trapping surfaces ewith ciency fluon when or ot traps her wer lubric e tr ants eated [29 with –31]. fluon. Our results demonstrated analogous increases in Cross-vane panel traps have also been used to e ectively trap Hemipterans, such as triatomines trapping efficiency when traps were treated with fluon. (Reduviidae: Cross-vane Triatominae) panel traps [ha 32ve ], bagrada also been bug used(Pentatomidae: to effectively trap Bagrada Hemipthilaris erans, ) s[ u 33 ch ],as and triatom brown ines marmorated stink bug (Pentatomidae: Halyomorpha halys) [34], but apparently are not well suited (Reduviidae: Triatominae) [32], bagrada bug (Pentatomidae: Bagrada hilaris) [33], and brown for marmo spotted rated lanternfly stink bug (Fulgoridae: (Pentatomida Lycorma e: Halyomor delicatula pha ) halys [35]. ) [No 34],traps but apparently specifically ar for e not Leptoglossus well suited spp. for have been developed. The scant literature includes a prototype bottle trap for L. zonatus [36], along spotted lanternfly (Fulgoridae: Lycorma delicatula) [35]. No traps specifically for Leptoglossus spp. have with been a deve study lop that ed. mentions The scant l the iter use ature of multi-funnel includes a pro traps totype for bo testing ttle trap L. occidentalis for L. zonatus attraction [36], along to caged with a aggregations of males and females [37]. Bycatch of non-target organisms in the cross-vane panel trap study that mentions the use of multi-funnel traps for testing L. occidentalis attraction to caged was aggr minimal, egations with of masome les and honeybees females [37]. (Apidae: Bycatch Apis of no mellifera n-target ) recover organis ed ms inin blue the and cross gr -v een ane traps panel and trap assassin bugs (Reduviidae: Zelus spp.) in blue and yellow traps (data not shown). was minimal, with some honeybees (Apidae: Apis mellifera) recovered in blue and green traps and assassin The bug e ect s (Reduv of trapiicolor dae: Zel has us been spp.) in widely blue a evaluated nd yellow traps across(d multiple ata not shown insect).or ders, including Coleoptera [38–40], Lepidoptera [41–43], Hymenoptera [44–47], and Hemiptera [48–52]. The only The effect of trap color has been widely evaluated across multiple insect orders, including pr Co evious leoptera study [38to –40 evaluate ], Lepido Leptoglossus ptera [41–43 spp. ], Hymeno responses pter to a color [44–47 was ], an a d laboratory Hemipter study a [48,–which 52]. Th found e only that L. zonatus adults and nymphs were primarily attracted to blue and green [53]. These results were previous study to evaluate Leptoglossus spp. responses to color was a laboratory study, which found partially that L. zona complimented tus adults and in our nymp study hs ,were in which primar blue ily and attrgr acted een wer to blu e the e and second green and [53 thir ]. Th d es most e res attractive ults were colors after yellow. Response of L. zonatus to trap color in the current study may have been skewed by partially complimented in our study, in which blue and green were the second and third most di attractive erences col in trap ors af temperatur ter yellow. e, Res which pons likely e of L. varied zonatbetween us to trap the color lighter in th and e current darker study color ed ma traps y hav under e been field conditions. This may be an important consideration, given that a recent study of L. occidentalis, skewed by differences in trap temperature, which likely varied between the lighter and darker colored traps under field conditions. This may be an important consideration, given that a recent Adults /Trap /Week Insects 2020, 11, 358 6 of 9 a relative species of L. zonatus, indicated that this species utilizes infrared cues to locate host plants [54]. It may be that L. zonatus utilizes infrared cues in a similar way. As such, subsequent field evaluations of trap color e ects on L. zonatus could be improved by controlling for, or at least recording data on, trap temperature. 5. Conclusions Identification of the hanging cross-vane panel trap for L. zonatus represents an important step forward in the development of an e ective monitoring program for this pest, especially the highly mobile adult, and will allow for the future screening of candidate lures for this insect under field conditions [55]. Once paired with an attractive lure, studies will need to determine the most e ective density and spatial arrangement of traps to accurately reflect orchard populations of L. zonatus and correlate trap captures with economic thresholds. If perfected, this type of trap and lure sampling system will reduce the sampling e ort and lead to earlier and/or more accurate detection of L. zonatus populations in orchards. It is also possible that these traps could work well for other Leptoglossus pest species, such as L. occidentalis, which has recently invaded Europe, and may be worth further investigation in that context [56,57]. Author Contributions: Conceptualization, H.W. and K.M.D.; methodology, H.W. and J.J.M.; investigation, H.W. and J.J.M.; formal analysis, H.W.; writing—original draft preparation, H.W.; writing—review and editing, H.W., J.J.M. and K.M.D. All authors have read and agreed to the published version of the manuscript. Funding: This research was funded by the California Pistachio Research Board and the Almond Board of California. Acknowledgments: Authors thank the California Pistachio Research Board and the Almond Board of California for funding this research. Field studies and data collection were carried out with assistance from German Camacho, Jesus Ceja, Gabrielle Celaya, Tyler Colombero, Dani Evans, Javier Herrera, Garrett Morales, Joshua Reger, Austin Souza, May Yang, and Sunny Yang. Many thanks are owed as well to all collaborating growers for access to field sites to collect insects. Authors also extend thanks to Jocelyn Millar for providing useful comments and feedback on a draft version of this manuscript. Conflicts of Interest: The authors declare no conflict of interest. References 1. Allen, R.C. A revision of the genus Leptoglossus Guérin (Hemiptera: Coreidae). Entomol. Am. 1969, 45, 35–140. 2. Brailovsky, H. 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