William R. Morrison

Attraction of the invasive halyomorpha halys (Hemiptera: Pentatomidae) to traps baited with semiochemical stimuli across the United States

ABSTRACT A recent identification of the two-component aggregation pheromone of the invasive stink bug species, Halyomorpha halys (Stål), in association with a synergist, has greatly improved the ability to accurately monitor the seasonal abundance and distribution of this destructive pest. We evaluated the attraction of H. halys to black pyramid traps baited with lures containing the pheromone alone, the synergist methyl (2E,4E,6Z)-decatrienoate (MDT) alone, and the two lures in combination. Traps were deployed around areas of agricultural production including fruit orchards, vegetables, ornamentals, or row crops in Delaware, Maryland, North Carolina, New Jersey, New York, Ohio, Oregon, Pennsylvania, Virginia, and West Virginia from mid-April to mid-October, 2012 and 2013. We confirmed that H. halys adults and nymphs are attracted to the aggregation pheromone season long, but that attraction is significantly increased with the addition of the synergist MDT. H. halys adults were detected in April with peak captures of overwintering adults in mid- to late May. The largest adult captures were late in the summer, typically in early September. Nymphal captures began in late May and continued season long. Total captures declined rapidly in autumn and ceased by mid-October. Captures were greatest at locations in the Eastern Inland region, followed by those in the Eastern Coastal Plain and Pacific Northwest. Importantly, regardless of location in the United States, all mobile life stages of H. halys consistently responded to the combination of H. halys aggregation pheromone and the synergist throughout the entire season, suggesting that these stimuli will be useful tools to monitor for H. halys in managed systems.

Evaluation of Trap Designs and Deployment Strategies for Capturing Halyomorpha halys (Hemiptera: Pentatomidae)

ABSTRACT Halyomorpha halys (Sta° l) is an invasive pest that attacks numerous crops. For growers to make informed management decisions against H. halys, an effective monitoring tool must be in place. We evaluated various trap designs baited with the two-component aggregation pheromone of H. halys and synergist and deployed in commercial apple orchards.We compared our current experimental standard trap, a black plywood pyramid trap 1.22 m in height deployed between border row apple trees with other trap designs for two growing seasons. These included a black lightweight coroplast pyramid trap of similar dimension, a smaller (29 cm) pyramid trap also ground deployed, a smaller limb-attached pyramid trap, a smaller pyramid trap hanging from a horizontal branch, and a semipyramid design known as the Rescue trap.We found that the coroplast pyramid was the most sensitive, capturing more adults than all other trap designs including our experimental standard. Smaller pyramid traps performed equally in adult captures to our experimental standard, though nymphal captures were statistically lower for the hanging traps. Experimental standard plywood and coroplast pyramid trap correlations were strong, suggesting that standard plywood pyramid traps could be replaced with lighter, cheaper coroplast pyramid traps. Strong correlations with small ground- and limb-deployed pyramid traps also suggest that these designs offer promise as well. Growers may be able to adopt alternative trap designs that are cheaper, lighter, and easier to deploy to monitor H. halys in orchards without a significant loss in sensitivity.

Indigenous arthropod natural enemies of the invasive brown marmorated stink bug in North America and Europe

Since the establishment of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) in North America and Europe, there has been a large, multi-group effort to characterize the composition and impact of the indigenous community of arthropod natural enemies attacking this invasive pest. In this review, we combine 98 indigenous natural enemy datasets spanning a variety of sampling methods, habitats, and geographic areas. To date, the vast majority of H. halys biological control research has focused on the egg stage, using sentinel egg masses to characterize indigenous parasitoid and predator communities and their contribution to H. halys egg mortality. Although egg parasitism and predation levels by indigenous natural enemies are low (typically <10% each) in most surveys, total egg mortality attributable to natural enemies can be higher (typically between 5 and 25%; up to 83%)—even though these values were likely underestimated in most cases because some mortality due to biological control was not recognized. In North America, where the most data are available, it appears that the relative prevalence of different indigenous parasitoid species varies among habitat types, particularly between crop and non-crop habitats. Predator species responsible for egg mortality are much less commonly identified, but appear to include a wide variety of generalist chewing and sucking predators. To date, studies of natural enemies attacking H. halys nymphs and adults are relatively rare. Based on our review, we identify a number of key research gaps and suggest several directions for future research.

Chemical ecology of Halyomorpha halys: discoveries and applications

There have been notable and significant advances in elucidating the chemical ecology of the invasive Halyomorpha halys (Hemiptera: Pentatomidae), brown marmorated stink bug. This highly destructive and polyphagous pest is originally from Korea, China, and Japan, but was accidentally introduced into North America and Europe. Prior to its invasion into these regions, little was known about its chemical ecology. However, since then, researchers have identified and synthesized its aggregation pheromone, documented its synergism with the pheromone of another Asian stink bug, Plautia stali, developed monitoring traps of various designs, and lures with reliable attractants have become commercially available. Furthermore, plant volatiles have been shown to have attractive, neutral, and repellent effects on attraction and retention of H. halys, and H. halys-derived volatiles have been shown to play a role in recruiting natural enemies. Finally, management strategies based on pheromone-based technology have been evaluated, including insecticide applications based on a cumulative threshold of adult captures in pheromone-baited traps, and the use of intensively baited trees in an attract-and-kill strategy to manage this pest. This review summarizes the available literature on the chemical ecology of H. halys and concludes with several research areas that should be explored in future research.

Characterizing spring emergence of adult Halyomorpha halys using experimental overwintering shelters and commercial pheromone traps

To improve our understanding of adult Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) overwintering biology and to better inform models of its population dynamics, its temporal pattern of spring emergence was investigated using experimental overwintering shelters in screened cages within protective structures. In 2012, plastic shelters containing 100 adults were deployed in unheated, unlighted buildings, and adjacent woodlots in Virginia, USA. In 2013 and 2014, wooden shelters containing 300 paint‐marked adults were deployed in pairs in six woodlots across Virginia, West Virginia, and Maryland, USA; one in a closed cage and one in a cage with the top removed, enabling emerged adults to be counted or to disperse, respectively. In 2013 and 2014, pheromone‐baited and non‐baited pyramid traps encircled the shelters at each site. Regular counts of adults that emerged into the closed cage and of marked and ‘wild’ (unmarked) adults captured in traps were conducted from February or March through early July. In 2012, emergence patterns from shelters in buildings and woodlots were very similar and matched those recorded from woodlots in 2013 and 2014. In all years, a small peak of emergence occurred in about mid‐April, a larger and more prolonged peak was observed between mid‐May and early June, and emergence ended by early July. Of the 449 H. halys adults captured in traps between 2013 and 2014, only three were marked individuals from shelters in the open cage, suggesting that adults emerging from overwintering sites may require a dispersal flight before responding to pheromone‐baited traps. In 2013 and 2014, respectively, 98 and 93% of captures were in pheromone‐baited traps, but there was no correlation between the weekly number of adults that emerged from shelters in the closed cages and captures in traps.

The consequences of sublethal exposure to insecticide on the survivorship and mobility of Halyomorpha halys (Hemiptera: Pentatomidae)

BACKGROUND The direct lethal effects of conventional and organic insecticides have been investigated thoroughly for all life stages of Halyomorpha halys. However, the sublethal effects of insecticides on the behavior of H. halys have not been well documented. Our aims were to evaluate the impact of a brief 5 min exposure to residues of bifenthrin, dinotefuran, methomyl, thiamethoxam and thiamethoxam + λ-cyhalothrin on survivorship, horizontal and vertical movement, and flight capacity of adult H. halys under laboratory conditions. RESULTS Over half of the insecticide-exposed adults were classified as affected, moribund or dead after the 5 min exposure, compared with only 6% of the adults in the water-only control. We found that the horizontal movement, vertical climbing and flight capacity of adults exposed to insecticides were decreased by 20-60% overall relative to the water-only control. The most lethal insecticide was bifenthrin. CONCLUSION Many insecticide-exposed H. halys adults retained significant mobility and flight capacity, with flight most pronounced immediately after exposure. These results suggest that brief exposure periods to efficacious insecticides will result in high dispersal and low mortality. Therefore, management strategies that enhance the retention of H. halys on insecticide-coated surfaces should be considered to ensure that adults are exposed to a lethal dose of insecticide.

Attraction of the invasive Halyomorpha halys in its native Asian range to traps baited with semiochemical stimuli

The brown marmorated stink bug, Halyomorpha halys, is considered a serious invasive species capable of causing significant agricultural and nuisance problems. Researchers in the USA recently identified the two-component H. halys aggregation pheromone from populations in North America and found that when it is combined with the pheromone synergist methyl decatrienoate (MDT), it resulted in reliable, season-long captures of H. halys throughout the USA. However, no study has assessed whether H. halys populations in the native range are attracted to and can also be reliably captured by the combination of these stimuli. In this study, our goal was to evaluate the response of H. halys adults, nymphs, and non-target organisms to traps baited with the aggregation pheromone, MDT alone, or in combination at three locations in the native range. Traps baited with combined stimuli reliably captured the greatest numbers of H. halys adults and nymphs, and traps baited with either lure treatment caught a unique community of non-target organisms. In addition, Plautia stali was cross-attracted to the H. halys aggregation pheromone. Overall, we demonstrate that the pheromone-based tools developed in the USA may be used for worldwide detection and surveillance programs for H. halys and P. stali.

Behavioral Responses of the Invasive Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) to Light-Based Stimuli in the Laboratory and Field

Halyomorpha halys (Stål), brown marmorated stink bug, is an invasive insect native to Asia that was accidently introduced into the United States. The species is a polyphagous pest that has caused serious economic injury to specialty and row crops in the mid-Atlantic region. Growers have targeted H. halys with broad-spectrum materials by increasing the number of and decreasing the interval between insecticide applications. While it is known that adults reliably respond to semiochemical cues, much less is known about the response of H. halys to visual stimuli. Field observations suggest that H. halys adults respond to light-based stimuli, with large aggregations of adults documented at outdoor light sources and captured in commercial blacklight traps. Therefore, we conducted a series of studies aimed at identifying optimal wavelengths and intensities of light attractive to H. halys adults. We found that intensity and wavelength of light affected H. halys response in the laboratory and field. In the laboratory, H. halys demonstrated positive phototactic responses to full-spectrum and wavelength-restricted stimuli at a range of intensities, though the levels of stimulus acceptance and attraction, respectively, changed according to intensity. The species is most attracted to white, blue and black (ultraviolet) wavelength-restricted stimuli in the laboratory and field. In the field, traps baited with blue light sources were less attractive to non-target insect species, but white light sources were more attractive to H. halys indicating that these two light sources may be good candidates for inclusion in light-based monitoring traps.

Behavioural response of the invasive Halyomorpha halys (Hemiptera: Pentatomidae) to host plant stimuli augmented with semiochemicals in the field

Although much work has focused on understanding how the invasive brown marmorated stink bug, or Halyomorpha halys, responds to pheromonal stimuli, very little research has explored the response of H. halys to plant volatiles and other host stimuli. The present study aimed to determine (i) whether more acceptable, less acceptable or unacceptable host plants augmented with plant volatile mixes and/or pheromone can enhance the retention capacity of plants for H. halys in the field and (ii) whether plant volatiles [apple, peach or green leaf volatile (GLV) mixtures] can increase attraction to pheromone‐baited pyramid traps. The presence of the H. halys pheromone was the primary factor in increasing the retention capacity of tagged, released adults to host plants, although plant volatile mixtures added a small increase in retention. Plant species helped to modulate the effectiveness of both the pheromone and additional plant volatiles in retaining individuals. Plant volatiles did not increase attraction of adults to baited pyramid traps and may have inhibited the attraction of nymphs. Overall, the results of the present study suggest that host plant stimuli, construed broadly, are important for the foraging decisions of H. halys, although further research is needed to identify the most effective stimuli.

Behavioral Response of the Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) to Semiochemicals Deployed Inside and Outside Anthropogenic Structures During the Overwintering Period

The brown marmorated stink bug, Halyomorpha halys (Stål), is an invasive species from Asia capable of causing severe agricultural damage. It can also be a nuisance pest when it enters and exits anthropogenic overwintering sites. In recent years, pheromone lures and traps for H. halys have been developed and used to monitor populations in field studies. To date, no study has investigated the applicability of these monitoring tools for use indoors by building residents during the overwintering period. Herein, we 1) assessed when in late winter (diapause) and spring (postdiapause) H. halys begins to respond to its pheromone (10,11-epoxy-1-bisabolen-3-ol), 2) evaluated whether pheromone-based tools can be used reliably for monitoring H. halys adults in unheated and heated buildings, and 3) elucidated the potential for indoor management using pheromone-baited traps. A 2-yr trapping study suggested that H. halys began to respond reliably to pheromone-baited traps after a critical photoperiod of 13.5 h in the spring. Captures before that point were not correlated with visual counts of bugs in buildings despite robust populations, suggesting currently available pheromone-baited traps were ineffective for surveillance of diapausing H. halys. Finally, because baited traps captured only 8-20% of the adult H. halys known to be present per location, they were not an effective indoor management tool for overwintering H. halys. Our study contributes important knowledge about the capacity of H. halys to perceive its pheromone during overwintering, and the ramifications thereof for building residents with nuisance problems.