Halyomorpha halys (brown marmorated stink bug)

Pictures

Picture	Title	Caption	Copyright
Title Adult feeding Caption Brown marmorated stink bug (Halyomorpha halys); adult feeding on a cherry. Copyright ©CABI Switzerland - 2012	Adult feeding	Brown marmorated stink bug (Halyomorpha halys); adult feeding on a cherry.	©CABI Switzerland - 2012
Title Adults feeding Caption Adult brown marmorated stink bugs (Halyomorpha halys) feeding on cherries Copyright ©CABI Switzerland - 2012	Adults feeding	Adult brown marmorated stink bugs (Halyomorpha halys) feeding on cherries	©CABI Switzerland - 2012
Title Egg mass Caption Egg mass of brown marmorated stink bug (Halyomorpha halys) Copyright ©CABI Switzerland - 2012	Egg mass	Egg mass of brown marmorated stink bug (Halyomorpha halys)	©CABI Switzerland - 2012
Title Newly emerged nymphs Caption Brown marmorated stink bug (Halyomorpha halys); newly emerged nymphs around egg mass. Copyright ©CABI Switzerland - 2012	Newly emerged nymphs	Brown marmorated stink bug (Halyomorpha halys); newly emerged nymphs around egg mass.	©CABI Switzerland - 2012
Title Various nymphal instars Caption Various nymphal instars of the brown marmorated stink bug (Halyomorpha halys). Copyright ©CABI Switzerland - 2012	Various nymphal instars	Various nymphal instars of the brown marmorated stink bug (Halyomorpha halys).	©CABI Switzerland - 2012
Title Natural enemy Caption Natural enemy; parasitoid wasps (Trissolcus halyomorphae) parasitizing eggs of brown marmorated stink bug (Halyomorpha halys). Copyright ©CABI Switzerland - 2012	Natural enemy	Natural enemy; parasitoid wasps (Trissolcus halyomorphae) parasitizing eggs of brown marmorated stink bug (Halyomorpha halys).	©CABI Switzerland - 2012

Identity

Preferred Scientific Name

• Halyomorpha halys (Stål)

Preferred Common Name

• brown marmorated stink bug

Other Scientific Names

• Halyomorpha brevis
• Halyomorpha mista
• Halyomorpha remota
• Pentatoma halys Stål

International Common Names

• English: yellow-brown marmorated stink bug; yellow-brown stink bug
• French: punaise diabolique

Local Common Names

• Germany: Marmorierte Baumwanze

English acronym

• BMSB

EPPO code

• HALYHA (Halyomorpha halys)

Summary of Invasiveness

Following the accidental introduction and initial discovery of H. halys in Allentown, Pennsylvania, USA, this species has been detected in 41 states and the District of Columbia in the USA. Isolated populations also exist in Switzerland, France, Italy and Canada. Recent detections also have been reported in Germany and Liechtenstein. BMSB has become a major nuisance pest in the mid-Atlantic region and Pacific Northwest, USA, due to its overwintering behaviour of entering human-made structures in large numbers. BMSB also feeds on numerous tree fruits, vegetables, field crops, ornamental plants, and native vegetation in its native and invaded ranges. In the mid-Atlantic region, serious crop losses have been reported for apples, peaches, sweetcorn, peppers, tomatoes and row crops such as field maize and soyabeans since 2010. Crop damage has also been detected in other states recently including Oregon, Ohio, New York, North Carolina and Tennessee.

Taxonomic Tree

• Domain: Eukaryota
•     Kingdom: Metazoa
•         Phylum: Arthropoda
•             Subphylum: Uniramia
•                 Class: Insecta
•                     Order: Hemiptera
•                         Suborder: Heteroptera
•                             Family: Pentatomidae
•                                 Genus: Halyomorpha
•                                     Species: Halyomorpha halys

Notes on Taxonomy and Nomenclature

Considerable confusion regarding the systematics of Halyomorpha halys has existed since its original description as Pentatoma halys by Stål in 1855 (Rider, 2005). Distant (1880, 1893, 1899) considered H. halys as a junior synonym of H. picus (Fabricius). Since then H. halys was determined to be distinct from H. picus and has been referred to as H. mista, H. brevis, and H. remota (Rider et al., 2002; Rider, 2005). Josifov and Kerzhner (1978) determined that only one species of Halyomorpha, H. halys, is present in eastern China, Japan and Korea and all references to Halyomorpha spp. from these locations are considered synonymous with H. halys (Rider et al., 2002). Common names in Asia include the yellow-brown stink bug and the brown marmorated stink bug, but the latter is the recognized common name in the USA or abbreviated as BMSB.

Description

Although somewhat variable in size and coloration, adult specimens of H. halys range from 12 to 17 mm in length, and in humeral width of 7 to 10 mm. The common name brown marmorated stink bug is a reference to its generally brownish and marbled or mottled dorsal coloration, with dense punctation. Detailed redescriptions and diagnoses of adults are provided by Hoebeke and Carter (2003) and Wyniger and Kment (2010). Eggs are smooth and pale in colour, approximately 1.3 mm in diameter by 1.6 mm in length, and are laid in clusters of 20-30. The brightly coloured, black and reddish-orange first instars remain clustered about the egg mass after hatching and move away once moulting to second instars has occurred. There are five nymphal instars, which are described in Hoebeke and Carter (2003) with a key and illustrated with colour photos.

Distribution

The brown marmorated stink bug, H. halys, is native to China, Japan, Korea and Taiwan (Hoebeke and Carter 2003; Lee et al., 2013a). The first USA populations were discovered in the mid-1990s in or near Allentown, Pennsylvania. In 2001, Karen Bernhardt with Penn State Cooperative Extension recognized that the insect invading homes was probably not native and sent a specimen to Richard Hoebeke at Cornell University who identified it as H. halys (Hoebeke and Carter, 2003). As of 2013, H. halys has been detected in 41 states and the District of Columbia in the USA though Colorado is still considered an unofficial find. In Delaware, Maryland, New Jersey, Pennsylvania, Virginia and West Virginia, H. halys has become a severe agricultural and nuisance pest, is considered an agricultural/nuisance pest in New York, North Carolina, Ohio and Tennessee, and a nuisance only pest in 10 additional states (Leskey and Hamilton, 2012).

Detections also have been reported in Hamilton, Ontario, Canada (Fogain and Graff, 2011), Switzerland (Wermelinger et al., 2008), Liechtenstein (Arnold, 2009), Germany (Heckmann, 2012), Italy (Pansa et al., 2013), France (Callot and Brua, 2013) and Hungary (Vétek et al., 2014).

Ecological niche modelling indicates that the area of invasion suitable for H. halys is quite extensive worldwide. H. halys could become established in northern Europe, north-eastern North America, portions of southern Australia and much of New Zealand, areas of South America (Uruguay, southern Brazil and northern Argentina) and parts of Africa (northern Angola and adjacent areas of Congo and Zambia) (Zhu et al., 2012).

Distribution Table

The distribution in this summary table is based on all the information available. When several references are cited, they may give conflicting information on the status. Further details may be available for individual references in the Distribution Table Details section which can be selected by going to Generate Report.

History of Introduction and Spread

H. halys is native to China, Japan, Korea and Taiwan (Hoebeke and Carter 2003; Lee et al., 2013a). The first USA populations were discovered in the mid-1990s in or near Allentown, Pennsylvania. In 2001, Karen Bernhard with Penn State Cooperative Extension recognized that the insect invading homes was probably not native and sent a specimen to Richard Hoebeke at Cornell University who identified it as H. halys (Hoebeke and Carter, 2003). As of 2013, H. halys has been detected in 41 states and the District of Columbia in the USA, though Colorado is still considered an unofficial find. H. halys has become a severe agricultural and nuisance pest in Delaware, Maryland, New Jersey, Pennsylvania, Virginia and West Virginia, is considered an agricultural/nuisance pest in New York, North Carolina, Ohio and Tennessee, and a nuisance only pest in 10 additional states (Leskey and Hamilton 2012). Genetic studies of mitochondrial cytochrome c oxidase (CO) subunit II gene, COI and 12S ribosomal RNA gene have revealed that H. halys populations in the USA originated from a single introduction from the region of Beijing, China (Xu et al., 2013). 

In Canada, interceptions of H. halys at various ports of entry across the country began in 1993 from countries including China, Japan, Korea and the USA, with reports of homeowner finds beginning in the Province of Ontario as of 2010 (Fogain and Graff, 2011) and established breeding populations in the field confirmed as of July 2012 (Fraser and Gariepy, unpublished). On the basis of molecular data and interception records it appears likely that H. halys in Canada is derived from the movement of established US populations (Gariepy et al., 2013).

In Europe BMSB was first officially reported from the canton of Zurich in Switzerland in 2007 (Wermelinger et al., 2008). However, later investigations showed that it was already present in Zurich in 2004 (Gariepy et al., 2013). In the same year, a single individual was found near Balzers in Liechtenstein, which probably originated from nearby founder populations in Zurich (Arnold, 2009). In Switzerland three haplotypes were found, which were not identical with haploytypes found in North America. The dominant haplotype in Switzerland was consistent with Asian samples collected in the Hebei and Beijing provinces; however, it was not the dominant haplotype in these regions. The remaining two haplotypes were unique to Switzerland and their origin in Asia remains unknown (Gariepy et al., 2013). Outside Switzerland, a single individual was found near Konstanz in southern Germany (Heckmann, 2012) and most recently breeding populations established in the Alsace region of France (Callot and Brua, 2013) and northern Italy (EPPO, 2013; Pansa et al., 2013).

Ecological niche modelling indicates that the area of invasion suitable for H. halys is quite extensive worldwide. H. halys could become established in northern Europe, north-eastern North America, portions of southern Australia and much of New Zealand, areas of South America (Uruguay, southern Brazil and northern Argentina) and parts of Africa (northern Angola and adjacent areas of Congo and Zambia) (Zhu et al., 2012).

Introductions

Risk of Introduction

Most interceptions of Halyomorpha halys during quarantine inspections or surveys have been adults, and the entry pathways for eggs and nymphs are considered to be much lower risk (Holtz and Kamminga, 2010; Duthie et al., 2012; Gariepy et al., 2013). This is because adults have more interaction with inanimate objects, making use of various structures and materials for their winter aggregations. Immature stages are not present in aggregations and are more closely associated with host plant material. It is possible that egg masses and nymphs could be transported on fresh fruits, vegetables and nursery stock. However, eggs are sensitive to temperature and may not survive well under the cool temperatures that would be typical in produce shipments. Moreover, eggs typically hatch within a few days, and transport could potentially disrupt first-instar nymphs from feeding on the egg mass after emergence, causing increased mortality. Risk for introduction is slightly higher for second- through to fifth-instar nymphs on fresh host material, but the likelihood of survival and establishment is low on produce destined for market. Transport of nursery stock is a potential mechanism for the introduction of nymphs, but strict regulations governing transport and treatment of nursery plants greatly reduce this possibility for trans-oceanic, inter-state or long distance introductions (Duthie et al., 2012).

Although interceptions of individual H. halys are more common, aggregations clearly represent the biggest risk for establishment with multiple insects of both sexes represented. Transported aggregations by people relocating from the eastern to the western USA have been the source of potential introductions into the states of California, Washington and Idaho. Introduction pathways involving adults are most likely to occur with non-plant material and are associated with adults exhibiting aggregation behaviour. These adults are sexually immature, so the introduction of isolated individuals may represent relatively little risk compared to aggregations. In exporting countries that can be regarded as major source populations of H. halys including China, Korea, Japan and the USA, aggregations begin forming in August and September (Hoebeke and Carter, 2003; Hamilton, 2009). Interceptions of H. halys tend to increase during these times in quarantine inspections, and may correlate with transport of goods stored outside during these periods in the source country (Duthie et al., 2012). Individuals are more likely to be incidentally transported by personal items such as luggage, and aggregations are more likely to occur in larger cargos. Large items that have been left in place for extended periods of time while winter aggregations of H. halys are forming have the highest risk for harbouring aggregations. Ocean-going cargo containers or packing crates appear to be one of the most common pathways of introduction, and may have been responsible for the initial introduction of H. halys into the USA in the mid 1990s (Hoebeke and Carter, 2003; Hamilton, 2009). However, H. halys has also been intercepted from ship decks and other cargo including transported machinery, furniture and cars (Holtz and Kamminga, 2010; Duthie et al., 2012).

The risk of introduction of adults on produce or other plant material is considered low or moderate, but may have been the mechanism of introduction of H. halys into Switzerland (Wermelinger et al., 2008). However, transport packaging for plant materials, particularly if stored outside, are always a potential source of introduction. Once established, continental spread is likely to follow paths of human activity, including highways and railways. Cars, tractor-trailers, recreational vehicles and moving trucks are all known pathways of introduction over land. Deliberate introductions are unlikely as H. halys is regarded as a pest under every circumstance and has no known unintended uses.

Habitat List

Hosts/Species Affected

H. halys has over 100 reported host plants. It is widely considered to be an arboreal species and can frequently be found among woodlots. Such host plants are important for development as well as supporting populations, particularly during the initial spread into a region. In Canada for example, established populations of H. halys have only been recorded in the Province of Ontario. Homeowner finds have previously been identified in the City of Hamilton (Fogain and Graff, 2011) as well as the Greater Toronto Area, the City of Windsor, Newboro and Cedar Springs (Ontario) (Fraser and Gariepy, unpublished data). However, preliminary surveys confirmed an established breeding population in Hamilton, Ontario, as of July 2012 (Fraser and Gariepy, unpublished data). At present, these populations are localized along the top of the Niagara escarpment in urban/natural habitats within Hamilton, and have not yet been recorded in agricultural crops. Reproductive hosts from which H. halys eggs, nymphs and adults have been collected on in Ontario include: ash, buckthorn, catalpa, choke cherry, crabapple, dogwood, high bush cranberry, honeysuckle, lilac, linden, Manitoba maple, mulberry, rose, tree of heaven, walnut and wild grape (Gariepy et al., unpublished data).

The list of host plants in Europe contains 51 species in 32 families, including many exotic and native plants. High densities of nymphs and adults were observed on Catalpa bignonioides, Sorbus aucuparia, Cornus sanguinea, Fraxinus excelsior and Parthenocissus quinquefolia (Haye et al., unpublished data).

Multiple host plants seem to be important for development and survival of H. halys. This species can complete its development entirely on paulownia (Paulownia tomentosa), tree of heaven (Ailanthus altissima), English holly and peach. More details on host plants and host plant utilization can be found at http://www.stopbmsb.org/where-is-bmsb/host-plants/ as well as http://www.halyomorphahalys.com, Panizzi (1997), Nielsen and Hamilton (2009b) and Lee et al. (2013a).

In Asia, H. halys is an occasional outbreak pest of tree fruit (Funayama, 2002). Damage to apples and pears in the USA was first detected in Allentown, Pennsylvania, and Pittstown, New Jersey (Nielsen and Hamilton, 2009a). In orchards where H. halys is established in the USA, it quickly becomes the predominant stink bug species and, unlike native stink bugs, is a season-long pest of tree fruit (Nielsen and Hamilton, 2009a; Leskey et al., 2012a). In particular, peaches, nectarines, apples and Asian pears are heavily attacked. Feeding injury causes depressed or sunken areas that may become cat-faced as fruit develops. Late season injury causes corky spots on the fruit. Feeding may also cause fruiting structures to abort prematurely. Similar damage occurs in fruiting vegetables such as tomatoes and peppers, although frequently later in the season. Feeding can cause failure of seeds to develop in crops such as maize or soyabean. There is frequently a distinct edge effect in crop plots as H. halys an aggregated dispersion and moves between crops or woodlots. In soyabeans, this can result in a 'stay green' effect where pods fail to senesce at the edges due to H. halys feeding injury.

Host Plants and Other Plants Affected

Growth Stages

Symptoms

Adults and nymphs cause feeding damage. On tree fruits, feeding injury causes depressed or sunken areas that may become 'cat-faced' as the fruit develops. Late season injury causes corky spots on the fruit. Feeding may also cause fruiting structures to abort prematurely. Similar damage occurs in fruiting vegetables such as tomatoes and peppers, although frequently later in the season. Feeding can cause failure of seeds to develop in crops such as maize or soyabean. There is frequently a distinct edge effect in crop plots as H. halys has an aggregated dispersion and moves between crops or woodlots. In soyabeans, this can result in a 'stay green' effect where pods fail to senesce at the edges due to H. halys feeding injury.

List of Symptoms/Signs

Biology and Ecology

H. halys is a multivoltine species with up to five generations reported in southern China (Hoffman, 1931). In the mid-Atlantic region of the USA, it has one or two generations per year (Nielsen et al., 2008). In Switzerland H. halys has one generation per year (Haye et al., 2014). Non-reproductive adults overwinter and gradually emerge from overwintering sites beginning around March or April. There are few host plant resources available at this time and individuals are difficult to find in the field. Termination of diapause is probably driven by photoperiod ( > 14.75 h light per d (Yanagi and Hagihara 1980)); however, there is an interaction between photoperiod and temperature, and when the daylength threshold of H. halys has been reached, sexual development begins. This results in a delay between the initial adult dispersal from diapause and reproductive maturity, as females need an additional 148 DD prior to first oviposition (Nielsen et al., 2008). It is during this time period when the first movement to crops, specifically peaches, occurs. Hardwood trees and shrubs are also important early season hosts. Adults mate, with females being polyandrous, and eggs are oviposited in clusters on the underside of leaves in groups of 28 (Kawada and Kitamura, 1992). H. halys has five nymphal instars. Development from egg to adult takes 538 DD with a minimum temperature threshold of 14.14°C and a maximum temperature threshold of 35°C (Nielsen et al., 2008). At 30°C, this takes 32-35 days. H. halys can complete development on peaches, but more than 100 host plants including tree fruits, small fruits, vegetables, ornamentals and field crops (Leskey et al., 2012a) have been recorded.

Overwintering Ecology

H. halys is well-known for being a nuisance problem, as massive numbers of adults often invade human-made structures to overwinter inside protected environments (Inkley, 2012). This behaviour is generally uncommon among Pentatomidae and has been estimated to give H. halys an increased overwintering survivorship relative to other species such as Nezara viridula (Yanagi and Hagihara, 1980). Similar to other pentatomid species, H. halys will also overwinter in natural landscapes, at least in the mid-Atlantic region (Lee and Leskey, unpublished data). Overwintering H. halys were recovered from dry crevices in dead, standing trees with thick bark, particularly oak (Quercus spp.) and locust (Robinia spp.). For those trees with overwintering H. halys present, ~6 adults/tree were recovered when 20% of the total above-ground tree area was sampled.

Associations

H. halys is a vector of Paulownia witches' broom (Yuan, 1984).

Climate

Latitude/Altitude Ranges

Air Temperature

Natural enemies

Notes on Natural Enemies

Among hymenopterous natural enemies, a number of egg parasitoids have been recorded in Asia including the generalist parasitoids Anastatus spp. (Eupelmidae) (Kawada and Kitamura, 1992; Arakawa and Namura, 2002; Hou et al., 2009) and Ooencyrtus spp. (Encyrtidae) (Kawada and Kitamura, 1992; Arakawa and Namura, 2002; Qiu 2007). A pteromalid, Acroclisoides sp., has been reported (Qiu, 2007) but it is probably a hyperparasitoid, as it has been documented from other pentatomids. More common and more host-specific are telenomines (Platygastridae) in the genus Trissolcus, including T. japonicus (= T. halyomorphae) (Kawada and Kitamura, 1992; Li and Liu, 2004; Talamas et al., 2013; Yang et al., 2009), T. flavipes (Zhang et al., 1993; Qiu, 2007; Qiu et al., 2007), T. mitsukurii and T. itoi (Arakawa and Namura, 2002). The platygastrids Gryon japonicum (Noda, 1990) and G. obesum (Buffington, unpublished data) also have been recorded. A tachinid fly, Bogosia sp., is known to attack adult H. halys (Kawada and Kitamura 1992). No nymphal parasitoids are known. The highest levels of parasitism, ranging from 63 to 85%, have been attributed to Trissolcus (Zhang et al., 1993; Qiu, 2007; Yang et al., 2009) and to Anastatus (Hou et al., 2009). Predatory arthropods reported in Asia include the pentatomid Arma chinensis, the asilid Astochia virgatipes, an anthocorid, Orius sp., and the thomisid spiders Misumena tricuspidata [Misumenops tricuspidatus] (Qiu, 2007) and Isyndus obscurus (Oda et al., 1982; Kawada and Kitamura, 1992). Several other reports mention the entomopathogen Ophiocordyceps nutans (Sasaki et al., 2012) and the intestinal virus of Plautia stali (Nakashima et al., 1998). In North America, commonly found predators of eggs, nymphs and adults have also been reported in the Anthocoridae, Geocoridae, Reduviidae, Asilidae, Chrysopidae and Melyridae. In crop and ornamental plots surveyed in Maryland, Ooencyrtus sp. and Telenomus podisi were among the most commonly found species emerging from H. halys eggs in soyabean, maize and vegetable plots, while Anastatus reduvii and A. pearsalli were commonly found on ornamental plants, but were absent or rare in maize and soyabean plots (Hooks, unpublished data). In apple orchards surveyed in Pennsylvania, T. podisi was the most common species found to attack H. halys egg masses (Biddinger, unpublished data). In Delaware, successful parasitism by Trissolcus brochymenae, T. euschisti, T. edessae and Anastatus spp. of sentinel H. halys egg masses on Paulownia was typically low  < 1-3%). Parasitism of adult H. halys by tachinid flies in Pennsylvania and Delaware averaged 1-5% (but with up to 20% in some locations) and a negligible emergence rate (Biddinger, unpublished data; Hoelmer, unpublished data). In North America, commonly found predators of eggs, nymphs and adults have also been reported in the Anthocoridae, Geocoridae, Reduviidae, Asilidae, Chrysopidae and Melyridae.

The impact of natural enemies on H. halys populations in Europe is unknown, but laboratory tests with common European pentatomid egg parasitoids, e.g. Trissolcus semistriatus, Trissolcus flavipes and Telenomus chloropus suggest that H. halys is not a suitable host (Haye and Gariepy, unpublished data).

Means of Movement and Dispersal

H. halys has a strong capacity to disperse at landscape levels throughout most periods of its lifetime. In laboratory studies where H. halys adults were tethered to a flight mill, wild populations flew on average 2 km over a day (Wiman et al., 2013). Where free flight of H. halys was directly observed and tracked in field studies, the mean flight speed was 3 m/s along a straight line from take-off to landing (Lee et al., 2013b). Adult flight activity also occurs at night as adults seek out mates or alternate food resources. Black light traps are good monitoring tools for landscape-level movement of H. halys. Because a lot of activity occurs at night, adults that are dispersing for new resources (food or mates) may be caught in the trap. This method has demonstrated a 75% annual increase in H. halys' population size in New Jersey from 2004 to 2011. Although activity changes throughout the year, a large peak in flight activity occurs at 685 DD14.17 (Nielsen et al., 2013). Nymphs also actively disperse to host plants. For nymphs, although the first instars tend to remain aggregated around the egg mass, later instars show a strong capacity to disperse in the laboratory and field. In the laboratory, the older instars were capable of climbing 6-8 m in 15 min. In the field, the third and fifth instars walked on average 1.3 and 2.6 m over 30 minutes on a grassy surface (Lee and Leskey, unpublished data).

Pathway Causes

Pathway Vectors

Plant Trade

Wood Packaging

Impact Summary

Impact

In 2008-2009, increasing H. halys populations in the mid-Atlantic region of the USA caused late-season problems to tree fruit (Leskey and Hamilton, 2010a) though H. halys was not a widely recognized pest until late in the 2010 season. To date, H. halys has been recorded in many important USA agricultural production regions. H. halys distribution has continued to spread in the USA and has recently been recorded in orchard crop production regions in Oregon (Wiman et al., 2013) and could spread to other major production regions of similar crops throughout much of North America (Zhu et al., 2012). Susceptible crops in the USA where the bug is present are worth > $40 billion (NASS, 2013).

Nuisance impacts are especially problematic in rural areas, and have been reported in many urban and metropolitan regions. In the autumn, H. halys moves to structures, often by the thousands, generating numerous complaints (Inkley, 2012). Similar to the impacts on commercial growers, homeowners are also experiencing damage to backyard fruit and vegetable gardens.

H. halys attacks tree fruit (Nielsen and Hamilton, 2009a; Leskey et al., 2012a), small fruit, vegetables (Kuhar et al., 2012a), tree nuts (Hedstrom et al., 2013), ornamentals (Martinson et al., 2013) and row crops (Nielsen et al., 2011; Owens et al., 2013). In tree fruit, economic damage due to H. halys has resulted in increased production inputs and secondary pest outbreaks (Leskey et al., 2012a). In some cases, up to four-fold more pesticides were applied in affected fruit orchards (Leskey et al., 2012a). An outbreak in 2010 in the mid-Atlantic region resulted in > $37 million losses to apple alone and some stone fruit growers lost 90% of their crop (Leskey and Hamilton, 2010 a, b). Even unnoticeable populations in tree fruit may cause significant crop losses of up to 25% (Nielsen and Hamilton, 2009a). Tuncer and Ecevit (1997) and Tuncer et al. (2005) found that indigenous stink bugs in Turkey cause up to 3% direct crop loss to hazelnut. Should a similar scenario unfold in nut production areas in the USA, this may result in $200 million losses to tree nuts annually. Vegetables most at risk are sweetcorn, peppers, tomato, okra, aubergine, asparagus, cucurbits, crucifers and edible beans. Damage exceeding 50% is common under heavy infestations. With the exception of early sweetcorn, which may be damaged in early July, most vegetable crops are attacked from late July to September (Kuhar et al., 2012a). Taint and contamination of harvested fruit may also be an issue, particularly for small fruit and grapes. In wine made from H. halys-contaminated grapes, trans-2-decenal was the main taint compound (Mohekar et al., 2013) associated with H. halys. In some cases taint from stink bugs is transient and does not survive the fermentation/bottling process (Fiola 2012). Nevertheless, wines containing certain levels of this compound were perceived to be inferior compared to uncontaminated wines (Tomasino et al., 2013a, b). H. halys has been successfully removed from clusters just before harvest in order to prevent 'stink bug taint' (Pfeiffer et al., 2012).

To date only a single incidence of economic damage on pepper crops has been reported in Europe from the Canton Aargau in Switzerland (Sauer, 2012).

Social Impact

Large numbers of H. halys can become a nuisance when they seek shelter in houses during autumn and winter months.

Risk and Impact Factors

• Proved invasive outside its native range
• Has a broad native range
• Is a habitat generalist
• Tolerant of shade
• Capable of securing and ingesting a wide range of food
• Highly mobile locally
• Benefits from human association (i.e. it is a human commensal)
• Has high reproductive potential
• Gregarious

• Changed gene pool/ selective loss of genotypes
• Host damage
• Negatively impacts agriculture
• Negatively impacts livelihoods
• Reduced amenity values
• Damages animal/plant products
• Negatively impacts trade/international relations

• Causes allergic responses
• Competition - monopolizing resources
• Pest and disease transmission
• Herbivory/grazing/browsing

• Highly likely to be transported internationally accidentally
• Difficult to identify/detect as a commodity contaminant
• Difficult/costly to control

Detection and Inspection

H. halys adults can be detected throughout the active growing season using blacklight traps and baited pheromone traps and nymphal populations can be detected with pheromone traps. However, each trap has limitations. Blacklight traps are attractive from early spring through September with reduced attractiveness as adults begin seeking overwintering sites. Baited pheromone trap effectiveness depends on the lure deployed. The use of methyl (2E,4E,6Z)-decatrienoate only provides late season adult attractivess, whereas the use of (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol alone or in combination with methyl (2E,4E,6Z)-decatrienoate provides season-long adult attractiveness.

In cropping systems, H. halys adults and nymphs can be detected through the use of timed visual counts, whole plant inspections, beat sheets counts and sweep netting.  Timed visual counts are effective in field maize, nursery, nut, tree fruit and vegetable crops. Whole plant inspections are possible in various vegetables, field and sweetcorn by inspecting a specified number of plants per field or through the use of counts per linear foot of row. Beat sheet counts can be employed in nursery, nut and tree fruit; however, they are discouraged in nuts and tree fruit after thinning or June drop has occurred due to the potential removal of fruit. Sweep netting can be used in soyabeans but should be confined to field borders.

H. halys adults seek concealed, cool, tight and dry locations to overwinter. Because of this overwintering behaviour and need for specific microhabitats, many suitable sites can be generated by human-made materials and used by this insect as an overwintering sites such as inside cardboard boxes, other shipping containers and luggage, between wooden boards, within layers of folded tarps, and within machinery motors and vehicles. Thus, inspection for H. halys in shipments of goods from areas where it is present will require thorough visual inspections.

Similarities to Other Species/Conditions

The superficial similarity in colour and overall appearance of H. halys to a number of other pentatomids requires that accurate identifications be based on sound morphological characters. This is particularly true for species that are found in the same habitats or utilize the same host plants, or which exhibit similar aggregation and overwintering behaviours. Rhaphigaster nebulosa is a prime example of a common European species often misidentified as H. halys because of its similar appearance, habitat preference and behaviour. Although adult H. halys present among invasive populations in Europe and North America are rather uniform in appearance, notable colour variations exist among different geographic populations in China (Hoelmer, unpublished observations of museum specimens). For North America, Hoebeke and Carter (2003) discuss possible confusion of adult H. halys with species of Brochymena in tribe Halyini and Euschistus, Holcostethus and Thyanta among members of tribe Pentatomini. For each genus, they give appropriate diagnostic characters distinguishing species from H. halys. Paiero et al. (2013) can also be used to distinguish H. halys from similar North American species. Wyniger and Kment (2010) provide an excellent dichotomous key, well illustrated with colour photographs, to distinguish H. halys from a number of native European pentatomids in the subfamily Asopine genera Arma, Picromerus, Pinthaeus and Troilus and the Pentatomine subfamily genera Carpocapsis, Dolycoris, Holcostethus, Peribalus, Pentatoma and Rhaphigaster, that are similar in appearance to H. halys. 

Prevention and Control

Susceptible Crops

Soyabean. Research has revealed three H. halys characteristics that are allowing for development of better management practices in soyabean: H. halys tends to invade soyabean fields during the R4 plant growth stage (fully elongated pods) to R6 (fully developed seed) and does the most crop injury by feeding on developing seed during R5; feeding injury is similar to that caused by native stink bug species; and populations typically infest only field edges, especially those bordering maize fields, woody edges or farm structures. While still under development, tentative thresholds are 1-2 H. halys/row foot, or 5 per 15 sweep-net sweeps. Scouting field edges is recommended during R4-R6 and making field edge-only treatments if populations exceed tentative thresholds. Several insecticides provide control, and a single field edge-only treatment is effective, if applied at the right time.

Maize. H. halys populations are highest ( > 3 per ear) during ear formation, the milk (R3) and soft dough (R3-R4) stages. Populations are typically highest within 12 m of field edges and decrease significantly toward the centres of fields. The highest populations are in maize fields bordering woods, followed by alfalfa, buildings and sorghum with the fewest in fields adjacent to open areas. Economic thresholds are under development.

Vegetables. Research shows that the vegetables most at risk to H. halys damage are sweetcorn, most varieties of pepper, tomato, okra, aubergine and edible beans. Plants are typically attacked in late summer when fruiting structures are present. Several foliar-applied insecticides provide effective control including pyrethroids (i.e., bifenthrin, permethrin and fenpropathrin); neonicotinoids (dinotefuran) and acephate (on peppers) (Kuhar et al., 2012 b, c, d, e). Neonicotinoids applied as a soil drench or via drip chemigation provide control for up to 14 days after treatment in vegetables such as pepper and tomato.

Tree fruit. H. halys adults can move into orchards at any time. Stone fruit, particularly peaches and nectarines are vulnerable in the early season, but the majority of fruit injury to pome fruit occurs later in the season. It takes several weeks for feeding injury on apple to appear; injury close to harvest can be expressed after harvest in cold storage. Issues with PHI (pre-harvest intervals) in mixed apple blocks severely restrict the availability of most insecticides used for control in the USA. Effective control can be achieved with applications of neonicotinoids and pyrethroids (Leskey et al., 2012b). Field and laboratory assays indicate that residual activity is limited. In general, damage in orchard crops has been mitigated by increases in insecticide applications against H. halys (Leskey et al., 2012a). This practice can disrupt IPM programmes, causing outbreaks of secondary pests such as European red mites, woolly apple aphids and San Jose scale. In general, overwintered H. halys populations are easier to kill with insecticide applications than the new generation adults present later in the season.

Biological Control

The egg parasitoid Anastatus has been mass-reared in the laboratory for experimental field trials in China (Hou et al., 2009) but is not yet widely applied. The role of indigenous natural enemies, primarily invertebrate predators and hymenopterous parasitoids, in the control of H. halys in crops, orchards and ornamentals surveyed in North America in Maryland, Delaware and Pennsylvania is highly variable. In Maryland, predators contributed ~40-70% of H. halys egg mortality found in some maize and soyabean plots, respectively. In Pennsylvania orchards, an estimated 25% of H. halys egg mortality is due to predation by Coccinellidae, particularly Harmonia axyridis, and earwigs (Forficulidae). In addition, late H. halys instars comprise the majority of nest provisioning by sand wasps (Crabronidae), up to 96% of discovered nests in orchards (Biddinger, unpublished data). Thus, species composition and attack rates of H. halys egg masses by native egg parasitoids appear to be highly variable depending on the crop or ecosystem studied. On the basis of the considerably higher rates of parasitism reported for Trissolcus spp. in Asia, these species are currently being evaluated in quarantine facilities in the USA as candidate agents for possible field releases.

Monitoring and Surveillance

Black light traps have been used to track H. halys activity in Japan (e.g., Moriya et al., 1987) and New Jersey. Relative pest pressure and spread of H. halys throughout New Jersey have been successfully tracked and documented using a network of black lights (Nielsen et al., 2013). In addition, baited black pyramid traps can be used to monitor H. halys (Leskey et al., 2012a). Khrimian et al. (2008) confirmed that the aggregation pheromone of Plautia stali, methyl (2E,4E,6Z)-decatrienoate (Sugie et al., 1996), is cross-attractive to H. halys, as reported in Asia (Tada et al., 2001a, b). However, adults are reliably attracted only late in the season, though nymphs are attracted season-long. In addition, the aggregation pheromone has been identified for H. halys and includes (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol (Zhang et al., 2013). These stimuli can be used in combination with pyramid-style traps to monitor presence, abundance and seasonal activity of H. halys.

Gaps in Knowledge/Research Needs

Host use patterns and preferences and related movement of H. halys need to be elucidated during the period between dispersal from overwintering sites and invasion into cultivated crops. Some wild host plant species, particularly hardwood trees, could play a key role in supporting overwintered and new generation H. halys populations. However, little is known regarding host plant selection factors, including specific visual, olfactory and host quality cues, host plant preferences including wild and cultivated throughout the season and movement patterns at landscape levels. A greater understanding of these factors will provide many opportunities to manage H. halys as their temporal movement patterns and associated at-risk crops would be known.

The impact of abiotic conditions on population dynamics of H. halys during the active growing season and the overwintering period is poorly understood. In the USA, populations have fluctuated dramatically from year to year in areas in the mid-Atlantic with well-established populations since 2010, but key factors promoting or reducing survivorship remain unknown.

Similarly, the overall impact of native natural enemies on H. halys populations in invaded regions is also poorly understood. Although there are some climatic models predicting where H. halys can become established, more precise models could be used to better predict where H. halys poses a significant risk to agriculture. Furthermore, the taxonomy of many natural enemies, particularly Trissolcus spp., is presently in a confused state; efforts are presently underway to resolve not only East Asian species, but also provide updated identification tools for native North American species.

Dispersal capacity of adults and nymphs is not well established. The impact of factors such a mating status, age and feeding state on behaviour and dispersal are not known. How adult H. halys select overwintering sites is unknown. H. halys will overwinter in human-made structures and in dead, standing trees in forests, but how H. halys selects particular locations and why the density of adults at particular locations varies greatly is unknown.

Attractants for H. halys are available including methyl (2E,4E,6Z)-decatrienoate and its aggregation pheromone. However, optimal dose, distance of response at a particular concentration, physiological status of adults and nymphs that respond to olfactory stimuli are all factors that still require further study. Furthermore, why adults are responsive to methyl (2E,4E,6Z)-decatrienoate in the late summer while nymphs respond season-long is unknown. Similarly, the distance of response to light traps is unknown.

Management tools have been developed but revolve around the use of a select number of materials applied frequently. This level of use may not be sustainable due to outbreaks of secondary pests, impacts on natural enemies and pollinators, and the increasing potential for the development of resistance. Effective tools are also not available to organic growers. The development of economic thresholds and new classes of insecticides, resistance monitoring programs, and the use of trap, barrier and repellent crops need further investigation.

References

Arakawa R, Namura Y, 2002. Effects of temperature on development of three Trissolcus spp. (Hymenoptera: Scelionidae), egg parasitoids of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Entomological Science, 5(2):215-218.

Arnold K, 2009. Halyomorpha halys (Stal, 1855), a stink bug species newly detected among the European fauna (Insecta: Heteroptera, Pentatomidae, Pentatominae, Cappaeini). Mitteilungen des Thuringer Entomologenverbandes, e.V.16:10.

CABI/EPPO, 2010. Halyomorpha halys. [Distribution map]. Distribution Maps of Plant Pests, No.June. Wallingford, UK: CABI, Map 736.

CABI/EPPO, 2013. Halyomorpha halys. [Distribution map]. Distribution Maps of Plant Pests, No.December. Wallingford, UK: CABI, Map 736 (1st revision).

Callot H, Brua C, 2013. Halyomorpha halys (Stal,1855), the marmorated stink bug, new species for the fauna of France (Heteroptera Pentatomidae). LÕEntomologiste, 69:69-71.

Distant WL, 1880. Notes on some exotic Hemiptera, with descriptions of new species. Entomologist's Monthly Magazine, 16:201-203.

Distant WL, 1893. On some allied Pentatomidae, with synonymical notes. Annals and Magazine of Natural History, 6(11):389-394.

Distant WL, 1899. Rhynchotal notes. - III Heteroptera: Discocephalinae and Pentatominae (part). Annals and Magazine of Natural History, 7(4):421-445.

Duthie CD, Michael T, Stephenson B, Yamoah E, McDonald B, 2012. Risk analysis of Halyomorpha halys (brown marmorated stink bug) on all pathways. Wellington, New Zealand: Biosecurity Risk Analysis Group, Ministry of Agriculture and Forestry of New Zealand, 57 p.

EPPO, 2014. PQR database. Paris, France: European and Mediterranean Plant Protection Organization. http://www.eppo.int/DATABASES/pqr/pqr.htm

EPPO, 2018. EPPO Global Database https://gd.eppo.int/

Fiola JA, 2012. Brown marmorated stinkbug in grapes and wine. Good Fruit Grower, 63(16):44-46.

Fogain R, Graff S, 2011. First records of the invasive pest, Halyomorpha halys (Hemiptera: Pentatomidae), in Ontario and Quebec. Journal of the Entomological Society of Ontario, 142:45-48. http://www.entsocont.com/pub.htm

Funayama K, 2002. Comparison of the susceptibility to injury of apple cultivars by stink bugs. Japanese Journal of Applied Entomology and Zoology, 46(1):37-40.

Gariepy TD, Haye T, Fraser H, Zhang J, 2013. Occurrence, genetic diversity, and potential pathways of entry of Halyomorpha halys in newly invaded areas of Canada and Switzerland. Journal of Pest Science. http://rd.springer.com/article/10.1007%2Fs10340-013-0529-3

Goto S, Sato T, Abe O, Saito T, Marukawa T, 2002. Damage to persimmons by stink bugs and their seasonal prevalence in Shonai, Yamagata. 53rd Annual Report of the Society of Plant Protection of North Japan, 276-278; 8 ref.

Hamilton GC, 2009. Brown marmorated stink bug. Am. Entomol, 55:19-20.

Harris AC, 2010. Halyomorpha halys (Hemiptera: Pentatomidae) and Protaetia brevitarsis (Coleoptera: Scarabaeidae: Cetoniinae) intercepted in Dunedin. The Weta, 40:42-44.

Haye T, Abdallah S, Gariepy T, Wyniger D, 2014. Phenology, life table analysis, and temperature requirements of the invasive brown marmorated stink bug, Halyomorpha halys, in Europe. Journal of Pest Science. http://rd.springer.com/article/10.1007/s10340-014-0560-z#

Haye T, Wyniger D, 2013. Current Distribution of Halyomorpha halys in Europe. http://www.halyomorphalhalys.com/aktuelle-verbreitungskarts-current-distribution.html

Heckmann R, 2012. First evidence of Halyomorpha halys (Stal, 1855) (Heteroptera: Pentatomidae) in Germany. Heteropteron H, 36:17-18.

Hedstrom C, Walton VM, Shearer PW, Olsen J, 2013. Feeding damage of brown marmorated stink bug (Halyomorpha halys) on commercial hazelnut (Corylus avellana). In: 72nd Proceedings of the Pacific Northwest Insect Pest Management Conference, Portland, Oregon, January 7-8, 2013., USA. http://www.ipmnet.org/PNWIMC/2013_PNWIMC_Conference_Proceedings.pdf

Hoebeke ER, Carter ME, 2003. Halyomorpha halys (St+l) (Heteroptera: Pentatomidae): a polyphagous plant pest from Asia newly detected in North America. Proceedings of the Entomological Society of Washington, 105(1):225-237; many ref.

Hoffman WE, 1931. A pentatomid pest of growing beans in south China. Peking Natural History Bulletin, 5(2):25.

Holtz T, Kamminga K, 2010. Qualitative analysis of the pest risk potential of the brown marmorated stink bug (BMSB), Halyomorpha halys (Stal), in the United States., USA: USDA-APHIS-PPQ, 33 p.

Hou Z, Liang H, Chen Q, Hu Y, Tian H, 2009. Application of Anastatus sp. against Halyomorpha halys. Forest Pest Disease, 4(39-40):43.

Inkley DB, 2012. Characteristics of home invasion by the brown marmorated stink bug (Hemiptera: Pentatomidae). Journal of Entomological Science, 47(2):125-130.

Josifov MV, Kerzhner IM, 1978. Heteroptera aus Korea. Teil (Aradidae, Berytidae, Lygaeidae, Pyrrhocoridae, Rhopalidae, Alydidae, Coreidae, Urostylidae, Acanthosomatidae, Scutelleridae, Pentatomidae, Cydnidae, Plataspidae). Fragmenta Faunistica, 23:137-196.

Karun NC, Sridhar KR, 2013. Incidence of entomophagous medicinal fungus, Ophiocordyceps nutans on stink bug, Halyomorpha halys (Stal) in the Western Ghats of India. Journal of Biological Control, 27(2):139-143. http://journalofbiologicalcontrol.com/index.php/jbc/article/view/45592/36929

Kawada H, Kitamura C, 1992. The tachinid fly, Bogosia sp. (Diptera: Tachinidae) as a parasitoid of the brown marmorated stink bug, Halyomorpha mista Uhler (Heteroptera: Pentatomidae). Japanese Journal of Applied Environmental Entomology and Zoology, 4:65-70.

Khrimian A, Shearer PW, Zhang AJ, Hamilton GC, Aldrich JR, 2008. Field trapping of the invasive brown marmorated stink bug, Halyomorpha halys, with geometric isomers of methyl 2,4,6-decatrienoate. Journal of Agricultural and Food Chemistry, 56(1):197-203. http://pubs.acs.org/journals/jafcau/index.html

Kuhar TP, Doughty H, Kamminga K, Wallingford A, Philips C, Aigner J, 2012. Evaluation of insecticides for the control of brown marmorated stink bug in bell peppers in Virginia experiment 1, 2011. Arthropod Management Tests, 37:E37. http://www.entsoc.org/category/amt-hosts/pepper-bell

Kuhar TP, Doughty H, Kamminga K, Wallingford A, Philips C, Aigner J, 2012. Evaluation of insecticides for the control of brown marmorated stink bug in bell peppers in Virginia experiment 2, 2011. Arthropod Management Tests, 37:E38. http://www.entsoc.org/category/amt-hosts/pepper-bell

Kuhar TP, Doughty H, Kamminga K, Wallingford A, Philips C, Aigner J, 2012. Evaluation of insecticides for the control of brown marmorated stink bug in bell peppers in Virginia experiment 3, 2011. Arthropod Management Tests, 37:E39. http://www.entsoc.org/category/amt-hosts/pepper-bell

Kuhar TP, Doughty H, Kamminga K, Wallingford A, Philips C, Aigner J, 2012. Evaluation of insecticides for the control of brown marmorated stink bug in bell peppers in Virginia experiment 4, 2011. Arthropod Management Tests, 37:E40. http://www.entsoc.org/category/amt-hosts/pepper-bell

Kuhar TP, Kamminga KL, Whalen J, Dively GP, Brust G, Hooks CRR, Hamilton G, Herbert DA, 2012. The pest potential of brown marmorated stink bug on vegetable crops. Plant Health Progress, No.May:PHP-2012-0523-01-BR. http://www.plantmanagementnetwork.org/sub/php/brief/2012/stinkbug/

Lee DH, Wright SE, Boiteau G, Vincent C, Leskey TC, 2013. Effectiveness of glues for harmonic radar tag attachment on Halyomorpha halys (Hemiptera: Pentatomidae) and their impact on adult survivorship and mobility. Environmental Entomology, 42(3):515-523. http://esa.publisher.ingentaconnect.com/content/esa/envent/2013/00000042/00000003/art00013

Lee DooHyung, Short BD, Joseph SV, Bergh JC, Leskey TC, 2013. Review of the biology, ecology, and management of Halyomorpha halys (Hemiptera: Pentatomidae) in China, Japan, and the Republic of Korea. Environmental Entomology, 42(4):627-641. http://esa.publisher.ingentaconnect.com/content/esa/envent/2013/00000042/00000004/art00003

Leskey T, Hamilton GC, 2010. Brown Marmorated Stink Bug Working Group Meeting held at Alson H Smith Research and Extension Center, Virginia Agriculture Experiment Station, Virginia Tech, Winchester, Virginia, USA, November 17, 2010. http://projects.ipmcenters.org/Northeastern/FundedProjects/ReportFiles/Pship2010/Pship2010-Leskey-ProgressReport-237195-Meeting-2010_11_17.pdf

Leskey T, Hamilton GC, 2010. Brown Marmorated Stink Bug Working Group Meeting held at Appalachian Fruit Research Station, Kearneysville, West Virginia, June 15-16. http://projects.ipmcenters.org/Northeastern/FundedProjects/ReportFiles/Pship2010/Pship2010-Leskey-ProgressReport-237195

Leskey T, Hamilton GC, 2012. Brown Marmorated Stink Bug Working Group Meeting held at Alson H. Smith Jr. Agricultural Research and Extension Center, Winchester, Virginia, USA, November 27, 2012. Brown Marmorated Stink Bug Working Group Meeting held at Alson H. Smith Jr. Agricultural Research and Extension Center, Winchester, Virginia, USA, November 27, 2012. http://www.northeastipm.org/neipm/assets/File/BMSB-Working-Group-Meeting-Report-Nov-2012.pdf

Leskey TC, Lee DH, Short BD, Wright SE, 2012. Impact of insecticides on the invasive Halyomorpha halys (Hemiptera: Pentatomidae): analysis of insecticide lethality. Journal of Economic Entomology, 105(5):1726-1735. http://docserver.ingentaconnect.com/deliver/connect/esa/00220493/v105n5/s32.pdf?expires=1350877016&id=0000&titleid=10264&checksum=8FF65650F2FE2A85272B708746130CA1

Leskey TC, Short BD, Butler BR, Wright SE, 2012. Impact of the invasive brown marmorated stink bug, Halyomorpha halys (Stal), in mid-Atlantic tree fruit orchards in the United States: case studies of commercial management. Psyche: A Journal of Entomology, 2012:Article ID 535062. http://www.hindawi.com/journals/psyche/2012/535062/

Li Z, Liu Y, 2004. Effect of temperature on development of egg parasitoid Trissolcus halyomorphae and the eggs of its host, Halyomorpha halys. Chinese Journal of Biological Control, 20(1):64-66.

Macavei LI, Bâetan R, Oltean I, Florian T, Varga M, Costi E, Maistrello L, 2015. First detection of Halyomorpha halys Stal, a new invasive species with a high potential of damage on agricultural crops in Romania. Lucrari Stiintifice, Universitatea de Stiinte Agricole Si Medicina Veterinara "Ion Ionescu de la Brad" Iasi, Seria Agronomie, 58(1):105-108. http://www.revagrois.ro/volum/Vol-58-1_2015.pdf

Maistrello L, Dioli P, Vaccari G, Nannini R, Bortolotti P, Caruso S, Costi E, Montermini A, Casoli L, Bariselli M, 2014. First records in Italy of the Asian stinkbug Halyomorpha halys, a new threat for fruit crops. (Primi rinvenimenti in italia della cimice esotica Halyomorpha halys, una nuova minaccia per la frutticoltura.) In: Atti, Giornate Fitopatologiche, Chianciano Terme (Siena), 18-21 marzo 2014, Volume primo [ed. by Brunelli, A.\Collina, M.]. Bologna, Italy: Alma Mater Studiorum, Universitá di Bologna, 283-288.

Martinson HM, Raupp MJ, Shrewsbury PM, 2013. Invasive stink bug wounds trees, liberates sugars, and facilitates native hymenoptera. Annals of the Entomological Society of America, 106(1):47-52. http://www.bioone.org/doi/abs/10.1603/AN12088

Milonas PG, Partsinevelos GK, 2014. First report of brown marmorated stink bug Halyomorpha halys Stal (Hemiptera: Pentatomidae) in Greece. Bulletin OEPP/EPPO Bulletin, 44(2):183-186. http://onlinelibrary.wiley.com/journal/10.1111/(ISSN)1365-2338

Mityushev, I. M., 2016. First report of the brown marmorated stink bug, Halyomorpha halys St?l, in the Russian Federation., Monitoring and biological control methods of woody plant pests and pathogens: from theory to practice. Proceedings of International Conference, Moscow, Russia, April 18-22, 2016:147-148

Mohekar P, Lapis T, Lim J, Tomasino E, 2013. Retronasal detection and consumer rejection threshold of "brown marmorated stink bug taint" in commercial Pinot Noir. In: 64th ASEV National Conference, June 24-28, Monterey, California, USA., USA: American Society for Enology and Viticulture.

Moore A, 2014. Brown Marmorated Stink Bug Halyomorpha halys (Stal 1855) (Hemiptera: Pentatomidae). Guam New Invasive Species Alert No. 2014-01, No. 2014-01., Guam: University of Guam. http://guaminsects.net/anr/sites/default/files/brownMarmoratedStinkBug.pdf

Moriya S, Shiga M, Mabuci M, 1987. Analysis of light trap records in four major species of fruit piercing stink bugs with special reference to body size variation in trapped adults of Plautia stali Scott. Bulletin of Fruit Tree Research Station A, 14:79-84.

Nakashima N, Sasaki J, Tsuda K, Yasunaga C, Noda H, 1998. Properties of a new picorna-like virus of the brown-winged green bug, Plautia stali. Journal of Invertebrate Pathology, 71(2):151-158.

NASS, 2013. National Agricultural Statistics Service database., USA: National Agricultural Statistics Service. http://www.nass.usda.gov/

Nielsen AL, Hamilton GC, 2009. Life history of the invasive species Halyomorpha halys (Hemiptera: Pentatomidae) in Northeastern United States. Annals of the Entomological Society of America, 102(4):608-616. http://docserver.ingentaconnect.com/deliver/connect/esa/00138746/v102n4/s5.pdf?expires=1248335315&id=0000&titleid=10263&checksum=071BB0E53AA8E4BDE78912E70002F997

Nielsen AL, Hamilton GC, 2009. Seasonal occurrence and impact of Halyomorpha halys (Hemiptera: Pentatomidae) in tree fruit. Journal of Economic Entomology, 102(3):1133-1140. http://docserver.ingentaconnect.com/deliver/connect/esa/00220493/v102n3/s35.pdf?expires=1264487009&id=0000&titleid=10264&checksum=23593EA7942CFE2816F170695B74D1BA

Nielsen AL, Hamilton GC, Matadha D, 2008. Developmental rate estimation and life table analysis for Halyomorpha halys (Hemiptera: Pentatomidae). Environmental Entomology, 37(2):348-355. http://www.bioone.org/doi/abs/10.1603/0046-225X%282008%2937%5B348%3ADREALT%5D2.0.CO%3B2

Nielsen AL, Hamilton GC, Shearer PW, 2011. Seasonal phenology and monitoring of the non-native Halyomorpha halys (Hemiptera: Pentatomidae) in soybean. Environmental Entomology, 40(2):231-238. http://docserver.ingentaconnect.com/deliver/connect/esa/0046225x/v40n2/s7.pdf?expires=1303713903&id=0000&titleid=10265&checksum=F70628290C131429DB4658549F56D45F

Nielsen AL, Holmstrom K, Hamilton GC, Cambridge J, Ingerson-Mahar J, 2013. Using black light traps to monitor abundance, spread and flight behavior of Halyomorpha halys (Hemiptera: Pentatomidae). Journal of Economic Entomology, 106(3):1495-1502.

Noda T, 1990. Laboratory host range test for the parasitic wasp, Gryon japonicum (Ashmead) (Hymenoptera: Scelionidae). Japanese Journal of Applied Entomology and Zoology, 34(3):249-252

Oda M, Nakanishi Y, Uesumi Y, 1982. Ecological studies of stink bugs attacking fruit trees. Report 4: fluctuations in the hibernated population of the brown-marmorated stink bug, Halyomorpha halys (Stal) and seasonal prevalence of the adults after hibernation. Bulletin of Nara Agricultural Station, 13:66-73.

Oregon Department of Agriculture, 2005. Pest Alert: Brown Marmorated Stink Bug. Oregon, USA. http://egov.oregon.gov/ODA/PLANT/docs/pdf/ippm_halyomorpha.pdf.

Owens DR, Herbert DA Jr, Dively GP, Reisig DD, Kuhar TP, 2013. Does feeding by Halyomorpha halys (Hemiptera: Pentatomidae) reduce soybean seed quality and yield? Journal of Economic Entomology, 106(3):1317-1323. http://esa.publisher.ingentaconnect.com/content/esa/jee/2013/00000106/00000003/art00030

Panizzi AR, 1997. Wild hosts of pentatomids: ecological significance and role in their pest status on crops. Annual Review of Entomology, 42:99-122.

Pansa MG, Asteggiano L, Costamagna C, Vittone G, Tavella L, 2013. First discovery of Halyomorpha halys in peach orchards in Piedmont. (Primo ritrovamento di Halyomorpha halys nei pescheti piemontesi.) Informatore Agrario, 69(37):60-61. http://www.informatoreagrario.it

Papp V, Redei D, Haltrich A, Vétek G, 2014. Brown marmorated stink bug [Halyomorpha halys (Stal, 1855)] (Heteroptera: Pentatomidae) in Hungary. (Az ázsiai márványospoloska [Halyomorpha halys (Stal, 1855)] (Heteroptera: Pentatomidae) Magyarországon.) Növényvédelem, 50(11):489-495.

Pfeiffer DG, Leskey TC, Burrack HJ, 2012. Threatening the harvest: The threat from three invasive insects in late season vineyards. In: Arthropod Management in Vineyards: Pests, Approaches, and Future Directions [ed. by Bostanian, \N. J. \Vincent, C. \Isaacs, R.]. Dordrecht, The Netherlands: Springer, 449-474.

Qiu L, Yang Z, Tao W, 2007. Biology and population dynamics of Trissolcus halyomorphae. Scientia Silvae Sinicae, 43(11):62-65.

Qiu L-F, 2007. Studies on biology of the brown-marmorated stink bug, Halyomorpha halys (Stal) (Hemiptera: Pentatomidae), an important pest for pome trees in China and its biological control. PhD dissertation. Beijing, China: Chinese Academy of Forestry.

Rider DA, 2005. Halyomorpha halys Stal, 1855. Halyomorpha halys Stal, 1855. Fargo, USA: North Dakota State University. http://www.ndsu.nodak.edu/ndsu/rider/Pentatomoidea/Species_Cappaeini/Halyomorpha_halys.htm

Rider DA, Zheng LY, Kerzhner IM, 2002. Checklist and nomenclatural notes on the Chinese Pentatomidae (Heteroptera). II. Pentatominae. Zoosystematica Rossica, 11(1):135-153.

Sasaki F, Miyamoto T, Yamamoto A, Tamai Y, Yajima T, 2012. Relationship between intraspecific variations and host insects of Ophiocordyceps nutans collected in Japan. Mycoscience, 53(2):85-91. http://www.springerlink.com/content/e0n5684220wq8170/

Sauer C, 2012. The Marbled tree bug occurs again on the DeutschschweizerGemu Sebau. (Die Marmorierte Baumwanze tritt neu im DeutschschweizerGemüsebau auf.) Extension Gemüsebau, Forschungsanstalt Agroscope Changins-Wädenswil, Gemüsebau Info, 28(12):4-5.

Šeat, J., 2015. Halyomorpha halys (St?l, 1855) (Heteroptera: Pentatomidae) a new invasive species in Serbia., Acta Entomologica Serbica, 20(1):167-171 http://aes.bio.bg.ac.rs/index.php/aes/article/view/63/pdf_23

Song HW, Wang CM, 1993. Damage by Halyomorpha halys (Stal) and Erthesina fullo (Thunberg) to jujube trees and their control. Entomological Knowledge, 30(4):225-228; 3 ref.

Sugie H, Yoshida M, Kawasaki K, Noguchi H, Moriya S, Takagi K, Fukuda H, Fujiie A, Yamanaka M, Ohira Y, Tsutsumi T, Tsuda K, Fukumoto K, Yamashita M, Suzuki H, 1996. Identification of the aggregation pheromone of the brown-winged green bug, Plautia stali Scott (Heteroptera: Pentatomidae). Applied Entomology and Zoology, 31(3):427-431.

Tada N, Yoshida M, Sato Y, 2001. 52nd Annual Report of the Society of Plant Protection of North Japan. Akita, Japan: Society of Plant Protection of North Japan, 224-226.

Tada N, Yoshida M, Sato Y, 2001. 52nd Annual Report of the Society of Plant Protection of North Japan. Akita, Japan: Society of Plant Protection of North Japan, 227-229.

Talamas E, Buffington M, Hoelmer K, 2013. New Synonymy of Trissolcus halyomorphae. Journal of Hymenoptera Research, 33:113-117.

Tindall KV, Fothergill K, McCormack B, 2012. Halyomorpha halys (Hemiptera: Pentatomidae): a first Kansas record. Journal of the Kansas Entomological Society, 85(2):169. http://www.bioone.org/perlserv/?request=get-current-issue

Tomasino E, Mohekar P, Lapis T, Wiman N, Walton V, Lim J, 2013. Effect of brown marmorated stink bug on wine - Impact to Pinot Noir quality and threshold determination of taint compound trans-2-decenal. In: The 15th Australian Wine Industry Technical Conference, July 13-18, Sydney, Australia., Australia: Australian Wine Industry Technical Conference.

Tomasino E, Wiman N, Osborne J, Hedstom C, Walton V, 2013. Impact of brown marmorated stink bug on Pinot Noir quality. In: 64th ASEV National Conference, June 24-28, Monterey, California, USA., USA: American Society for Enology and Viticulture.

Tuncer C, Ecevit O, 1997. Current status of hazelnut pests in Turkey. Acta Horticulturae, 445.

Tuncer C, Saruhan I, Akça I, 2005. The insect pest problem affecting hazelnut kernel quality in Turkey. Acta Horticulturae [Proceedings of the Sixth International Congress on Hazelnut, Tarragona-Reus, Spain, 14-18 June, 2004.], No.686:367-375. http://www.actahort.org

Vétek G, Papp V, Haltrich A, Rédei D, 2014. First record of the brown marmorated stink bug, Halyomorpha halys (Hemiptera: Heteroptera: Pentatomidae), in Hungary, with description of the genitalia of both sexes. Zootaxa, 3780(1):194-200. http://www.mapress.com/zootaxa/2014/f/z03780p200f.pdf

Wermelinger B, Wyniger D, Forster B, 2008. First records of an invasive bug in Europe: Halyomorpha halys Stal (Heteroptera: Pentatomidae), a new pest on woody ornamentals and fruit trees? Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 81(1/2):1-8.

Wiman NG, Shearer P, Walton V, Rondon S, 2013. Documenting an invasion: Brown marmorated stink bug in Oregon. In: 87th Western Orchard Pest and Disease Management Conference, January 9-11, Portland, Oregon, USA., USA.

Wiman NG, Walton VM, Shearer PW, Rondon SI, Lee JC, 2013. Observations on flight activity of Oregon populations of brown marmorated stink bug, Halyomorpha halys (Hemiptera: Pentatomidae). Environmental Entomology.

Wyniger D, Kment P, 2010. Key for the separation of Halyomorpha halys (Stal) from similar-appearing pentatomids (Insecta: Heteroptera: Pentatomidae) occurring in Central Europe, with new Swiss records. Mitteilungen der Schweizerischen Entomologischen Gesellschaft, 83(3/4):261-270.

Xu J, Foneseca DM, Hamilton GC, Hoelmer KA, Nielsen AL, 2013. Tracing the origin of US brown marmorated stink bugs, Halyomorpha halys. Biological Invasions. http://rd.springer.com/article/10.1007%2Fs10530-013-0510-3

Yanagi T, Hagihara Y, 1980. Ecology of the brown marmorated stink bug. Plant Protection, 34:315-321.

Yang Z-Q, Yao Y-X, Qiu L-F, Li Z-X, 2009. A new species of Trissolcus (Hymenoptera: Scelionidae) parasitizing eggs of Halyomorpha halys (Heteroptera: Pentatomidae) in China with comments on its biology. Annals of the Entomological Society of America, 102(1):39-47.

Yuan TL, 1984. Some studies on witches' broom disease of Paulownia in China. International Journal of Tropical Plant Diseases, 2(2):181-190

Zhang A, Khrimian A, Aldrich JR, Leskey TC, Weber DC, 2013. Compositions and methods to attract brown marmrorated stink bug (BMSB), Halyomorpha halys. U.S. Provisional Application No. 61/724,475., USA. http://www.google.com/patents/WO2013090703A1?cl=en

Zhang C-T, Yao XY, Qiu LF, Li ZF, 1993. A study on the biological characteristics of Halyomorpha picus and Erthesina fullo. Forest Research, 6:271-275.

Zhu GengPing, Bu WenJun, Gao YuBao, Liu GuoQing, 2012. Potential geographic distribution of Brown Marmorated Stink Bug invasion (Halyomorpha halys). PLoS ONE, 7(2):e31246. http://www.plosone.org/article/info%3Adoi%2F10.1371%2Fjournal.pone.0031246

Links to Websites

Contributors

23/08/13 Original text by:

Tracey C. Leskey, USDA-ARS, Appalachian Fruit Research Station, 2217 Wiltshire Road, Kearneysville, WV 25430, USA
George C. Hamilton, Department of Entomology, Rutgers University, 93 Lipman Drive, New Brunswick, NJ 08901, USA
David J. Biddinger, Department of Entomology, Penn State University, Fruit Research and Extension Center, 290 University Drive, Biglerville, PA 17307, USA
Matthew L. Buffington,Systematic Entomology Laboratory, National Museum of Natural History, Washington, D.C 20013-7012, USA
Christine Dieckhoff, USDA-ARS, Beneficial Insects Introduction Research Unit, Newark, DE 19713-3814, USA
Galen P. Dively, Department of Entomology, University of Maryland, 4112 Plant Sciences Building, College Park, MD 20742, USA
Hannah Fraser, Ontario Ministry of Agriculture and Food and Ministry of Rural Affairs, 4890 Victoria Ave North, Vineland, Ontario, Canada L0R 2E0
Tara Gariepy, Agriculture and Agri-Foods Canada, 1391 Sandford St, London, Ontario, Canada N5V 4T3
Christopher Hedstrom, Department of Horticulture, Oregon State University, 4017 Ag and Life Sciences Bldg, Corvallis, OR 97331-7304, USA
D. Ames Herbert, Department of Entomology, Virginia Tech, Tidewater AREC, 6321 Holland Road, Suffolk, VA 23437, USA
Kim A. Hoelmer, USDA-ARS, European Biological Control Laboratory, CS90013 Montferrier-sur-Lez, 34988 St. Gély du Fesc CEDEX, France
Cerruti R.R. Hooks, Department of Entomology, University of Maryland, 4112 Plant Sciences Building, College Park, MD 20742, USA
Douglas Inkley, National Wildlife Federation, 11100 Wildlife Center Drive, Reston, VA 20190, USA
Greg Krawczyk, Department of Entomology, Penn State University, Fruit Research and Extension Center, 290 University Drive, Biglerville, PA 17307, USA
Thomas P. Kuhar, Department of Entomology, Virginia Tech, 216 Price Hall, Blacksburg, VA 24061, USA
Doo-Hyung Lee, USDA-ARS, Appalachian Fruit Research Station, 2217 Wiltshire Road, Kearneysville, WV 25430 and Department of Entomology, Rutgers University, 93 Lipman Drive, New Brunswick, NJ 08901, USA
Anne L. Nielsen, Department of Entomology, Rutgers University, 93 Lipman Drive, New Brunswick, NJ 08901, USA
Douglas G. Pfeiffer, Department of Entomology, Virginia Tech, 216 Price Hall, Blacksburg, VA 24061, USA
Cesar Rodriguez-Saona, Department of Entomology, Rutgers University, 93 Lipman Drive, New Brunswick, NJ 08901, USA
Peter W. Shearer, Mid-Columbia Agricultural Research and Extension Center, Oregon State University, 3005 Experiment Station Drive, Hood River, OR 97031-9512, USA
Elijah Talamas, Systematic Entomology Laboratory, National Museum of Natural History, Washington, D.C 20013-7012, USA
Elizabeth Tomasino, Department of Food Science and Technology, Oregon State University, 100 Wiegand Hall, Corvallis, OR 97331-7304, USA
John Tooker, Department of Entomology, Penn State University, 506 ASI Bldg, University Park, PA 16802, USA
P. Dilip Venugopal, Department of Entomology, University of Maryland, 4112 Plant Sciences Building, College Park, MD 20742, USA
Joanne Whalen, Department of Entomology and Wildlife Ecology, University of Delaware, 250 Townsend Hall, Newark, DE 19716-2160, USA
Vaughn Walton, Department of Horticulture, Oregon State University, 4017 Ag and Life Sciences Bldg, Corvallis, OR 97331-7304, USA
Nik Wiman, Department of Horticulture, Oregon State University, 4017 Ag and Life Sciences Bldg, Corvallis, OR 97331-7304, USA

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