Tracy C. Leskey

Biology, Ecology, and Management of Brown Marmorated Stink Bug (Hemiptera: Pentatomidae)

Brown marmorated stink bug, Halyomorpha halys Stal, is an invasive, herbivorous insect species that was accidentally introduced to the United States from Asia. First discovered in Allentown, PA, in 1996, H. halys has now been reported from at least 40 states in the United States. Additional invasions have been detected in Canada, Switzerland, France, Germany, Italy, and Lichtenstein, suggesting this invasive species could emerge as a cosmopolitan pest species. In its native range, H. halys is classified as an outbreak pest; however, in North America, H. halys has become a major agricultural pest across a wide range of commodities. H. halys is a generalist herbivore, capable of consuming >100 different species of host plants, often resulting in substantial economic damage; its feeding damage resulted in US

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

37 million of losses in apple in 2010, but this stink bug species also attacks other fruit, vegetable, field crop, and ornamental plant species. H. halys has disrupted integrated pest management programs for multiple cropping systems. Pesticide applications, including broad-spectrum insecticides, have increased in response to H. halys infestations, potentially negatively influencing populations of beneficial arthropods and increasing secondary pest outbreaks. H. halys is also challenging because it affects homeowners as a nuisance pest; the bug tends to overwinter in homes and outbuildings. Although more research is required to better understand the ecology and biology of H. halys , we present its life history, host plant damage, and the management options available for this invasive pest species.

Impact of the Invasive Brown Marmorated Stink Bug, Halyomorpha halys (Stål), in Mid-Atlantic Tree Fruit Orchards in the United States: Case Studies of Commercial Management

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.

Discovery of the Aggregation Pheromone of the Brown Marmorated Stink Bug (Halyomorpha halys) through the Creation of Stereoisomeric Libraries of 1‑Bisabolen-3-ols

Four commercial orchards in the mid-Atlantic region of the United States were surveyed weekly in 2010 and 2011 for the presence of brown marmorated stink bug and the injury caused to both apple and peaches. Among tested sampling techniques, pyramid traps baited with the aggregation pheromone of Plautia stali Scott, methyl-(2E,4E,6Z)-decatrienoate, yielded the most brown marmorated stink bug adults and nymphs, followed by visual observations. Brown marmorated stink bugs began to feed on apples and peaches soon after fruit set and continued to feed on fruit throughout the growing season. Injury to apple was relatively inconsequential until after mid-June, whereas feeding on peaches resulted in immediate economic injury as the surface became distorted, dented, discolored, and the flesh beneath turned brown. Significantly more apples were injured and with greater severity in 2010 than in 2011. Likewise, percent injury on the exterior portion of each apple plot was significantly greater than injury reported from the interior in both years. Growers increased the number of insecticide applications nearly 4-fold from 2010 to 2011. In addition to the increased number of targeted insecticide applications, growers also reduced the interval between treatments in 2011. A metric was created to compare the relative intensity of each growers commercial management program between seasons and amongst each other.

Impact of Insecticides on the Invasive Halyomorpha halys (Hemiptera: Pentatomidae): Analysis of Insecticide Lethality

We describe a novel and straightforward route to all stereoisomers of 1,10-bisaboladien-3-ol and 10,11-epoxy-1-bisabolen-3-ol via the rhodium-catalyzed asymmetric addition of trimethylaluminum to diastereomeric mixtures of cyclohex-2-enones 1 and 2. The detailed stereoisomeric structures of many natural sesquiterpenes with the bisabolane skeleton were previously unknown because of the absence of stereoselective syntheses of individual stereoisomers. Several of the bisabolenols are pheromones of economically important pentatomid bug species. Single-crystal X-ray crystallography of underivatized triol 13 provided unequivocal proof of the relative and absolute configurations. Two of the epoxides, (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (3) and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (4), were identified as the main components of a male-produced aggregation pheromone of the brown marmorated stink bug, Halyomorpha halys, using GC analyses on enantioselective columns. Both compounds attracted female, male, and nymphal H. halys in field trials. Moreover, mixtures of stereoisomers containing epoxides 3 and 4 were also attractive to H. halys, signifying that the presence of additional stereoisomers did not hinder attraction of H. halys and relatively inexpensive mixtures can be used in monitoring, as well as control strategies. H. halys is a polyphagous invasive species in the U.S. and Europe that causes severe injury to fruit, vegetables, and field crops and is also a serious nuisance pest.

Development of Behaviorally-Based Monitoring Tools for the Brown Marmorated Stink Bug (Heteroptera: Pentatomidae) in Commercial Tree Fruit Orchards

ABSTRACT The efficacy of 37 insecticide treatments against adult Halyomorpha halys (Stål) was established based on exposure to 18-h old dry insecticide residue in laboratory bioassays. Individual adult H. halys were exposed to an insecticide residue for 4.5 h and then monitored daily for survivorship over a 7-d period. The proportion of dead and moribund insects was used as an estimate of overall insecticide efficacy against H. halys immediately after the exposure period and over the 7-d trial. Among all materials evaluated, 14 insecticides exhibited increasing efficacy, in which the percentage of dead and moribund insects (used as a measure of insecticide efficacy) increased by >10% after 7 d. By contrast, insecticide efficacy values of eight insecticides declined by >10% (based on recovery of adults from a moribund state) over the 7-d period with most belonging to the pyrethroid class. In this study, the efficacy value of neonicotinoid, acetamiprid, showed the greatest decline from 93 to 10% over 7 d. A lethality index (scale of 0–100) was developed to compare insecticides based on quantifying the immediate and longer-term effects of insecticide exposure on H. halys. Among all materials evaluated, dimethoate, malathion, bifenthrin, methidathion, endosulfan, methomyl, chlorpyrifos, acephate, fenpropathrin, and permethrin yielded the highest values (>75) because of a high degree of immediate mortality with very little recovery. Our results provide baseline information regarding potential of candidate insecticides against adult H. halys and highlight the need to consider longer-term effects in establishing overall efficacy ratings against this invasive species.

Synergy of Aggregation Pheromone with Methyl (E,E,Z)-2,4,6-Decatrienoate in Attraction of Halyomorpha halys (Hemiptera: Pentatomidae)

Abstract Captures of the invasive brown marmorated stink bug, Halyomorpha halys (Stål), were significantly greater in pyramid traps baited with the known attractant, methyl (2E,4E,6Z)- decatrienoate, compared with unbaited traps. A dose-dependent response by adults to lures formulated with increasing amounts of methyl (2E,4E,6Z)-decatrienoate and deployed in association with black pyramid traps also was observed. Among pyramid traps representing different visual stimuli including black, green, yellow, clear, white and yellow, significantly greater captures were recorded in baited black pyramid traps for adults in 2009 and nymphs in 2010 compared with other trap types; the dark upright silhouette created by this trap likely represents a trunk-mimicking visual stimulus to foraging bugs. A ground-deployed baited black pyramid trap also captured significantly greater numbers of nymphs and adults compared with canopy-deployed commercially available baited traps from Japan. Based on semi-field cage studies, brown marmorated stink bug was confirmed to be bivoltine within the mid-Atlantic region. Thus, the need for a reliable monitoring tool to detect presence, abundance and seasonal activity of brown marmorated stink bug in tree fruit and other cropping systems is critical.

Monitoring Plum Curculio, Conotrachelus nenuphar (Coleoptera: Curculionidae), Populations in Apple and Peach Orchards in the Mid-Atlantic

ABSTRACT The reported male-produced aggregation pheromone of the brown marmorated stink bug, Halyomorpha halys (Stål) (Hemiptera: Pentatomidae), identified as a mixture of (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol, offers new opportunities for its management. We found that black pyramid traps deployed along crop borders in Maryland and West Virginia, containing lures with both stereoisomers of this reported aggregation pheromone combined with methyl (E,E,Z)-2,4,6-decatrienoate (MDT) lures, attracted more adult and nymphal H. halys than either the aggregation pheromone or MDT alone. In season-long totals, combined lures acted synergistically by catching 1.9–3.2 times more number of adults, and 1.4–2.5 times more number of nymphs, than expected from an additive effect of the lures deployed individually. There were no significant differences in patterns of male and female captures. MDT alone was not significantly attractive to adults during most of the growing season, but became increasingly attractive to adults and especially nymphs in autumn. Mixed-isomer lures containing eight stereoisomers of 10,11-epoxy-1-bisabolen-3-ol, including the two active stereoisomers, were as effective at catching adults and nymphs with or without MDT as were lures loaded only with the two active stereoisomers in the natural ratio ((3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol: (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol) of 3.5:1. These results identify a combination of semiochemicals that is attractive season-long for detection, monitoring, and potential control of this polyphagous invasive pest of North America and Europe.

Efficacy of insecticide residues on adult Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) mortality and injury in apple and peach orchards.

We evaluated responses of plum curculio, Conotrachelus nenuphar (Herbst), to four trap types in commercial and unsprayed apple and peach orchards. Trap types included black pyramid and clear Plexiglas panel traps deployed outside the orchard 2 m from the border row, and branch-mimicking cylinder and trunk-mounted screen traps attached to trees in the border row. Bait treatments evaluated in conjunction with each trap type included the synthetic fruit volatile benzaldehyde, the aggregation pheromone grandisoic acid (GA), benzaldehyde in combination with GA, and an unbaited control treatment. In commercial apple orchards, significantly more plum curculio were captured in traps baited with benzaldehyde + GA compared with traps baited with other treatments. Furthermore, significantly more plum curculio were captured by screen traps baited with benzaldehyde + GA compared with unbaited control traps. Significantly more plum curculio were captured by screen traps compared with other trap types in an unsprayed apple orchard. Very few captures were recorded in commercial peach orchards. Dissections of trapped females indicate that bivoltine populations are present in the mid-Atlantic. In general, correlations between timing and amount of trap captures and timing and amount of fruit injury inflicted concurrently or 1 wk after trap captures were very weak for all trap types and bait combinations. Our results agree with previous studies in the northeastern United States in which trap captures are increased by presence of semiochemical baits but fail to serve as reliable tools to determine need for and timing of insecticide application against plum curculio.

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

BACKGROUND The primary threat from Halyomorpha halys (Stål) (Hemiptera: Pentatomidae) originates from populations continuously dispersing from and among wild and cultivated hosts, so many individuals may not be directly sprayed with insecticides. Limited information exists regarding field-based residual activity of insecticides for management of H. halys in tree fruit. Thus, we conducted field-based bioassays in apple and peach orchards to evaluate residual activity of insecticides commonly applied against H. halys. Adults used in these trials were collected from wild and cultivated hosts less than one week prior to testing to more accurately reflect the susceptibility of wild H. halys populations in the field throughout the season. RESULTS Significantly higher mortality rates of Halyomorpha halys were observed early in the growing season, when overwintered adults were prevalent, compared with populations present later in the growing season that included new generation adults. Significantly higher mortality was recorded for adults exposed to fresh insecticide applications compared with three- and seven-day old residues. Typically, the addition of an adjuvant did not enhance efficacy or residual activity of insecticides. Significantly fewer injury sites were recorded on apples treated with dinotefuran and fenpropathrin compared with the untreated apples for all residue ages. CONCLUSIONS Overwintered Halyomorpha halys populations are easier to kill with insecticide applications than the first and second generation which are present in the field during the mid- to late-season. Residual activity of nearly all insecticides decreased significantly three days after application and adjuvants generally did not increase residual activity. These factors should be considered in developing season-long programs for management of this invasive species in tree fruit.