Landscape-scale spatiotemporal dynamics of Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) populations: implications for spatially-based pest management.

BACKGROUND: Brown marmorated stink bug (BMSB), Halyomorpha halys (Stål), is an invasive and severe pest of specialty and row crops. A 2-year field study conducted in four Mid-Atlantic states in the USA characterized the spatial and temporal dynamics of BMSB populations and its association with landscape elements in commercial agriculture settings. In each state, two 1 km2 sites included typical landscape elements (i.e., tree fruit orchards, annual field and vegetable crops, woodlands, and human-made structures). Twenty-seven georeferenced pheromone traps were deployed per site and the number of BMSB adults and nymphs captured was counted throughout the growing season. RESULTS: Findings from spatial analysis by distance indices, along with time-series maps of BMSB distribution, showed that BMSB exhibited significant spatial aggregation, and that its distribution was spatially consistent between years. Analyses with geographic information systems (GIS) revealed that BMSB 'hot spots' occurred in different landscape elements throughout each season. Most patches (i.e., clusters of significantly higher trap captures) were found near woodlands early in the season, near tree fruit orchards in summer, and on the border of annual field crops in autumn. Buffer analysis with GIS indicated that more BMSB adults were captured closer to woodlands compared with other landscape elements. CONCLUSION: Understanding the spatial and temporal movement and distribution of BMSB is critical to predicting their potential impact and ultimately devising strategies to mitigate this risk to vulnerable crops. The results of this study can be used to design streamlined, spatially-based areawide management of BMSB in heterogeneous and complex agricultural landscapes. © 2023 Society of Chemical Industry. This article has been contributed to by U.S. Government employees and their work is in the public domain in the USA.

The Influence of Marking Methods on Mobility, Survivorship, and Field Recovery of Halyomorpha halys (Hemiptera: Pentatomidae) Adults and Nymphs.

Halyomorpha halys (Stål), the brown marmorated stink bug, is an invasive and highly polyphagous insect that has caused serious economic injury to specialty and row crops in the United States and Europe. Here, we evaluated the effects of marking adult and nymphal H. halys with four different colors of fluorescent powder (Blaze Orange, Corona Pink, Horizon Blue, and Signal Green) on mobility and survivorship in laboratory bioassays. Adults and nymphs were marked using liquified fluorescent powder solutions and allowed to dry prior to bioassay. The presence of the marking solution had no significant effects on adult or nymphal mobility, adult survivorship, nymphal development, or adult flight capacity. We also evaluated the persistence of neon marker applied to the pronotum of H. halys adults and found this technique remained detectable for 2 wk under field conditions. Although both marking techniques are inexpensive, persist for ≥1 wk, and do not affect mortality, the neon marker method is more time-consuming, taking ~12 times longer to mark 50 adult H. halys compared with the liquified fluorescent powders. Thus, we would recommend using fluorescent powders for large-scale mark-release-recapture studies.

Brown marmorated stink bug overwintering aggregations are not regulated through vibrational signals during autumn dispersal.

The brown marmorated stink bug, Halyomorpha halys (Heteroptera: Pentatomidae), is regarded as one of the world's most pernicious invasive pest species, as it feeds on a wide range of economically important crops. During the autumn dispersal period, H. halys ultimately moves to potential overwintering sites, such as human-made structures or trees where it will alight and seek out a final overwintering location, often aggregating with other adults. The cues used during this process are unknown, but may involve vibrational signals. We evaluated whether vibrational signals regulate cluster aggregation in H. halys in overwintering site selection. We collected acoustic data for six weeks during the autumn dispersal period and used it to quantify movement and detect vibrational communication of individuals colonizing overwintering shelters. Both movement and vibrational signal production increased after the second week, reaching their maxima in week four, before decaying again. We found that only males produced vibrations in this context, yet there was no correlation between movement and vibrational signals, which was confirmed through playback experiments. The cues regulating the formation of aggregations remain largely unknown, but vibrations may indicate group size.

Attractiveness of Pheromone Components With and Without the Synergist, Methyl (2E,4E,6Z)-2,4,6-Decatrienoate, to Brown Marmorated Stink Bug (Hemiptera: Pentatomidae).

The brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is attracted to its male-produced aggregation pheromone, a ~3.5:1 mixture of (3S,6S,7R,10S)- and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (SSRS and RSRS respectively), and also to the pheromone of its Asian sympatric species Plautia stali Scott (Hemiptera: Pentatomidae), methyl (2E,4E,6Z)-2,4,6-decatrienoate (MDT). A stereoisomeric mixture of (7R) 10,11-epoxy-1-bisabolen-3-ols (= mixed murgantiols) is used together in commercialized products with MDT because the latter is a synergist for H. halys attraction to mixed murgantiols. However, the optimal ratio for MDT combination with mixed murgantiols, and the sensitivity of bug captures to variation in ratio of the two pheromone components, have not been tested to date. Using black pyramid traps at two sites (in Maryland and West Virginia, United States), different ratios of mixed murgantiols to MDT were tested over two entire seasons. Also, captures using various ratios of the two active pheromone stereoisomers were undertaken in month-long trials with and without MDT. Results showed that H. halys adult and nymphal captures were relatively insensitive to the ratio of synthetic pheromone (mixed murgantiols) to MDT, as long as each was present in the trap. Captures of adults and nymphs were responsive to the lure loading of the SSRS isomer, but relatively insensitive to levels of the minor component, RSRS. The relative insensitivity of H. halys to these attractant ratios gives flexibility to development of more cost-efficient synthesis and trapping as well as other semiochemical-based management tactics.

Estimating Monitoring Trap Plume Reach and Trapping Area for Nymphal and Adult Halyomorpha halys (Hemiptera: Pentatomidae) in Crop and Non-crop Habitats.

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), the brown marmorated stink bug, is an invasive polyphagous insect that can cause serious economic injury to specialty and row crops in the United States and globally. To date, H. halys has been managed with repeated insecticide applications. While progress has been made toward development of trap-based monitoring tools to guide management decisions, little is known regarding the trapping area over which a single pheromone-baited trap captures H. halys. We conducted single trap, multiple distance mark-release-recapture experiments; results were used to estimate trapping area for nymphs and adults in sites without host plants present (open field) and for adults in sites with host plants present (apple orchard). Plume reach for pheromone-baited sticky traps was consistently estimated to be <3 m. Maximum dispersive distance in an open field devoid of host plants was estimated to be 40 m for nymphs and 120-130 m for adults resulting in trapping areas of 0.58 ha and 4.83-5.56 ha, respectively. When traps were deployed in association with host plants within the border row of an apple orchard, adult maximum dispersive distance and trapping area was reduced to 70 m and 1.67 ha, respectively. These results indicate that the behavioral response of H. halys to pheromonal stimuli is influenced by the presence of host plants and that trapping area for pheromone-baited traps will likely change relative to the cropping system in which it is deployed. Caution should be taken when extrapolating these results, because the measured values may differ in other crop systems.

Overwintering Behavior of Drosophila suzukii, and Potential Springtime Diets for Egg Maturation.

Spotted wing drosophila, Drosophila suzukii (Matsumura) (Diptera: Drosophilidae), is a serious agricultural pest, which lays eggs in ripe and ripening fruits of several cultivated and wild host plants. Here we explore several factors that may be critical to winter survival and improve D. suzukii's ability to successfully overwinter in northern climates and reestablish populations in the spring. Cold acclimation improved mobility in low-temperature laboratory mobility assays and improved survivorship in two wintertime field studies. Acclimation improved survivorship in experiments where overwintering habitats were above ground level and where habitats were at soil level by 1.9- and 13.7-fold, respectively. Soil acts to buffer changes in temperature, and the groundcovers investigated here provided microclimates that were 1-2°C warmer than bare soil during chilling events, and roughly 5°C cooler than bare soil during warm spells. Acclimated flies preferred overwintering substrates with a food source (dropped apple) over any other substrate (leaf litter, barky sticks, or bare soil). Pigeon (Columba livia L.) droppings and mushrooms (Peziza sp.) were identified as potential overwintering protein sources in laboratory feeding studies. Laboratory-simulated winter stress negatively influenced return of female reproduction, so future assays should consider biologically relevant subjects.

Improved Trap Designs and Retention Mechanisms for Halyomorpha halys (Hemiptera: Pentatomidae).

Current monitoring systems for the invasive Halyomorpha halys (Stål) (Hemiptera; Pentatomidae) in orchard agroecosystems rely on ground-deployed tall black pyramid traps baited with the two-component H. halys aggregation pheromone and pheromone synergist. Pyramid traps are comparatively costly, require considerable time to deploy and service, and may not be best suited to grower needs. Therefore, we evaluated other traps for H. halys, including modified pyramid traps (lures deployed on the outside), a canopy-deployed small pyramid, a pipe trap, delta traps, and yellow sticky cards in 2015 and 2016 in commercial apple and peach orchards. We also compared various H. halys killing agents for use in standard pyramid trap collection jars, including VaporTape kill strips, cattle ear tags, and plastic netting treated with various pyrethroids. Finally, we evaluated the effect of positioning the lures inside versus outside the collection jar on standard pyramid traps on overall captures. Among trap types, modified pyramid and pipe traps were most effective, capturing more adults than all other trap designs. Adult captures in small canopy-deployed pyramid, delta, and yellow sticky traps were lower, but significantly correlated with the standard black pyramid. Placing lures on the outside of collection jars on pyramid traps resulted in significantly greater captures and insecticide-impregnated netting was as effective for retaining bugs as VaporTape strips. These studies demonstrate that trapping systems for H. halys can be simplified and improved by modifying the trap design, lure deployment location, and/or killing agent.

Monitoring and Biosurveillance Tools for the Brown Marmorated Stink Bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae).

Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is an invasive pest of numerous agricultural crops with an increasing global distribution. Finding simple and reliable monitoring tools for H. halys agricultural and surveillance programs is imperative. In 2016, we compared standard pyramid traps to clear sticky cards attached atop wooden stakes and evaluated two commercially formulated lures (Trécé and AgBio) with low and high rates of the H. halys aggregation pheromone (PHER) and pheromone synergist (MDT) at 12 sites (low: 5 mg PHER + 50 mg MDT; high: 20 mg PHER + 200 mg MDT). In 2017, we reevaluated lure efficacy using only the clear sticky traps at six locations. Sites were classified as having low, moderate, or high relative population densities of H. halys in 2016, and as very low or low densities of H. halys in 2017. Although clear sticky traps captured fewer adults and nymphs than pyramid traps, their captures were generally correlated at all population levels indicating that clear sticky traps can reliably monitor H. halys presence and relative abundance regardless of relative population density. During both years, adult and nymphal captures were significantly greater in traps baited with Trécé lures than with AgBio lures. Captures were greater in traps baited with high loading rate lures for each lure type, and with the exception of traps baited with AgBio lures at high relative density sites in 2016, H. halys captures in traps with low and high loading rates of each lure type were correlated for both years. Comparison of yellow and clear sticky cards indicated they performed equally, but yellow cards captured more nontargets. In summary, clear sticky traps attached atop wooden posts and baited with H. halys pheromone and pheromone synergist lures are an effective option for this pest monitoring and detection.

Identification of volatiles released by diapausing brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae).

The brown marmorated stink bug, Halyomorpha halys, is an agricultural and urban pest that has become widely established as an invasive species of major concern in the USA and across Europe. This species forms large aggregations when entering diapause, and it is often these aggregations that are found by officials conducting inspections of internationally shipped freight. Identifying the presence of diapausing aggregations of H. halys using their emissions of volatile organic compounds (VOCs) may be a potential means for detecting and intercepting them during international freight inspections. Headspace samples were collected from aggregations of diapausing H. halys using volatile collection traps (VCTs) and solid phase microextraction. The only compound detected in all samples was tridecane, with small amounts of (E)-2-decenal found in most samples. We also monitored the release of defensive odors, following mechanical agitation of diapausing and diapause-disrupted adult H. halys. Diapausing groups were significantly more likely to release defensive odors than diapause-disrupted groups. The predominant compounds consistently found from both groups were tridecane, (E)-2-decenal, and 4-oxo-(E)-2-hexenal, with a small abundance of dodecane. Our findings show that diapausing H. halys do release defensive compounds, and suggest that volatile sampling may be feasible to detect H. halys in freight.

Enhanced Response of Halyomorpha halys (Hemiptera: Pentatomidae) to Its Aggregation Pheromone with Ethyl Decatrienoate.

The invasive stink bug species, Halyomorpha halys (Stål) (Hemiptera; Pentatomidae), severely damages multiple agricultural commodities, resulting in the disruption of established IPM programs. Several semiochemicals have been identified to attract H. halys to traps and monitor their presence, abundance, and seasonal activity. In particular, the two-component aggregation pheromone of H. halys, (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (PHER), in combination with the pheromone synergist, methyl (2E,4E,6Z)-decatrienoate (MDT), were found to be attractive. Here, we report that an analogous trienoate, ethyl (2E,4E,6Z)-decatrienoate (EDT), enhances H. halys captures when combined with PHER. In trials conducted in Eastern and Western regions of the United States, we observed that when traps were baited with the H. halys PHER + EDT, captures were significantly greater than when traps were baited with PHER alone. Traps baited with EDT alone were not attractive. Thus, the addition of EDT to lures for attracting H. halys to traps may further improve monitoring efficiency and management strategies for this invasive species.

Development of an Attract-and-Kill Strategy for Drosophila suzukii (Diptera: Drosophilidae): Evaluation of Attracticidal Spheres Under Laboratory and Field Conditions.

Drosophila suzukii Matsumura (Diptera: Drosophilidae) is an invasive, polyphagous fruit fly that attacks soft-skinned fruits. Originally from Asia, D. suzukii has successfully invaded the United States and the European and South American countries. At present, calendar-based insecticide applications are used to combat D. suzukii. Here, we evaluate a behaviorally based attract-and-kill management technique using attracticidal spheres to reduce D. suzukii infestations in raspberries. In laboratory bioassays aimed at identifying effective toxicants, attracticidal spheres containing dinotefuran at 1.0% a.i. killed 100% of D. suzukii within 5 min. Spinetoram, spinosad, permethrin, lambda-cyhalothrin (CS) and lambda-cyhalothrin (WG), all at 1.0% a.i., killed 100% of D. suzukii within 24 h. In field trials, statistically equivalent infestation rates were recorded in raspberry plots protected by attracticidal spheres containing 1.0% a.i. spinetoram compared with standard weekly insecticide applications. In field trials using 1.0% a.i. dinotefuran, attracticidal spheres decreased D. suzukii infestations compared with control plots, but insecticide applications were more effective at reducing D. suzukii infestations, although differences in harvesting practices likely affected fly population densities and infestation rates in both years. Attracticidal spheres effectively attract and kill D. suzukii and reduce infestations rates under field conditions, indicating that this behavioral strategy holds promise in D. suzukii management.

Landscape Factors Influencing Stink Bug Injury in Mid-Atlantic Tomato Fields.

Landscape structure and diversity influence insect species abundance. In agricultural systems, adjacent crop and non-crop habitats can influence pest species population dynamics and intensify economic damage. To investigate the influence of landscape factors on stink bug damage in agricultural systems, we assessed stink bug damage from 30 processing tomato fields in the mid-Atlantic United States and analyzed landscape structure and geographic location. We found that forest shape and size, and geographic location strongly influenced stink bug damage. Landscapes with larger forest edge in southern portions of the mid-Atlantic region experienced the greatest damage, perhaps owing to the introduction of the invasive brown marmorated stink bug. We conclude that landscape structure will likely influence damage rates in nearby agricultural fields.

Behavioral Responses of Drosophila suzukii (Diptera: Drosophilidae) to Visual Stimuli Under Laboratory, Semifield, and Field Conditions.

Drosophila suzukii Matsumura (Diptera: Drosophilidae) is an invasive pest in North America and Europe that attacks soft-skinned ripening fruit such as raspberries, blackberries, and blueberries. Little is known regarding the specific cues D. suzukii utilizes to locate and select host fruit, and inconsistencies in trap performance indicate the need for the development of improved monitoring and management techniques for this insect. Our studies focused on identifying attractive visual cues for adult D. suzukii and incorporating these cues into a potential attract-and-kill tactic for D. suzukii management. We evaluated D. suzukii response to color, shape, and size-specific stimuli. For color, we evaluated 10.2-cm-diameter spheres painted black, red, purple, orange, green, yellow, blue, or white. Shape stimuli (254 cm3 surface area) included sphere, cube, pyramid, inverted pyramid, vertical or horizontal cylinder and were painted red. Size stimuli included red 2.5-, 10.2-, 15.2-, and 25.4-cm-diameter spheres. Trials were conducted under laboratory, semifield, and field conditions. For color, adults preferred black and red spheres to all other colors evaluated. Among shapes, there was no significant preference. For size, larger spheres captured significantly more D. suzukii compared with a small 2.5-cm-diameter sphere. Determining D. suzukii visual preference will aid in trapping and behaviorally based management programs.

Handheld lasers allow efficient detection of fluorescent marked organisms in the field.

Marking organisms with fluorescent dyes and powders is a common technique used in ecological field studies that monitor movement of organisms to examine life history traits, behaviors, and population dynamics. External fluorescent marking is relatively inexpensive and can be readily employed to quickly mark large numbers of individuals; however, the ability to detect marked organisms in the field at night has been hampered by the limited detection distances provided by portable fluorescent ultraviolet lamps. In recent years, significant advances in LED lamp and laser technology have led to development of powerful, low-cost ultraviolet light sources. In this study, we evaluate the potential of these new technologies to improve detection of fluorescent-marked organisms in the field and to create new possibilities for tracking marked organisms in visually challenging environments such as tree canopies and aquatic habitats. Using handheld lasers, we document a method that provides a fivefold increase in detection distance over previously available technologies. This method allows easy scouting of tree canopies (from the ground), as well as shallow aquatic systems. This novel detection method for fluorescent-marked organisms thus promises to significantly enhance the use of fluorescent marking as a non-destructive technique for tracking organisms in natural environments, facilitating field studies that aim to document otherwise inaccessible aspects of the movement, behavior, and population dynamics of study organisms, including species with significant economic impacts or relevance for ecology and human health.