The cranberry weevil, Anthonomus musculus Say (Coleoptera: Curculionidae), is a key (univoltine) pest of highbush blueberries in the northeast United States. To date, however, no trapping system has been developed to successfully monitor this pest. In 2012–2014, studies were conducted in commercial highbush blueberry farms in New Jersey to 1) evaluate the efficacy of various commercially available traps, designed for other weevil species (e.g., pepper weevil, plum curculio, boll weevil, red palm weevil, and black vine weevil), in capturing A. musculus adults; 2) test whether the relative location of traps within the blueberry canopy affects adult captures and 3) determine the effects of different colored (yellow, white, green, red, blue, brown, and black) sticky traps on weevil captures. For a comparison with existing techniques, we also monitored the number of overwintered adult weevils on blueberry bushes using beat sheet sampling. Of all traps and colors tested, the most A. musculus adults were caught on yellow sticky traps and more adults were captured when these traps were placed at the bottom half of the blueberry canopy, i.e., 0.5–1.0 m above ground. Most weevils were caught on colored traps late in the season (i.e., during bloom), which corresponds mostly to the second (summer) adult generation. Thus, number of overwintered adults caught on traps did not correlate with those on bushes. Although our study identified traps that can be used to capture A. musculus adults, these traps alone (i.e., without semiochemicals) have so far limited applicability for monitoring overwintered adult weevils in highbush blueberries. Key words: cranberry weevil, attraction, color, height, trap design The cranberry weevil, Anthonomus musculus Say (Coleoptera: their eggs into flower buds where the larvae develop (Szendrei and Curculionidae), also known as blueberry blossom weevil, causes Rodriguez-Saona 2009). Infested flower buds turn purple, fail to economic losses to commercial blueberry and cranberry growers open, and eventually fall to the ground. In mid-May through June, (Marucci 1966, Averill and Sylvia 1998, Long and Averill 2003). next-generation (summer) adults feed on blueberry leaves and then A. musculus is native to North America and its distribution in the move out of the blueberry fields to nearby wooded areas where they United States ranges from Massachusetts to New Jersey in the east may attack other hosts and/or overwinter (Szendrei and Rodriguez- coast, and Wisconsin and Michigan in the north central region Saona 2009). (Szendrei and Rodriguez-Saona 2009). Although some aspects of the In blueberries, current methods for monitoring the overwintered A. musculus life cycle remain unknown, it is known that this weevil A. musculus adults focus on beat sheet sampling along the edges of can complete a single generation in blueberry fields in New Jersey. fields facing wooded areas, starting at the end of March (bud break) Overwintered adults move into blueberry fields from surrounding until early May (beginning of bloom) (Szendrei and Rodriguez-Saona wooded areas in early spring (late March through April), where they 2009). Overwintered adults are the target of insecticide applications feed on the developing flower buds (Doehlert and Tomlinson 1947, to prevent oviposition on flower buds and subsequent injury by lar - Mechaber 1992). While it is unknown whether A. musculus adults val feeding/developing within buds, which is the main cause of eco- disperse through flying or a combination of flying and walking, nomic damage. An economic threshold based on beat sheet sampling once they reach the blueberry fields, overwintered females deposit is set at five A. musculus adults per bush; however, this sampling © The Author(s) 2018. Published by Oxford University Press on behalf of Entomological Society of America. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/4.0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is properly cited. For commercial re-use, please contact firstname.lastname@example.org Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 2 Journal of Insect Science, 2018, Vol. 18, No. 2 method is labor-intensive and often unreliable because adult wee- weevil species, on A. musculus adult captures in commercial blue- vils have cryptic behaviors and tend to be active mostly on sunny berry farms. All farmers followed standard crop management pro- days (Szendrei and Rodriguez-Saona 2009). Therefore, a cost-effec- cedures (i.e., pesticide use; according to Oudemans et al. 2017), and tive and reliable method for monitoring overwintered A. musculus insecticides (usually a pyrethroid) were used only once if the number adults is needed to more accurately time insecticide applications. of overwintered weevils exceeded the economic threshold of an aver- Insect traps are commonly used for monitoring pest populations in age of five weevils per bush (Szendrei and Rodriguez-Saona 2009). agricultural crops (Pedigo and Rice 2014) and may help improve the 2012 Experiment. This experiment was carried out at four timing of insecticide applications used for A. musculus. However, the commercial blueberry farms located in Burlington and Atlantic potential of using a trapping system for monitoring A. musculus has Counties in southern New Jersey (farm A: Latitude 39°35ʹ29.3ʺN, yet to be investigated. Longitude 74°46ʹ09.8ʺW, Hammonton township; farm B: Latitude Several different trap designs, including trap types and colors, 39°42ʹ18.8ʺN, Longitude 74°45ʹ01.8ʺW, Hammonton town- have been developed to monitor weevil species of agricultural ship; farm C: Latitude 39°55ʹ49.0ʺN, Longitude 74°36ʹ46.1ʺW, importance (Mizell and Tedders 1999, Cross et al. 2006, McQuate Pemberton township; farm D: Latitude 39°38ʹ43.3ʺN, Longitude et al. 2014, Tewari et al. 2014, Avalos and Soto 2015). A number 74°42ʹ32.1ʺW, Hammonton township). Farm selection was based of weevils, such as the pepper weevil, Anthonomus eugenii Cano on previous history of A. musculus infestation and farms were sep- (Coleoptera: Curculionidae), are attracted to simple trap designs like arated at least 8 km from each other. Five different trap types were colored sticky cards (Riley and Schuster 1994), while more sophis- tested: 1) yellow sticky traps (23 × 28 cm; Pherocon AM no-bait trap, ticated trap designs that incorporate a capturing devise are used for Trécé, Adair, OK; Fig. 1a); 2) Whalon modified Tedder’s traps, with a other species such as the plum curculio, Conotrachelus nenuphar collection top, used for monitoring plum curculio (C. nenuphar) and (Herbst) (Coleoptera: Curculionidae), (Prokopy et al. 2000) and pecan weevil (Curculio caryae (Horn) (Coleoptera: Curculionidae)) the boll weevil, Anthonomus grandis grandis Boheman (Coleoptera: (Great Lakes IPM, Vestaburg, MI; Fig. 1b); 3) boll weevil traps, with Curculionidae) (Hardee et al. 1996). Trap captures can be influenced a collection top, used in boll weevil (A. grandis) eradication programs also by their placement within the field such as the location of traps (Great Lakes IPM) (Fig. 1c); 4) ISCA pitfall traps, used for moni- within the crop canopy (Mulder et al. 1997, Prokopy et al. 2000, toring red palm weevil (R. ferrugineus) and South American palm Prokopy et al. 2001, Cross et al. 2006). For example, A. eugenii weevil (Rhynchophorus palmarum (L.) (Coleoptera: Curculionidae)) adults were more likely to be captured on yellow sticky cards placed (ISCA Technologies, Riverside, CA; Fig. 1d); and 5) ChemTica pitfall 10–60 cm above ground than at other heights (Riley and Schuster traps, used for monitoring black vine weevil (Otiorhynchus sulca- 1994). Fountain et al. (2017) reported that the strawberry blossom tus (F.) (Coleoptera: Curculionidae)) (ChemTica International S.A., weevil, Anthonomus rubi Herbst (Coleoptera: Curculionidae), was Heredia, Costa Rica; Fig. 1e). Two of these traps (sticky trap and more likely to be trapped at 0 m than at 0.5 or 1.5 m above the soil sur- boll weevil trap) are designed to intercept flying weevils, whereas face. Color often plays an important role in weevil attraction to traps. the other three traps are designed to capture walking insects. Yellow Mizell and Tedders (1999) showed that the root weevils Hylobius sticky traps were used as our standard trap based from a previous pales (Herbst) (Coleoptera: Curculionidae) and Pachylobius picivorus study (Szendrei et al. 2011) and were placed vertically (i.e., with the (Germar) (Coleoptera: Curculionidae) are more attracted to black or narrow edge perpendicular to the ground and the long trap dimen- brown pyramid-shaped Tedder’s traps than to yellow or white traps. sion horizontal) at mid-canopy (1–1.5 m above the ground) using Similarly, the red palm weevil, Rhynchophorus ferrugineus (Oliver) 2.5-m metal poles. The Whalon modified Tedder’s trap is a 1.2-m tall (Coleoptera: Curculionidae), is attracted to black traps (Abuagla and pyramid trap that is placed on the ground and has a capturing device Al-Deeb 2012, Al-Saoud 2013). In contrast, A. eugenii is attracted at the top of the trap (Fig. 1b); the insect flies near the trap, which to yellow traps (Riley and Schuster 1994). A study by Szendrei et al. it reaches by walking, and then accesses the trap device by walking (2011) employed yellow sticky traps to capture A. musculus adults. upward on one of the trap panes. Boll weevil traps were hung at Whether other trap designs and colors are, however, effective at cap- mid-canopy (1–1.5 m above the ground) using bamboo stakes; the turing A. musculus in the field has not been investigated. insects attracted to this yellow-green color trap land on the outside Here, we present results of a three year (2012–2014) study done of the body, crawl to the inside of the cone, and enter the collec- in commercial highbush blueberry, Vaccinium corymbosum L., fields tion chamber through an opening at the top of the cone (Fig. 1c). to determine the effects of trap design, location, and color on cap- The ISCA and ChemTica pitfall traps were placed at ground level tures of A. musculus adults in the absence of semiochemical attract- (i.e., 0 m); a major difference between these traps besides size is that ants. Experiments were conducted to address the following specific the ISCA trap has the opening (entrance) at the top (Fig. 1d), while questions: 1) Which of various commercially available traps designed the opening in the ChemTica trap is at the bottom (Fig. 1e), of the for other curculionid beetles is most effective at capturing A. mus- trap. For plum curculio and boll weevil traps, a killing strip (Hercon culus adults? 2) Are A. musculus adult captures affected by trap Vaportape II insecticidal strip; Gempler’s, Janesville, WI) was placed placement within the blueberry canopy? 3) Do A. musculus adults inside the collection top to prevent weevils from exiting. Ethylene respond to different colored traps? and 4) At what period during the glycol (antifreeze) and a sticky card, placed at the bottom of trap blueberry growing season are weevils most responsive to these traps? interiors, were used in ISCA and ChemTica traps, respectively, to These studies intended to identify a monitoring tool for A. musculus kill weevils. Killing strips were replaced every three weeks, while the adults that could be combined in the future with semiochemicals and antifreeze and sticky cards were replaced weekly. to learn about the visual cues that trigger its foraging behaviors. Treatments were arranged as a randomized block design. Each block consisted of a set of five different trap types, one of each type, and there were three blocks at each site (i.e., farm) (N = 12 repli- Materials and Methods cates per trap type). Traps were placed in a straight line inside blue- Trap Type berry fields parallel to the field’s edge, 5 m from the edge of the field, A 2yr study (2012–2013) was conducted to evaluate the efficacy of and at least 10 m apart from each other within each block. Because various commercially available trap types, used for monitoring other A. musculus disperses into blueberry fields from adjacent wooded Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 3 Fig. 1. Trap designs tested in this study for cranberry weevil, A. musculus: (a) yellow sticky trap (Pherocon AM no-bait trap); (b) Whalon modified Tedder’s trap with a collection top, used for monitoring plum curculio and pecan weevil (Great Lakes IPM); (c) boll weevil trap with a collection top, used in cotton boll weevil eradication programs (Great Lakes IPM); (d) ISCA pitfall trap, used for monitoring red palm weevil and South American palm weevil (ISCA Technologies); (e) ChemTica pitfall trap, used for monitoring black vine weevil (ChemTica International S.A.); and (f) white sticky trap (Great Lakes IPM). Note: the ISCA pitfall trap has an opening (entrance) at the top; the ChemTica pitfall trap has the opening (entrance) at the bottom of the trap. For plum curculio and boll weevil traps, a killing strip was placed inside the collection vial to prevent weevils from exiting. ISCA and ChemTica pitfall traps use ethylene glycol (antifreeze) and a sticky card, respectively, to kill weevils. areas (Szendrei and Rodriguez-Saona 2009), all traps were placed Trap Height near the field’s edge and facing the forest. Distance between blocks An experiment was conducted to determine the effect of trap height was at least 20 m. Traps were placed at the end of March and were within the canopy for capturing A. musculus adults. The experi- rotated (e.g. sequentially moved down a space) weekly. The number ment was conducted in four commercial blueberry farms located in of weevils per trap was counted weekly for 12 wk between 20 March southern New Jersey (farm A, farm B, farm C, and farm D) in 2013. and 11 June 2012; this period corresponded from bud break until We used yellow sticky traps in this experiment because they were fruit set/maturation, when A. musculus adults are active in commer- effective at capturing A. musculus adults based on previous experi- cial blueberry fields in New Jersey. ments (see Results). We tested four different trap heights: 1) ground 2013 Experiment. This experiment was conducted in four com- level (i.e., 0 m); 2) bottom of the bush canopy (i.e., 0.5–1.0 m above mercial blueberry farms located in southern New Jersey at farms A, ground); 3) middle of the canopy (i.e., 1.0–1.5 m above ground); and B, and C, as mentioned above, and Farm E (Latitude 39°55ʹ43.1ʺN, 4) top of the canopy (i.e., 1.5–2.0 m above ground). This 0.5 m vari- Longitude 74°30ʹ06.7ʺW, Pemberton township). Three of the same ation within canopy sections accommodated for variation in canopy traps used in 2012 were tested in 2013: 1) yellow sticky traps; height among bushes. Within the canopy, the middle part of the trap 2) Whalon modified Tedder’s traps; and 3) boll weevil traps. ISCA was adjusted to each of the heights such that the trap was located and ChemTica pitfall traps were not included because they were inef- at the center of each canopy height. Traps were randomly placed ficient at capturing A. musculus adults (see Results). In addition, we at one of the four heights in each bush, all trap heights were tested added white sticky traps used for tarnished plant bugs, Lygus lineo- concurrently in different bushes, and trap height within bushes was laris (Palisot de Beauvois) (Hemiptera: Miridae) (23 × 28 cm; Great changed weekly by a systematic height rotation schedule, as described Lakes IPM; Fig. 1f), to test for color preference. White sticky traps above. Traps were attached to 2.5-m vertical poles, and trap height had the same size, shape, and placement as the yellow sticky traps. was adjusted along the pole. Each trap height was replicated four Treatments were arranged as a randomized block design with six rep- times (blocks) at each of the four farms in a randomized block design licates at each site (i.e., farm) (N = 24 replicates per trap design; see (N = 16 replicates per trap height). Distance between traps within above). Distance between traps within sites and their placement were farms and placement within fields were the same as described above. the same as described above for the 2012 experiment. Traps were Traps were monitored weekly for 9 wk between 8 April (bud break) placed in early April and rotated weekly. The number of weevils per and 5 June (fruit set per maturation). Farmers followed standard pest trap was recorded weekly for 9 wk between 8 April and 3 June 2013. management procedures. Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 4 Journal of Insect Science, 2018, Vol. 18, No. 2 we performed analysis of variance (ANOVA) using linear mixed-ef- Trap Color fects analysis of covariance models lme() using the ‘nlme’ package in A study was conducted to test A. musculus adult preference for R. The models included treatment (trap type or height or color; fixed different color traps. The experiment was done in three commer- factor), week, and block (sites within farms) as main effects, and all cial blueberry farms in New Jersey (farms A, B, and C) in 2014. possible two-way interactions among them. Blocks were nested with Seven color traps were tested: yellow (used as our standard; Szendrei farm, with farm as a random factor. Three-way interactions were not et al. 2011), white, green, blue, red, brown, and black. All traps included in the models because the degrees of freedom were too limited. were 22.8 × 14.0 cm made of (3.12-mm thick) colored acrylic sheets A significant ANOVA was followed by Tukey’s HSD test (α = 0.05; (Laird Plastics, Bristol, PA; catalog nos. = 103617, 103416, 207486, ‘agricolae’ package in R). If needed, data were transformed prior to 102249, 103220, 102318, and 102091 for yellow, white, green, blue, ANOVA using Log to meet assumptions of normality. Untransformed red, brown, and black, respectively), and were coated on both sides data are presented in figures. In addition, the number of weevils on with Tangle-Trap Insect Trap coating (The Tanglefoot Co., Grand colored traps was correlated with the number of weevils on bushes Rapids, MI). Treatments were arranged as a randomized block using Pearson correlation (Minitab version 16; Minitab 2010). design with three replicates (blocks) at each site (farm), as described above for trap design and placement (N = 9 replicates per colored trap). Traps were placed at mid-canopy height (1.0–1.5 m above Results ground) and attached vertically to metal poles. Traps within each site were placed at least 10 m apart from each other and rotated Trap Type weekly, as described above. Distance between blocks was at least 20 2012 Experiment. In 2012, trap type had a significant effect on m. The number of weevils per trap was recorded weekly for three A. musculus adult captures (Table 1). On average, the yellow sticky consecutive months (from 8 April until 3 July). trap caught 45 and 4.5 times more A. musculus adults than the In addition, numbers of overwintered A. musculus adults on Whalon modified Tedder’s trap and the boll weevil trap, respec- bushes were monitored weekly at each of the sites from 8 April tively; whereas the ISCA and ChemTica pitfall traps did not catch until 6 May using beat sheet sampling. Beat sheet samples were any weevils (Fig. 2a). There was also a significant effect of week and stopped from the beginning of bloom following grower recommen- a significant interaction between trap type and week, indicating that dations (Szendrei and Rodriguez-Saona 2009) and to avoid damage the effect of trap type on weevil captures was influenced by the week to the crop. Ten randomly selected bushes near the colored sticky of sampling. Trap Type-by-Block(Farm) and Week-by-Block(Farm) traps were sampled for adult weevils with a 71 × 71-cm beat sheet interactions were also significant, indicating that the effect of trap (BioQuip Products Inc.). These bushes were located either within the type and week of sampling on weevil captures varied among geo- same row as the traps or the row adjacent to the traps closest to the graphic locations (Table 1). forest and were at least 3 m from the nearest trap. For each bush, 2013 Experiment. In 2013, trap type and week had a significant two random (mid-canopy) branches were beaten on the sheet, which effect on A. musculus adult captures (Table 1). The yellow sticky trap corresponds to about 1/5 of the bush, and the number of weevils on captured significantly more A. musculus adults than the boll weevil the sheet was counted. We then calculated the average number of trap (Fig. 2b) but was not different from the white sticky trap and weevils per bush for the 10 bushes per site (block; N = 30 bushes per the Whalon modified Tedder’s trap (Fig. 2b). There were also signif- farm) and each sampling date. All beat sheet samples were taken on icant Trap Type-by-Block(Farm) and Week-by-Block(Farm) interac- the same day as the trap counts. Farmers used standard pest man- tions, indicating that the effect of trap type and week of sampling on agement procedures. weevil captures varied among geographic locations (Table 1). Color Attributes Trap Height To better understand the perception of various colors by A. muscu- Trap height had a significant effect on captures of A. musculus adults lus adults, the color reflectivity of the seven different colored traps (Table 2). Traps placed at the bottom of the bush canopy captured tested here (yellow, white, red, blue, green, black, and brown) was twice as many A. musculus adults as traps placed at the top of the obtained by reflectance measurements. For this, we used a Varian canopy (Fig. 3), but numbers of weevils at the bottom of the canopy Cary 500 Scan UV-VIS-NIR spectrophotometer (Varian Inc., Palo Alto, CA), in the spectral wavelength range from 400 to 700 nm Table 1. Effects of trap type, week, and block nested within (visible light), and equipped with a diffuse reflectance model Varian farm, and their interactions, on the number of cranberry weevil, DRA110 mm. Varian UV Scan application software version 3.00 A. musculus, adults (2012 and 2013) (399) was used for reflectance data acquisition. Three independent Year Variables F df P reflectance measurements were conducted for each colored trap; the average percent reflectance from these three measurements is 2012 Trap type 8.80 4, 481 <0.001 reported here. All measurements were done without an adhesive Week 4.04 11, 481 <0.001 because a previous study using similar colored traps found very Block(Farm) 1.15 9, 481 0.31 little difference in the wavelength reflectance due to the adhesive Trap type × Week 2.83 44, 481 <0.001 (Rodriguez-Saona et al. 2012). Trap type × Block(Farm) 3.05 36, 481 <0.001 Week × Block(Farm) 1.53 99, 481 0.01 2013 Trap type 3.66 3, 480 0.01 Statistical Analyses Week 2.06 7, 480 0.04 Data on weekly numbers of A. musculus adult captures per trap were Block(Farm) 1.24 18, 480 0.22 checked for normality using the Shapiro–Wilk test (Shapiro and Wilk Trap type × Week 1.09 21, 480 0.34 1965) and for homoscedasticity using the Levene’s test (‘car’ package Trap type × Block(Farm) 1.69 54, 480 <0.002 in R; R version 3.3.1; R Development Core Team 2016). To test for Week × Block(Farm) 1.27 126, 480 0.03 the effects of trap type, trap height, and trap color on weevil captures, Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 5 were not significantly different than those from traps placed in the Trap Color middle of the canopy or at ground level (Fig. 3). There were no inter- Color significantly affected attraction of A. musculus adults action effects between trap height and week of sampling or between (Table 3). Yellow was the most attractive color, followed by white trap height and block(farm) on weevil captures (no two-way interac- (Fig. 4). In contrast, blue, brown, and black were the least attractive tions, Table 2), indicating that the effect of trap height on weevil cap- colors whereas attraction to green and red was intermediate (Fig. 4). tures was not influenced by week of sampling or geographic location. Numbers of A. musculus captured were also significantly influenced by the week of sampling (Table 3), but there was no significant Trap Color × Week interaction (Table 3), indicating that weevils responded similarly to all colored traps throughout the sampling period. The number of A. musculus adults on colored traps increased from 6 May until 30 May (summer adults), which coincided with bloom, with a peak in numbers by mid- to end of bloom (Fig 5a). There were significant Trap Color × Block(Farm) and Week × Block(Farm) inter - actions, indicating that the effect of color and time of season (week) on number of weevils captured on traps varied based on geographic location (Table 3). We found no correlation between the number of A. musculus adults on beat sheet samples from the blueberry brushes versus those trapped on yellow sticky cards (Pearson correlation = -0.077; P = 0.784) or on any of the other colored traps (all Ps >0.05). In April, we found high numbers of overwintered A. musculus adults on bushes, which exceeded the economic threshold on 14 April and 22 April (Fig. 5b), but the number of weevils remained very low on traps during this period (Fig. 5a). Fig. 2. Total (mean ± SE) number of cranberry weevil, A. musculus, adults per trap (2012–2013). Five trap designs were tested in 2012 (a): yellow sticky Fig. 3. Total (mean ± SE) number of cranberry weevil, A. musculus, adults trap, Whalon modified Tedder’s trap, boll weevil trap, ISCA pitfall trap, and per yellow sticky trap (2013). Traps were placed at four different heights: top ChemTica pitfall traps (see Fig. 1). Four trap designs were tested in 2013 of the bush canopy (i.e., 1.5–2.0 cm above ground), middle of the canopy (b): yellow sticky trap, white sticky trap, Whalon modified Tedder’s trap, and (i.e., 1.0–1.5 cm above ground), bottom of the canopy (i.e., 0.5–1.0 m above boll weevil trap. Different letters indicate significant differences among trap ground), and at ground level (i.e., 0 m). Different letters indicate significant designs, P ≤ 0.05. differences among trap heights, P ≤0.05. Table 2. Effects of trap height, week, and block nested within Table 3. Effects of trap color, week, and block nested within farm, and their interactions, on the number of cranberry weevil, farm, and their interactions, on the number of cranberry weevil, A. musculus, adults (2013) A. musculus, adults (2014) Variables F df P Variables F df P Trap height 3.10 3, 357 0.02 Trap color 7.33 6, 574 <0.001 Week 3.91 8, 357 <0.001 Week 6.51 12, 574 <0.001 Block(Farm) 1.48 12, 357 0.12 Block(Farm) 1.46 6, 574 0.18 Trap height × Week 1.10 24, 357 0.33 Trap color × Week 1.82 72, 574 0.36 Trap height × Block(Farm) 1.26 36, 357 0.14 Trap color × Block(Farm) 1.75 36, 574 0.004 Week × Block(Farm) 1.90 96, 357 <0.001 Week × Block(Farm) 1.76 72, 574 <0.001 Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 6 Journal of Insect Science, 2018, Vol. 18, No. 2 Fig. 4. Total (mean ± SE) number of cranberry weevil, Anthonomus musculus, adults caught on sticky traps of various colors: yellow, white, green, red, blue, brown, and black (2014). All traps were 22.8 × 14.0 cm made of Plexiglas. Different letters indicate significant differences among trap colors, P ≤ 0.05. Trap Attributes The colored traps used in our study had differences in reflectance along the visible spectrum (400–700 nm) (Fig. 6). White traps had high reflec- tance (> 80%) at wavelengths above 420 nm. In contrast, black and brown had zero or close to zero reflectance at all wavelengths measured. Yellow traps also had high reflectance (> 60%) from 530 to 700 nm. The reflectance of blue traps was between 10 and 30% from 400 to 500 nm, with a peak around 450 nm, while green traps had spectral reflectance ranging from 450 to 560 nm, with a peak at 530 nm. Red traps had high reflectance (∼ 90%) at wavelengths ≥650 nm (Fig 6). Fig. 5. Seasonal patterns (mean number per sampling date ± SE) of Discussion A. musculus adult captures on sticky traps of various colors: yellow, white, green, red, blue, brown, and black (a) and from beat sheet samples (b) at This study provides the first insights into the visual ecology and for - three commercial blueberry farms in New Jersey (2014). Beat sheet samples aging behavior of the cranberry weevil, A. musculus, which is nec- were conducted from 8 April (bud break) until 6 May (bloom), while sticky essary for the development of a trapping system. We demonstrated traps were checked from 8 April (bud break) until 3 July (fruit maturation/ that 1) yellow sticky traps captured the highest numbers of A. mus- harvest). Beat sheet sampling was stopped at the beginning of bloom to culus adults; 2) more A. musculus adults were caught on yellow avoid damage to the crop. Insecticides (pyrethroid) were applied only once if sticky traps when placed in the lower half of blueberry bushes; and numbers exceeded the economic threshold (ET). 3) yellow traps attracted more A. musculus adults than other colored traps, which correspond to a reflectance specific for yellow of 550– 650 nm. The number of overwintered A. musculus adults caught on flying insects. It is worth noting, however, that although the Whalon yellow sticky traps did not, however, correlate with the estimated modified Tedder’s traps, used to monitor plum curculio (C. nenuphar) number of weevils on bushes. In fact, the relatively lower catch of populations, were designed to intercept walking rather than flying the overwintered generation on yellow sticky traps indicates that, in individuals (Blanchett 1987, Duan et al. 1996, Prokopy et al. 1999), the absence of other cues (e.g., chemical), these traps have limited the collection vial in these traps is located 1.2 m above ground, which practicability for monitoring the most damaging (overwintered) gen- matches the height of the bottom half of the blueberry canopy. In our eration of A. musculus adults in highbush blueberries. study, A. musculus adults were recovered only from colored sticky, Among all trap types tested in this study, colored sticky traps boll weevil, and Whalon modified Tedder’s traps; whereas no weevils (yellow) were most effective at capturing A. musculus adults. Yellow were found in ISCA and ChemTica pitfall traps. These results sug- sticky traps have been used to monitor other weevils including the gest that A. musculus adults are unlikely to locate blueberry bushes pepper weevil, A. eugenii (Riley and Schuster 1994) and the pea leaf by walking but instead they likely flew to find their host plant; thus, weevil, Sitona lineatus (L.) (Coleoptera: Curculionidae) (Fisher and traps located at canopy level to intercept flying weevils will be best at O’Keeffe 1979). Two of the trap types we tested (colored sticky traps capturing this weevil pest in highbush blueberry fields. However, the and boll weevil traps) were placed at canopy level, while the other location of traps within the blueberry canopy affected A. musculus traps (Whalon modified Tedder’s and ISCA and ChemTica pitfall adult captures, i.e., yellow sticky traps placed in the bottom half of traps) were placed at ground level. The Whalon modified Tedder’s the canopy captured more weevils than those placed in the upper half and ISCA and ChemTica pitfall traps are designed for walking insects, or on the ground. Altogether our results from the trapping design and while colored sticky and boll weevil traps are designed to intercept placement experiments suggest that A. musculus do not walk to locate Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 Journal of Insect Science, 2018, Vol. 18, No. 2 7 Fig. 6. Percentage reflectance curves over the spectral wavelength range from 400 nm to 700 nm (visible light) for the seven colored traps tested in this study. Measurements were taken using a Varian Cary 500 Scan UV-VIS-NIR spectrophotometer. a blueberry host plant but rather fly at heights between 0.5 and 1.5 m 1976, Otálora-Luna and Dickens 2011). Our goal was to identify above ground. The role of wind on A. musculus dispersal and with- an effective trap that farmers could use to monitor A. musculus in-canopy pattern of capture needs further investigation. adults, regardless of their gender. Thus, weevils were not sexed due A. musculus adults were more attracted to yellow than to red, to the difficulties of sexing them in the field. In any case, a study by blue, black, and brown. These findings agree with the visual response Szendrei et al. (2011) found no indication that males and females of the boll weevil (A. grandis), the pepper weevil (A. eugenii), and A. musculus differ in their response to yellow sticky traps. the root weevil (Sitona lepidus Gyllenhal), which are also attracted This study aimed at understanding the visual ecology of A. muscu- to yellow (Cross et al. 1976, Riley and Schuster 1994, Hardwick lus and, thus, semiochemicals were not used in traps. Semiochemicals, and Harens 2007). On the other hand, two root weevils, H. pales mainly aggregation pheromones, are commonly used to monitor and P. picivorus, respond better to black and brown than to other weevil pests of agricultural crops (reviewed by Tewari et al. 2014). colors (Mizell and Tedders 1999). Therefore, different weevil spe- Szendrei et al. (2011) identified (Z)-2-(3,3-dimethyl-cyclohexylidene) cies respond differently to colors probably depending on their spe- ethanol (Z grandlure II), (Z)-(3,3-dimethylcyclohexylidene) acet- cific resource and environmental needs. In fact, attraction to colors aldehyde (grandlure III), and (E)-(3,3-dimethylcyclohexylidene) in A. musculus was related to the crop phenology as overwintered acetaldehyde (grandlure IV) as components of the male-produced adults were not responsive to any colors, while yellow attracted aggregation pheromone in A. musculus; a fourth component, (E)- mostly the summer generation adults. In blueberries, summer gen- 3,7-dimethyl-2,6-octadien-1-ol (geraniol), was produced by both eration A. musculus adults become active in May–June, when plants males and females. However, the A. musculus aggregation phero- are producing new vegetation and flowering (peak bloom). It is likely mone has performed inconsistently in field trials, pointing at the pos- that these weevils utilize the color of blueberry foliage as one cue sibility of key components missing in the blend (C.R.-S. and H.T.A., to locate their host plant. In fact, yellow is a known foliage-type unpublished data). Moreover, weevil pheromones usually synergize stimulus for many insects (Prokopy and Owens 1983, Lasa et al. with host plant odors (Tewari et al. 2014), and there is also some 2014, Do Bae et al. 2015, Devi and Roy 2017). Interestingly, boll evidence that A. musculus may utilize host-plant volatiles to locate weevil traps also mimic the color of foliage (yellow-green) but blueberry plants (Szendrei et al. 2009, D.S., unpublished data). were much less attractive to A. musculus adults than sticky traps Further studies are needed to optimize an attractant for A. musculus of similar color, indicating that trap design, and not simply color, is and to test whether combining visual and chemical cues enhance the important for capturing this weevil. In addition to color, Szendrei capture of overwintered adults on traps. et al. (2009) reported that volatiles from blueberry flowers are Understanding the behavior of insect pests is critical for the attractive to A. musculus adults, which suggests that multiple cues development of an effective trapping system (Foster and Harris might be employed during host location. More research is needed 1997, Prokopy 1997). From our studies, we learned that A. muscu- to understand the different cues used by overwintered adults dur- lus adults likely fly (rather than walk) to locate highbush blueberry ing their movement into blueberry fields. Attraction of insects to plants and that this flight takes place at heights between 0.5 and colors is based on their sensitivity to different wavelengths of light 1.5 m above ground. We also learned that these weevils seek colors (Li et al. 2017). Yellow, the most attractive to A. musculus adults with high reflectance like yellow during foraging. Additionally, we of those tested here, reflects light at wavelengths between 550 and identified and optimized placement within the canopy of a trap that 600 nm (this study, Mensah et al. 1996, Rodriguez-Saona et al. could be used to monitor A. musculus adults in highbush blueberry 2012). Previous studies have also shown that similar wavelength fields. Yellow sticky traps capture more A. musculus adults than traps ranges (500–600 nm) are most suitable for trapping other weevil designed for other weevil species and colors; and, they need to be species such as A. grandis and Diaprepes abbreviatus L. (Cross et al. placed at the bottom half of blueberry bushes. These traps can reduce Downloaded from https://academic.oup.com/jinsectscience/article-abstract/18/2/19/4915564 by Ed 'DeepDyve' Gillespie user on 16 March 2018 8 Journal of Insect Science, 2018, Vol. 18, No. 2 labor costs associated with the current beat sampling method. The Foster, S. P., and M. O. Harris. 1997. Behavioral manipulation methods for insect pest-management. Annu. Rev. Entomol. 42: 123–146. colored sticky traps employed here attract mostly summer generation Fountain, M. T., C. Baroffio, A. K. Borg-Karlson, P. Brain, J. V. Cross, D. A. musculus adults and do not work well early in the season when I. Farman, and L. Sigsgaard. 2017. Design and deployment of semi- the dispersing overwintered adults are active. This is a major short- ochemical traps for capturing Anthonomus rubi Herbst (Coleoptera: coming because the overwintered adults cause most of the damage Curculionidae) and Lygus rugulipennis Poppius (Hetereoptera: Miridae) to the blueberry crop by feeding and ovipositing on the flower buds in soft fruit crops. Crop Prot. 99: 1–9. (Szendrei and Rodriguez-Saona 2009). Thus far, all visual (this study) Hardee, D. D., A. A. Weathersbee III, J. M. Gillespie, G. L. Snodgrass, and A. and chemical (Szendrei et al. 2011) cues identified for A. musculus R. Quisumbing. 1996. Performance of trap designs, lures, and kill strips for have worked best for the summer generation adults, while the cues the boll weevil (Coleoptera: Curculionidae). J. Econ. Entom. 89: 170–174. used by the overwintered generation have remained elusive. Research Hardwick, S., and B. Harens. 2007. Influence of trap colour, design and height is underway towards the development of a trapping system that inte- on catch of flying clover root weevil adults. N. Z. Plant Prot. 60: 217–222. Lasa, R., O. E. Velázquez, R. Ortega, and E. Acosta. 2014. Efficacy of com- grates visual and chemical cues to improve monitoring and manage- mercial traps and food odor attractants for mass trapping of Anastrepha ment of overwintered A. musculus adults in highbush blueberries. . ludens (Diptera: Tephritidae). J. Econ. Entomol. 107: 198–205. Li, L., H. Ma, L. Niu, D. Han, F. Zhang, J. Chen, and Y. Fu. 2017. Evaluation of chromatic cues for trapping Bactrocera tau. Pest Manag. Sci. 73: 217–222. Acknowledgments Long, B. B. and A. L. Averill. 2003. Compensatory response of cranberry Thanks to Sunil Tewari, Kris Dahl, Manuel Chacón-Fuentes, Sarah Ongaro, to simulated damage by cranberry weevil (Anthonomus musculus Say) and Gabrielle Pintauro for assistance in the field, and to the New Jersey blue- (Coleoptera: Curculionidae). J. Econ. Entomol. 96: 407–412. berry farmers (Macrie Brothers Blueberry Farm, Merlino Brothers Farm, Reeves Marucci, P. E. 1966. Insects and their control, pp. 199–235. In P. Eck and Berries Farm, and North Branch Blueberry & Co.) who kindly allowed us to N. F. Childers (eds.), Blueberry culture. Rutgers University Press, New use their properties as field sites for the experiments. We are also thankful to Dr. Brunswick, NJ. Jenny Lockard, Dr. Pavel Kucheryavy, and Robert Holdcraft for their assistance McQuate, G. T., and C. D. Silva. 2014. Trapping sweetpotato weevil, Cylas with reflectance measurements of colored traps, to Dr. Michael LuValle for sta- formicarius (Coleoptera: Brentidae), with high doses of sex pheromone: tistical advice, and to Dr. George Hamilton and three anonymous reviewers for Catch enhancement and weathering rate in Hawaii. Proc. Hawaii. helpful comments on an early version of the manuscript. This research was finan- Entomol. Soc. 46: 59–69. cially supported by the USDA Pest Management Alternatives Program (PMAP) Mechaber, W. L. 1992. Ecology of Anthonomus musculus: Hostplant finding (Project No. 2012-34381-20108), and a hatch project (No. NJ08192) to C.R-S. and oviposition by cranberry weevil. Ph.D. dissertation. Tufts University, Medford, MA. Mensah, R. K. 1996. Evaluation of coloured sticky traps for monitoring pop- References Cited ulations of Austroasca viridigrisea (Paoli) (Hemiptera: Cicadellidae) on Abuagla, M. A., and M. A. Al-Deeb. 2012. Effect of bait quantity and trap cotton farms. 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