J. Christopher Bergh

Review of the Biology, Ecology, and Management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea

ABSTRACT Native to China, Japan, Korea, and Taiwan, the brown marmorated stink bug, Halyomorpha halys (Sål) (Hemiptera: Pentatomidae) was first detected in the United States in the mid-1990s. Since establishing in the United States, this invasive species has caused significant economic losses in agriculture and created major nuisance problems for home and business owners, especially in the mid-Atlantic region. Basic and applied questions on H. halys have been addressed in its native range in Asia since the mid-1900s and the research outcomes have been published in at least 216 articles from China, Japan, and the Republic of Korea. In Asia, H. halys is described as an occasional or outbreak pest of a number of crops such as apple, pear, persimmon, and soybeans. This species is considered a nuisance pest as well, particularly in Japan. This review summarizes 100 articles primarily translated from Chinese, Japanese, and Korean to English. The content of this review focuses on the biology, ecology, and management of H. halys in Asia, with specific emphasis on nomenclature, life history, host range, damage, economic importance, sampling and monitoring tools, and management strategies. This information from the native range of H. halys provides greater context and understanding of its biology, ecology, and management in North America.

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 Pheromone-Based Management Strategies for Dogwood Borer (Lepidoptera: Sesiidae) in Commercial Apple Orchards

ABSTRACT The dogwood borer, Synanthedon scitula (Harris) (Lepidoptera: Sesiidae), is a serious wood-boring pest of apple in eastern North America. The recent identification of its sex pheromone and systematic documentation of the effect of a potent behavioral antagonist affords the opportunity to develop pheromone-based management strategies for this important pest. Here we evaluated the potential of pheromone-based mass trapping of males to reduce dogwood borer infestations and conducted preliminary evaluations of an antagonist-based pheromone blend for disruption of dogwood borer mate finding in commercial apple orchards in North Carolina, Virginia, and West Virginia. In the mass trapping study, treatments included a conventional trunk-drench application of chlorpyrifos, a low-density mass trapping regime of 5 traps/ha, a higher-density mass trapping regime of 20 traps/ha, and an untreated control. We removed large numbers of males from orchards at all locations, with 27,155, 8,418, and 7,281 removed from high-density trapping plots in North Carolina, Virginia, and West Virginia, respectively, over 2 yr. After 2 yr under each of these treatment regimes, infestation in high- and low-density mass trapping plots was not reduced to the level of chlorpyrifos-treated plots. An antagonist-based dispenser deployed at a rate of 250/ha effectively disrupted mate-finding by male dogwood borer. In plots with mating disruption dispensers, captures in pheromone-baited traps were virtually eliminated, and no males were captured in traps baited with virgin females.

Host Plant Effects on Halyomorpha halys (Hemiptera: Pentatomidae) Nymphal Development and Survivorship

Abstract Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) is a highly polyphagous invasive species and an important pest of orchard crops in the United States. In the Mid-Atlantic region, wild hosts of H. halys are common in woodlands that often border orchards, and H. halys movement from them into orchards poses ongoing management issues. To improve our understanding of host plant effects on H. halys populations at the orchard–woodland interface, nymphal survivorship, developmental duration, and adult fitness (size and fresh weight) on apple (Malus domestica Borkh.), peach (Prunus persica (L.) Batsch), Tree of Heaven (Ailanthus altissima (Mill.) Swingle), and northern catalpa (Catalpa speciosa (Warder)) were examined in laboratory studies. Specifically, we investigated nymphal performance on the foliage and fruiting structures of those hosts and on single- versus mixed-host diets, as well as the effects of host phenology on their suitability. Nymphal performance was poor on a diet of foliage alone, regardless of host. When fruiting structures were combined with foliage, peach was highly suitable for nymphal development and survivorship, whereas apple, Tree of Heaven, and catalpa were less so, although nymphal survival on Tree of Heaven was much greater later in the season than earlier. Mixed-host diets yielded increased nymphal survivorship and decreased developmental duration compared with diets of suboptimal single hosts. Adult size and weight were generally greater when they developed from nymphs reared on mixed diets. The implications of our results to the dispersal behavior, establishment, and management of H. halys are discussed.

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.

Spatial Distribution of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) Injury at Harvest in Mid-Atlantic Apple Orchards

ABSTRACT Brown marmorated stink bug, Halyomorpha halys (Stål), injury to late-season apple cultivars was measured at harvest in 2011 and 2012 in commercial orchards in four mid-Atlantic states. In each orchard block, a border zone (adjacent to woods), an interior zone (near orchard center), and an intermediate zone (between border and interior zones) comprised 1–3 tree rows per zone, depending on block size. Just before commercial harvest, 10 fruit were sampled from the upper, middle, and lower third of the canopy from five trees in each zone. After 3–5 wk in cold storage, fruit were examined for external and internal injury, and severity of internal injury (number of injury sites per fruit) from H. halys. A zero-inflated negative binomial model accounted for significant variation among the orchards and showed that apples from the upper canopy of border zone trees had the highest probability of experiencing external and internal injury. A minor interaction was detected among the orchards and zones for injury prevalence and severity, but there was no evidence of an orchard showing less expected injury in the border zone compared with other zones. Adjusting for orchard-to-orchard variation, differences in injury distributions among the zones and canopies were primarily due to injury prevalence rather than expected injury severity. The implications of these results to scouting and managing H. halys in eastern apple orchards are discussed.

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.

Factors Affecting Captures of Brown Marmorated Stink Bug, Halyomorpha halys (Hemiptera: Pentatomidae), in Baited Pyramid Traps

Abstract Trapping experiments targeting brown marmorated stink bug, Halyomorpha halys (Stål), addressed the effects of: (1) a modification to the trap container of a commercial trap, (2) the age of methyl (2E,4E,6Z)-decatrienoate lures, and (3) the age of dichlorvos-impregnated kill strips on bug captures. In the trap modification study, ventilation holes in the containers atop standard, commercial AgBio™ traps were modified to resemble a USDA prototype trap. Captures were compared among the standard traps, modified commercial traps, and prototype traps. Halyomorpha halys captures were significantly greater in the prototype trap than in standard commercial traps, whereas captures in modified commercial traps were intermediate between but not significantly different from AgBio or prototype traps. Traps baited with kill strips that were fresh or that had been field-aged for 1, 2, 3 or 4 wk showed no significant differences in the total number of H. halys captured over a 15-d trapping interval, although the percentage of dead bugs was significantly greater in traps containing fresh kill strips than in those with 3- or 4-wk-old kill strips. In the aged lure experiment, captures were not significantly different among traps baited with fresh, 1- and 2-wk-old lures or among those baited with 2-, 3- or 4-wk old lures or unbaited. Most (64.8%) bugs were captured during the first 3-d sample interval, during which traps with fresh lures captured more H. halys than those with each aged lure treatment. Weekly gravimetric measurements to determine the release of methyl (2E,4E,6Z)-decatrienoate from lures over 4 wk showed a sharp decrease in lure weight during the first 3-d interval at 20 and 25°C.

Comparison of Sex Pheromone Traps for Monitoring Pink Hibiscus Mealybug (Hemiptera: Pseudococcidae)

Abstract The pink hibiscus mealybug, Maconellicoccus hirsutus (Green) (Hemiptera: Pseudococcidae), is a highly polyphagous pest that invaded Florida in 2002 and has recently been reported from several locations in Louisiana. Although identification of its sex pheromone in 2004 improved monitoring capabilities tremendously, the effectiveness and efficiency of different pheromone trap designs for capturing males has not been evaluated. We deployed green Delta, Pherocon IIB, Pherocon V, Jackson, and Storgard Thinline traps in Homestead, FL, and compared the number of male M. hirsutus captured per trap, the number captured per unit of trapping surface area, the amount of extraneous material captured, and the time taken to count trapped mealybugs. Pheromone-baited traps with larger trapping surfaces (green Delta, Pherocon IIB, and Pherocon V) captured more males per trap than those with smaller surfaces (Jackson and Storgard Thinline), and fewest males were captured by Storgard Thinline traps. However, Jackson traps captured as many or more males per square centimeter of trapping surface as those with larger surfaces, and the time required to count males in Jackson traps was significantly less than in green Delta, Pherocon IIB, and Pherocon V traps. Although all trap designs accumulated some debris and nontarget insects, it was rated as light to moderate for all designs. Based on our measures of effectiveness and efficiency, the Jackson trap is most suitable for monitoring M. hirsutus populations. Additionally, unlike the other traps evaluated, which must be replaced entirely or inspected in the field and then redeployed, only the sticky liners of Jackson traps require replacement, enhancing the efficiency of trap servicing.

Temporal Effects on the Incidence and Severity of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae) Feeding Injury to Peaches and Apples during the Fruiting Period in Virginia.

ABSTRACT Exclusion cages were used to compare the incidence and severity of feeding injury from brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), on ‘Redhaven’ peaches, ‘Golden Delicious’ apples, and ‘Smoothee Golden’ apples at harvest, following sequential periods of exposure to natural H. halys populations during the 2011 and 2012 growing seasons in Virginia. The fruit used in these experiments were in orchards or on trees that were not managed for H. halys. Treatments were sets of 50 fruit that were always caged, never caged, or exposed during one interval during the fruiting period of peaches and apples in the Mid-Atlantic region of the United States. The cages effectively prevented feeding injury from H. halys. Peaches and apples that were never caged showed the highest percentages of injured fruit at harvest. Exposure treatment had a significant effect on the percentage of fruit showing external injury at harvest in both years for apples and in 2012 for peaches, and a significant effect on the percentage of apples and peaches showing internal injury at harvest in both years. There was no consistent effect of each exposure period on peach injury, but apples exposed during the mid- to latter portion of the season tended to show most injury. Across all exposure periods, more internal than external injuries were recorded at harvest from peaches, while apples tended to have equal or very similar numbers of both kinds of injury. The implications of these results to H. halys management in eastern apple orchards are discussed.