Numerous species of herbivorous stink bugs (Hemiptera: Pentatomidae), including both endemic and exotic species, are serious pests of many agronomic crops (Leskey and Nielsen 2018, McPherson and McPherson 2000) and are known to feed and develop on many horticultural plants, including trees and shrubs (McPherson and McPherson 2000, Tillman and Cottrell 2016a). Monitoring these pests is key to making management decisions to control them and is an important aspect of conducting research on them. Various methods have been used to monitor pest stink bugs including sweep netting (Awuni et al. 2015, Pezzini et al. 2019), black light traps (Kamminga et al. 2009, Nielsen et al. 2013), drop cloths (Pilkay et al. 2013), and pheromone traps (Cottrell et al. 2000, ni et al. 2019). Our focus is on pheromone traps and specifically the pyramid trap that has frequently been used to monitor stink bugs.

The Tedders trap, a black pyramid base topped with a boll weevil (Anthonomous grandis grandis Boheman) trap, was originally designed and used, without a lure, to monitor emergence of adult pecan weevil, Curculio caryae (Horn) (Coleoptera: Curculionidae) in pecan, Carya illinoinensis (Wangenh.) K. Koch, orchards (Tedders and Wood 1994, Tedders et al. 1996). Mizell and Tedders (1995) modified the original Tedders trap by painting it bright yellow and using a larger collection device made from screen to trap stink bugs, including Euschistus servus (Say), Euschistus tristigmus (Say), Oebalus pugnax (F.), Nezara viridula (L.), Acrosternum hilare (Say), Proxys punctulatus (Palisot), and Brochymena spp. In tests using the yellow pyramid trap combined with lures containing the Euschistus spp. aggregation pheromone methyl (2E,4Z) decadienoate (i.e., MDD) (Aldrich et al. 1991), 94% of trap capture in pecan orchards in central Georgia (Yonce and Mizell 1997) and 78% of trap capture in mid-Atlantic apple and peach orchards (Leskey and Hogmire 2005) was comprised of E. servus and E. tristigmus. Since, the yellow pyramid stink bug trap has been used in many studies documenting abundance and movement of stink bugs, usually in concert with a pheromone attractive to certain stink bug species (Cottrell et al. 2000, Cowell et al. 2015, Ni et al. 2019).

When the exotic brown marmorated stink bug, Halyomorpha halys Stål, began spreading through the mid-Atlantic United States (Leskey and Nielsen 2018), studies with this pest led to black pyramid traps being used in conjunction with the two-component aggregation pheromone and a synergist for H. halys (Akotsen-Mensah et al. 2018, Joseph et al. 2013, Leskey et al. 2012, Morrison et al. 2015, Rice et al. 2018). However, establishment of H. halys in the southeastern United States has been documented using pheromone-baited yellow pyramid traps (Penca and Hodges 2018, Tillman et al. 2017), which are commonly used for monitoring native stink bug species (Brennan et al. 2013, Cottrell and Tillman 2019, Ni et al. 2019, Tillman et al. 2010, Tillman and Cottrell 2019).

Because stink bug species of economic importance are polyphagous and are found attacking many of the same crops, using one type of trap or one color of a pyramid trap base for all species would be advantageous for monitoring purposes. Therefore, our objective was to compare yellow and black pheromone-baited pyramid traps to determine if one or the other was superior for trapping herbivorous stink bugs. Additionally, we documented residual activity of the pheromone lure, via trap capture, over 1-mo intervals.

Materials and Methods

Stink bug traps. Black and yellow pyramid traps were constructed as described by Tedders and Wood (1994) and Mizell and Tedders (1995). Traps consisted of 2.8-L clear plastic polyethylene terephthalate jars (United States Plastic Corp., Lima, OH) placed on top of 1.22-m-tall pyramid bases. An insecticidal ear tag (10% λ-cyhalothrin and 13% piperonyl butoxide) (Saber Extra, Schering-Plough Animal Health Corp., Union, NJ), as used by Cottrell (2001), was placed in each jar as a kill tactic to decrease stink bug escape (Cottrell 2001, Hogmire and Leskey 2006).

Pheromone lure. Traps were baited with a Stink Bug Xtra Combo lure (AgBio Inc., Westminster, CO), which was replaced monthly. This lure contains the aggregation pheromone (approximately 5 mg of 10,11-epoxy-1bisabolen-3-ol) and synergist (methyl [2E,4Z,6Z]-decatrienoate) (i.e., MDT) for H. halys and the aggregation pheromone of Euschistus spp. (approximately 50 mg of MDD) (Akotsen-Mensah et al. 2018, Weber et al. 2014). Trap samples were collected weekly, specimens were returned to the laboratory and stored in a freezer until identified, with the aid of a dissecting microscope when necessary.

Study sites. Four sites, one in central Georgia (USDA Agricultural Research Service [ARS], Southeastern Fruit and Tree Nut Research Laboratory, Byron), two in central Alabama (Auburn University main campus, Auburn; Auburn University, Chilton Research and Extension Center, Clanton), and one in southern Alabama (Auburn University, Gulf Coast Research and Extension Center, Fairhope) were used to monitor stink bugs during 2016 and 2017 (Table 1). At each site, four replicates of two traps (a black and a yellow trap) were used. Traps within replicates were 20–100 m apart and replicates were 20–100 m apart. Habitats included in the study varied by replicate and/or location (Table 1).

Table 1 Stink bug trapping locations, global positioning system (GPS) coordinates, habitats, and range of dates traps were sampled.

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Statistical analysis. Collection dates for traps were not started or stopped on the same date at each location (Table 1); thus, the interval encompassing the earliest and latest sample dates, common to all locations, was used for comparing capture in black versus yellow pyramid traps across locations. This provided an equal sampling interval done at the same time. Although data were collected weekly, cumulative data for the sampling interval of each year were subjected to analysis of variance (ANOVA) (JMP^®, Version 14.3, SAS Institute Inc., Cary, NC). Captures of adult H. halys and adult E. servus were analyzed singly, whereas other adult Euschistus spp. (excluding E. servus) were grouped for analysis. Similarly, all adults of native, herbivorous species of Pentatomidae were grouped for analysis. Nymphal H. halys collected during 2017 were analyzed similarly but during 2016 these data were only collected at the Byron, GA, location. Because no H. halys were captured at the Fairhope, AL, location either year, that location was excluded from analyses with H. halys. A mixed model repeated measures ANOVA (JMP, Version 14.3, SAS Institute Inc., Cary, NC) was used to analyze trap capture of adult H. halys and E. servus, from the Byron, GA, location only for 2016 (five 4-week intervals) and 2017 (eight 4-week intervals), with respect to time after pheromone placement in traps.

Results

Capture of H. halys occurred at all locations each year except at the most southerly location in Fairhope, AL, where none were captured either year. Pyramid trap color, black or yellow, did not influence capture of H. halys adults during 2016 (F = 0.93; df = 1, 7; P = 0.4053) or 2017 (F = 0.18; df = 1, 7; P = 0.6970) (Fig. 1). Similarly, capture of H. halys nymphs was not affected by trap color at one location during 2016 (F = 4.40; df = 1, 7; P = 0.1270) or three locations during 2017 (F = 7.68; df = 1, 5; P = 0.1093) (Fig. 2). Nymph data were not collected at either Alabama location during 2016.

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Although capture of E. servus was always numerically higher in yellow than black traps, the difference was not significant during 2016 or 2017 (F= 4.38; df = 1, 7; P = 0.1275 and F = 5.66; df = 1, 7; P = 0.0976, respectively) (Fig. 3). Other Euschistus spp. captured included E. tristigmus, Euschistus ictericus (L.), Euschistus quadrator Rolston, and Euschistus obscurus (Palisot). Their capture followed suit with numerically higher capture in yellow traps but was not significantly greater than in black traps either year (F= 1.98; df = 1, 7; P= 0.2538 and F= 1.35; df = 1, 7; P = 0.3295, respectively) (Fig. 4).

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Native Pentatomidae captured in traps included Amaurochrous spp., Banasa spp., Brochymena spp., Chinavia hilaris (Say), E. servus, E. tristigmus, E. quadrator, E. ictericus, E. obscurus, Holcostethus limbolarious (Say), Hymenarcys spp., Murgantia histrionica (Hahn), Oebalus pugnax, and Thyanta spp. Their capture in black versus yellow traps was significantly different during 2016 (F = 10.38; df = 1, 7; P = 0.0485) but not during 2017 (F = 6.12; df = 1, 7; P = 0.0898) (Fig. 5).

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Trap capture of the invasive H. halys was highest the first week following placement of a new lure in a trap compared with Weeks 2–4 during both 2016 and 2017 at Byron, GA (F = 33.46; df = 3, 21; P < 0.0001 and F = 16.55; df = 3, 21; P < 0.0001, respectively) (Fig. 6). No difference in trap capture was detected between Weeks 2 and 4. A similar effect was seen regarding capture of E. servus with significantly more captured the first week following lure placement than for Weeks 2–4 at Byron, GA, during 2016 and 2017 (F = 35.80; df = 3, 21; P < 0.001 and F = 21.30; df = 3, 21; P < 0.001, respectively). During 2016, however, significantly more E. servus were captured the second week following lure placement in a trap compared with Weeks 3–4 (Fig. 7).

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Discussion

Results from our study show that capture of H. halys adults was not significantly different when black or yellow pyramid traps were used in conjunction with the Stink Bug Xtra Combo lure. Also, the difference in capture of nymphs in yellow versus black pyramid traps was not significant, although numerically, more were captured in black traps. Finding no significant difference in capture between black and yellow pyramid traps supports using either color, with a pheromone lure, for monitoring H. halys adults and nymphs. Leskey et al. (2012) also showed no difference in capture of adult or nymphal H. halys when using black, green, white, yellow, or clear pyramid traps and whether using a lure or not. In fact, clear sticky traps used with a pheromone lure are now commonly used to monitor H. halys (Acebes-Doria et al. 2018). Capture of H. halys on clear sticky traps suggests that the pheromone used for monitoring H. halys is more important than visual cues provided by a trap. Similarly, capture of adult E. servus and other Euschistus spp., although always numerically higher in yellow than black traps, was never significantly different. The only significant difference in capture between black and yellow traps was when data for all native species were grouped and significantly more were captured in yellow traps during 2016, but not during 2017.

Captures of adult H. halys and E. servus were always significantly higher during the first week after a lure was placed in a trap than captures during Weeks 2–4, likely due to pheromone depletion of the lure. This is not surprising as a reduction in stink bug capture over time when using the same lure is generally expected, as reported by Cottrell and Horton (2011). Joseph et al. (2013) also report that lure age is a significant factor in H. halys capture. Their study was conducted during September starting with different aged lures for a discreet trapping interval, whereas our study was conducted across the season as lures aged in traps. In this study, traps were at least 4 m from host trees (i.e., peach or pear). This indicates that the area of attraction for these traps was at least 4 m and was likely affected by a decline in pheromone release from the lure. This study was run longer than fruit were present on trees with similar results, so it is not likely that presence or absence of fruit explains any difference in trap capture over time. Tillman and Cottrell (2016b) documented significantly more nymphs of E. servus, E. tristigmus, and Chinavia hilaris in yellow pyramid traps baited with MDD lures, replaced weekly, than in traps without lures. Nymphs were attracted by MDD from unknown distances but per the study parameters, probably more than a few meters, and likely followed a pheromone gradient across the ground to the trap. The distance from which a pheromone is received and acted upon is affected by many factors, and our results strongly suggest that pheromone depletion from lures over time is an important factor. In fact, Joseph et al. (2013) report that there is a high release rate of MDT during Days 1–3 after lure placement in a trap but a much lower and steadier release rate over the following weeks.

Our data suggest that traps, used in conjunction with a pheromone, to monitor multiple species of adult stink bugs, especially native species, would favor using yellow traps. Certainly, the objectives of an individual study or pest management practice directed against one pest species, such as H. halys, could be monitored using either trap color. However, as H. halys continues to spread across the southeastern United States, other pestiferous stink bug species will still need to be monitored and can be with yellow pyramid traps baited with appropriate pheromone lures changed at an interval of less than 1 mo. Future research regarding using yellow traps should focus on trap size and/or shape to determine if a smaller, more economical trap provides consistent capture and what role visibility of traps from various distances has on capture.