Shimat V. Joseph

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.

Thrips Vectors of Tospoviruses

Tospoviruses belong to the sole phytovirus genus, Tospovirus , in the family Bunyaviridae . Tospoviruses are known to be exclusively transmitted by thrips belonging to the family Thripidae and subfamily Thripinae. Of the known 1,710 species of Thripidae only 14 thrips species are currently reported to transmit tospoviruses. Thrips-transmitted tospoviruses cause severe yield losses to several economically important crops in the United States and worldwide. For instance, a single Tospovirus ( Tomato spotted wilt virus ) alone caused an estimated

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

1.4 billion in losses in the U.S. over 10 years. Global trade and associated movement of plant materials across borders have introduced tospoviruses and their vectors into newer areas. Advances in serological and molecular techniques have also led to identification of new tospoviruses. This scenario has also initiated new vector-pathogen interactions between introduced and native thrips species and tospoviruses. The goal of this manuscript is to provide a comprehensive and updated list of thrips species that serve as vectors of tospoviruses along with information pertaining to common names, key diagnostic characters, distribution, important crops economically affected, and thrips and Tospovirus -induced symptoms. The manuscript is prepared with special emphasis to the U.S., but information pertaining to other countries is also included.

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

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.

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

Influence of Plant Parameters on Occurrence and Abundance of Arthropods in Residential Turfgrass

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.

Effects of Fertilizer and Low Rates of Imidacloprid on Adelges tsugae (Hemiptera: Adelgidae)

ABSTRACT The effect of taxa [common Bermuda grass, Cynodon dactylon (L.); centipedegrass, Eremochloa ophiuroides Munro Hack; St. Augustinegrass, Stenotaphrum secundatum [Walt.] Kuntze; and zoysiagrass, Zoysia spp.], density, height, and weed density on abundance of natural enemies, and their potential prey were evaluated in residential turf. Total predatory Heteroptera were most abundant in St. Augustinegrass and zoysiagrass and included Anthocoridae, Lasiochilidae, Geocoridae, and Miridae. Anthocoridae and Lasiochilidae were most common in St. Augustinegrass, and their abundance correlated positively with species of Blissidae and Delphacidae. Chinch bugs were present in all turf taxa, but were 23–47 times more abundant in St. Augustinegrass. Anthocorids/lasiochilids were more numerous on taller grasses, as were Blissidae, Delphacidae, Cicadellidae, and Cercopidae. Geocoridae and Miridae were most common in zoysiagrass and were collected in higher numbers with increasing weed density. However, no predatory Heteroptera were affected by grass density. Other beneficial insects such as staphylinids and parasitic Hymenoptera were captured most often in St. Augustinegrass and zoysiagrass. These differences in abundance could be in response to primary or alternate prey, or reflect the influence of turf microenvironmental characteristics. In this study, Simpsons diversity index for predatory Heteroptera showed the greatest diversity and evenness in centipedegrass, whereas the herbivores and detritivores were most diverse in St. Augustinegrass lawns. These results demonstrate the complex role of plant taxa in structuring arthropod communities in turf. An increased understanding of how turf species and cultivars help shape pest and beneficial arthropod communities will enhance predictive abilities and further pest management objectives.

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 Healthy hemlock trees, Tsuga canadensis (L.) Carrière, and hemlock woolly adelgid, Adelges tsugae Annand (Hemiptera: Adelgidae), populations should favor retention and population growth of adelgid predators such as Laricobius nigrinus Fender (Coleoptera: Derodontidae) and Sasajiscymnus tsugae (Sasaji & McClure) (Coleoptera: Coccinellidae). Eastern hemlock trees between 15 and 38 cm diameter at breast height (dbh) were treated with 0, 10, or 25% of 1.5 g imidacloprid (Merit 75 WP) per 2.5 cm dbh and were either fertilized or not, in a 3 by 2 factorial design. After 2 yr, imidacloprid reduced the numbers of ovisacs and eggs found on trees in a dosage-dependent manner, while enhancing tree growth parameters such as new shoots or needles and the length of new shoots. Fertilized trees had greater adelgid fecundity, which was positively correlated with total foliar N in both winter generations. In February 2009 (27 mo after imidacloprid treatment), higher imidacloprid dosages to unfertilized trees resulted in reduced adelgid fecundity. Concentrations of N, P, and K were higher in the foliage of trees treated with insecticide, whereas foliar aluminum concentrations were consistently lower in trees with higher insecticide dosages. Trees treated with low rates of imidacloprid were healthier than untreated trees, but only trees treated with the 0.1 × dosage had sufficient adelgids to possibly sustain predators over extended periods.

Predatory Potential of Geocoris spp. and Orius insidiosus on Fall Armyworm in Resistant and Susceptible Turf

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.

Evidence of Protaphorura fimata (Collembola: Poduromorpha: Onychiuridae) feeding on germinating lettuce in the Salinas Valley of California

ABSTRACT Predatory potential and performance of the predaceous heteropterans, Geocoris punctipes (Say), G. uliginosus (Say) (Geocoridae), and Onus insidiosus (Say) (Anthocoridae), were evaluated using fall army worm, Spodoptera frugiperda (J. E. Smith), as prey on different turfgrass taxa (resistant zoysiagrasses, ‘Cavalier’ and ‘Palisades’; moderately resistant Bermuda grass, ‘TifSport’; and susceptible seashore paspalum, ‘Sea Isle 1’) through laboratory and field studies. When background mortality was taken into account, in small arena trials in the laboratory, the greatest mortality by predators occurred on TifSport. The predator impact on TifSport by O. insidiosus was 92.6% above the mortality in the no-predator treatment on that grass. Predator induced mortality was rarely significant on the highly resistant zoysiagrass cultivar Cavalier because mortality, even in the absence of predators, was so high. Survival of larvae on TifSport Bermuda grass was significantly reduced by the addition of just two O. insidiosus per pot in laboratory pot trials. An increase in predator density to 4, 6, 8, or 10 further suppressed larval survival. O. insidiosus reduced larval survival on Sea Isle 1 at all densities. On Sea Isle 1, a density of two O. insidiosus resulted in >50% reduction in live fall armyworms compared with the no predator treatment in laboratory trials. However, addition of O. insidiosus did not significantly reduce survival of fall armyworm larvae on this cultivar in the field in the presence of alternative prey and predators. O. insidiosus densities of six or higher per 181.4 cm2 did significantly reduce larval survival on TifSport Bermuda grass by as much as 80% during a 5-d trial period in the field. Predator-induced mortality among all trials was most consistent on a grass of intermediate resistance, TifSport Bermuda grass.