Halyomorpha halys (brown marmorated stink bug)
- Summary of Invasiveness
- Taxonomic Tree
- Notes on Taxonomy and Nomenclature
- Distribution Table
- History of Introduction and Spread
- Risk of Introduction
- Habitat List
- Hosts/Species Affected
- Host Plants and Other Plants Affected
- Growth Stages
- List of Symptoms/Signs
- Biology and Ecology
- Latitude/Altitude Ranges
- Air Temperature
- Natural enemies
- Notes on Natural Enemies
- Means of Movement and Dispersal
- Pathway Causes
- Pathway Vectors
- Plant Trade
- Wood Packaging
- Impact Summary
- Social Impact
- Risk and Impact Factors
- Detection and Inspection
- Similarities to Other Species/Conditions
- Prevention and Control
- Gaps in Knowledge/Research Needs
- Links to Websites
- Distribution Maps
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PicturesTop of page
IdentityTop of page
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
- HALYHA (Halyomorpha halys)
Summary of InvasivenessTop of page
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 TreeTop of page
- 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 NomenclatureTop of page
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.
DescriptionTop of page
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.
DistributionTop of page
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 TableTop of page
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.
|Continent/Country/Region||Distribution||Last Reported||Origin||First Reported||Invasive||Reference||Notes|
|China||Widespread||Native||CABI/EPPO, 2013; EPPO, 2014|
|-Anhui||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Fujian||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Guangdong||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Guangxi||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Guizhou||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Hebei||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Heilongjiang||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Henan||Present||Song and Wang, 1993; CABI/EPPO, 2013; EPPO, 2014|
|-Hubei||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Hunan||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Jiangsu||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Jiangxi||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Jilin||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Liaoning||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Nei Menggu||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Shaanxi||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Shandong||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Shanxi||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Sichuan||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Tibet||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Yunnan||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Zhejiang||Present||CABI/EPPO, 2013; EPPO, 2014|
|Georgia (Republic of)||Present, few occurrences||EPPO, 2018|
|Japan||Present||Native||Goto et al., 2002; CABI/EPPO, 2013; EPPO, 2014|
|-Honshu||Present||CABI/EPPO, 2013; EPPO, 2014|
|Korea, DPR||Present||EPPO, 2014|
|Korea, Republic of||Present||Native||CABI/EPPO, 2013; EPPO, 2014|
|Taiwan||Present||Native||CABI/EPPO, 2013; EPPO, 2014|
|Canada||Restricted distribution||CABI/EPPO, 2013; EPPO, 2014|
|-Alberta||Absent, intercepted only||CABI/EPPO, 2013; EPPO, 2014|
|-Ontario||Present, few occurrences||Fogain and Graff, 2011; CABI/EPPO, 2013; EPPO, 2014|
|-Quebec||Absent, intercepted only||Fogain and Graff, 2011; CABI/EPPO, 2013; EPPO, 2014|
|USA||Widespread||Introduced||CABI/EPPO, 2013; EPPO, 2014|
|-Alabama||Present, few occurrences||CABI/EPPO, 2013; EPPO, 2014|
|-Arizona||Present, few occurrences||CABI/EPPO, 2013; EPPO, 2014|
|-California||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Connecticut||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Delaware||Present||Introduced||Invasive||Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-District of Columbia||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Florida||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Georgia||Present, few occurrences||CABI/EPPO, 2013; EPPO, 2014|
|-Idaho||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Illinois||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Indiana||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Iowa||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Kansas||Present||Tindall et al., 2012; CABI/EPPO, 2013; EPPO, 2014|
|-Kentucky||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Maine||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Maryland||Present||Introduced||Invasive||Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-Massachusetts||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Michigan||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Minnesota||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Mississippi||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Missouri||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Montana||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Nebraska||Present, few occurrences||CABI/EPPO, 2013; EPPO, 2014|
|-Nevada||Present||CABI/EPPO, 2013; EPPO, 2014|
|-New Hampshire||Present||CABI/EPPO, 2013; EPPO, 2014|
|-New Jersey||Present||Introduced||Invasive||Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-New Mexico||Present||CABI/EPPO, 2013; EPPO, 2014|
|-New York||Present||CABI/EPPO, 2013; EPPO, 2014|
|-North Carolina||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Ohio||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Oregon||Present, few occurrences||Introduced||Invasive||Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-Pennsylvania||Present, few occurrences||Introduced||mid 1990s||Hoebeke and Carter, 2003; Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-Rhode Island||Present||CABI/EPPO, 2013; EPPO, 2014|
|-South Carolina||Present||Introduced||Invasive||Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-South Dakota||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Tennessee||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Texas||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Utah||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Vermont||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Virginia||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Washington||Present||CABI/EPPO, 2013; EPPO, 2014|
|-West Virginia||Present||Introduced||Invasive||Oregon Department of Agriculture, 2005; CABI/EPPO, 2013; EPPO, 2014|
|-Wisconsin||Present||CABI/EPPO, 2013; EPPO, 2014|
|-Wyoming||Present||CABI/EPPO, 2013; EPPO, 2014|
|Austria||Restricted distribution||EPPO, 2018|
|France||Restricted distribution||Introduced||CABI/EPPO, 2013; Callot and Brua, 2013; EPPO, 2014|
|Germany||Restricted distribution||Heckmann, 2012; CABI/EPPO, 2013; EPPO, 2014||Single specimen found.|
|Greece||Present||EPPO, 2014; Milonas and Partsinevelos, 2014|
|Hungary||Present, few occurrences||EPPO, 2014; Papp et al., 2014; Vétek et al., 2014|
|Italy||Restricted distribution||Introduced||CABI/EPPO, 2013; Pansa et al., 2013; EPPO, 2014; Maistrello et al., 2014; EPPO, 2018||Emilia-Romagna, Lombardy, Piedmont|
|-Sardinia||Present, few occurrences||EPPO, 2018|
|Liechtenstein||Present, few occurrences||Arnold, 2009; CABI/EPPO, 2013; EPPO, 2014|
|Romania||Restricted distribution||Macavei et al., 2015; EPPO, 2018|
|Russian Federation||Restricted distribution||Mityushev, 2016; EPPO, 2018|
|-Southern Russia||Restricted distribution||EPPO, 2018|
|Serbia||Restricted distribution||EPPO, 2018|
|Slovakia||Present, few occurrences||Hemala and Kment, 2017; EPPO, 2018|
|Slovenia||Present, few occurrences||EPPO, 2018|
|Spain||Present, few occurrences||EPPO, 2018|
|Switzerland||Restricted distribution||Introduced||Wyniger and Kment, 2010; CABI/EPPO, 2013; Haye and Wyniger, 2013; EPPO, 2014; EPPO, 2018|
|Guam||Present, few occurrences||EPPO, 2014; Moore, 2014|
|New Zealand||Absent, intercepted only||EPPO, 2014|
History of Introduction and SpreadTop of page
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).
IntroductionsTop of page
|Introduced to||Introduced from||Year||Reason||Introduced by||Established in wild through||References||Notes|
|Natural reproduction||Continuous restocking|
|Canada||North America||2010||Hitchhiker (pathway cause)||Yes||No||Fogain and Graff (2011); Gariepy et al. (2013)||Accidental introduction.|
|France||2012||Hitchhiker (pathway cause)||Yes||No||Callot and Brua (2013)||Accidental introduction.|
|Germany||2011||Hitchhiker (pathway cause)||No||No||Heckmann (2012)||Accidental introduction.|
|Italy||2012-2013||Hitchhiker (pathway cause)||No||No||Haye and Wyniger (2013)||Accidental introduction.|
|Liechtenstein||Switzerland||2007||Hitchhiker (pathway cause)||No||No||Arnold (2009); Gariepy et al. (2013)||Accidental introduction.|
|Switzerland||2007||Hitchhiker (pathway cause)||Yes||No||Gariepy et al. (2013); Wermelinger et al. (2008)||Accidental introduction.|
|USA||China||2001||Hitchhiker (pathway cause)||No||No||Hoebeke and Carter (2003); Xu et al. (2013)||Specimens collected in 1998. Accidental introduction.|
Risk of IntroductionTop of page
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 ListTop of page
|Terrestrial – Managed||Cultivated / agricultural land||Principal habitat||Harmful (pest or invasive)|
|Cultivated / agricultural land||Principal habitat||Productive/non-natural|
|Managed forests, plantations and orchards||Principal habitat||Harmful (pest or invasive)|
|Managed forests, plantations and orchards||Principal habitat||Productive/non-natural|
|Disturbed areas||Secondary/tolerated habitat||Productive/non-natural|
|Rail / roadsides||Secondary/tolerated habitat||Productive/non-natural|
|Urban / peri-urban areas||Principal habitat||Harmful (pest or invasive)|
|Urban / peri-urban areas||Principal habitat||Productive/non-natural|
|Buildings||Principal habitat||Harmful (pest or invasive)|
|Terrestrial ‑ Natural / Semi-natural||Natural forests||Present, no further details||Natural|
Hosts/Species AffectedTop of page
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 AffectedTop of page
|Abelia grandiflora (Glossy abelia)||Caprifoliaceae||Other|
|Abelmoschus esculentus (okra)||Malvaceae||Other|
|Acer campestre (field maple)||Aceraceae||Other|
|Acer japonicum (full-moon maple)||Aceraceae||Wild host|
|Acer macrophyllum (broadleaf maple)||Aceraceae||Other|
|Acer negundo (box elder)||Aceraceae||Other|
|Acer palmatum (Japanese maple)||Aceraceae||Other|
|Acer pensylvanicum (striped maple)||Aceraceae||Other|
|Acer platanoides (Norway maple)||Aceraceae||Other|
|Acer rubrum (red maple)||Aceraceae||Other|
|Acer saccharinum (silver maple)||Aceraceae||Other|
|Acer saccharum (sugar maple)||Aceraceae||Wild host|
|Aesculus glabra (Texas buckeye)||Hippocastanaceae||Other|
|Ailanthus altissima (tree-of-heaven)||Simaroubaceae||Other|
|Amaranthus caudatus (Love-lies-bleeding)||Amaranthaceae||Other|
|Amelanchier laevis (Allegheny serviceberry)||Rosaceae||Other|
|Antirrhinum majus (snapdragon)||Scrophulariaceae||Other|
|Arctium minus (common burdock)||Asteraceae||Other|
|Armoracia rusticana (horseradish)||Brassicaceae||Other|
|Asimina triloba (Pawpaw-apple)||Annonaceae||Wild host|
|Basella alba (Malabar spinach)||Basellaceae||Other|
|Betula nigra (river birch)||Betulaceae||Other|
|Betula papyrifera (paper birch)||Betulaceae||Other|
|Betula pendula (common silver birch)||Betulaceae||Other|
|Brassica oleracea (cabbages, cauliflowers)||Brassicaceae||Other|
|Capsicum annuum (bell pepper)||Solanaceae||Other|
|Caragana arborescens (Siberian pea-tree)||Fabaceae||Other|
|Carpinus betulus (hornbeam)||Betulaceae||Other|
|Carya illinoinensis (pecan)||Juglandaceae||Other|
|Carya ovata (shagbark hickory)||Juglandaceae||Other|
|Celastrus orbiculatus (Asiatic bittersweet)||Salacia||Other|
|Celosia argentea (celosia)||Amaranthaceae||Other|
|Celtis (nettle tree)||Ulmaceae||Other|
|Celtis occidentalis (hackberry)||Ulmaceae||Other|
|Cephalanthus occidentalis (common buttonbush)||Rubiaceae||Other|
|Cercidiphyllum japonicum (katsura)||Cercidiphyllaceae||Other|
|Cercis canadensis (eastern redbud)||Fabaceae||Wild host|
|Chenopodium (Goosefoot)||Chenopodiaceae||Wild host|
|Citrus junos (yuzu)||Rutaceae||Main|
|Cladrastis kentukea (American yellowwood)||Fabaceae||Other|
|Cornus florida (Flowering dogwood)||Cornaceae||Wild host|
|Cornus racemosa (gray dogwood)||Cornaceae||Other|
|Cornus sericea (redosier dogwood)||Cornaceae||Other|
|Crataegus monogyna (hawthorn)||Rosaceae||Wild host|
|Cucumis sativus (cucumber)||Cucurbitaceae||Other|
|Cucurbita pepo (marrow)||Cucurbitaceae||Other|
|Diospyros kaki (persimmon)||Ebenaceae||Main|
|Elaeagnus angustifolia (Russian olive)||Elaeagnaceae||Wild host|
|Elaeagnus umbellata (autumn olive)||Elaeagnaceae||Wild host|
|Ficus carica (common fig)||Moraceae||Other|
|Fraxinus americana (white ash)||Oleaceae||Wild host|
|Fraxinus pennsylvanica (downy ash)||Oleaceae||Wild host|
|Ginkgo biloba (kew tree)||Ginkgoaceae||Other|
|Gleditsia triacanthos (honey locust)||Fabaceae||Other|
|Glycine max (soyabean)||Fabaceae||Main|
|Hamamelis virginiana (Virginian witch-hazel)||Hamamelidaceae||Wild host|
|Hibiscus rosa-sinensis (China-rose)||Malvaceae||Other|
|Humulus lupulus (hop)||Cannabaceae||Other|
|Ilex aquifolium (holly)||Aquifoliaceae||Other|
|Juglans nigra (black walnut)||Juglandaceae||Wild host|
|Juniperus virginiana (eastern redcedar)||Cupressaceae||Other|
|Koelreuteria paniculata (golden rain tree)||Sapindaceae||Other|
|Lagerstroemia indica (Indian crape myrtle)||Lythraceae||Other|
|Larix kaempferi (Japanese larch)||Pinaceae||Other|
|Ligustrum sinense (Chinese privet)||Oleaceae||Wild host|
|Liquidambar styraciflua (Sweet gum)||Hamamelidaceae||Other|
|Liriodendron tulipifera (tuliptree)||Magnoliaceae||Wild host|
|Lonicera (honeysuckles)||Caprifoliaceae||Wild host|
|Lonicera tatarica (Tatarian honeysuckle)||Caprifoliaceae||Wild host|
|Lythrum salicaria (purple loosestrife)||Lythraceae||Wild host|
|Magnolia grandiflora (Southern magnolia)||Magnoliaceae||Other|
|Mahonia aquifolium (Oregongrape)||Berberidaceae||Wild host|
|Malus baccata (siberian crab apple)||Rosaceae||Other|
|Malus domestica (apple)||Rosaceae||Main|
|Mimosa (sensitive plants)||Fabaceae||Other|
|Morus alba (mora)||Moraceae||Other|
|Paulownia tomentosa (paulownia)||Scrophulariaceae||Wild host|
|Phaseolus lunatus (lima bean)||Fabaceae||Other|
|Phaseolus vulgaris (common bean)||Fabaceae||Other|
|Pisum sativum (pea)||Fabaceae||Main|
|Prunus avium (sweet cherry)||Rosaceae||Main|
|Prunus cerasifera (myrobalan plum)||Rosaceae||Other|
|Prunus laurocerasus (cherry laurel)||Other|
|Prunus mume (Japanese apricot tree)||Rosaceae||Other|
|Prunus persica (peach)||Rosaceae||Main|
|Prunus serotina (black cherry)||Rosaceae||Wild host|
|Prunus serrulata (Japanese flowering cherry)||Rosaceae||Other|
|Prunus subhirtella (weeping Japanese cherry)||Rosaceae||Other|
|Pyrus calleryana (bradford pear)||Rosaceae||Other|
|Pyrus communis (European pear)||Rosaceae||Other|
|Pyrus pyrifolia (Oriental pear tree)||Rosaceae||Other|
|Quercus alba (white oak)||Fagaceae||Other|
|Quercus coccinea (scarlet oak)||Fagaceae||Other|
|Quercus robur (common oak)||Fagaceae||Other|
|Quercus rubra (northern red oak)||Fagaceae||Other|
|Rhamnus cathartica (buckthorn)||Rhamnaceae||Wild host|
|Robinia pseudoacacia (black locust)||Fabaceae||Wild host|
|Rosa canina (Dog rose)||Rosaceae||Other|
|Rosa multiflora (Multiflora rose)||Rosaceae||Wild host|
|Rosa rugosa (rugosa rose)||Rosaceae||Other|
|Rubus (blackberry, raspberry)||Rosaceae||Other|
|Rubus idaeus (raspberry)||Rosaceae||Other|
|Salix (willows)||Salicaceae||Wild host|
|Sassafras albidum (common sassafras)||Lauraceae||Wild host|
|Solanum lycopersicum (tomato)||Solanaceae||Other|
|Solanum melongena (aubergine)||Solanaceae||Other|
|Solanum nigrum (black nightshade)||Solanaceae||Other|
|Sorbus americana (American mountainash)||Rosaceae||Wild host|
|Sorbus aria (whitebeam)||Rosaceae||Other|
|Tilia americana (basswood)||Tiliaceae||Other|
|Tilia cordata (small-leaf lime)||Tiliaceae||Other|
|Tilia tomentosa (silver lime)||Tiliaceae||Other|
|Tsuga canadensis (eastern hemlock)||Pinaceae||Wild host|
|Ulmus americana (American elm)||Ulmaceae||Other|
|Ulmus parvifolia (lacebark elm)||Ulmaceae||Other|
|Ulmus procera (english elm)||Ulmaceae||Other|
|Vaccinium corymbosum (blueberry)||Ericaceae||Other|
|Vitis riparia (riverbank grape (USA))||Vitaceae||Wild host|
|Vitis vinifera (grapevine)||Vitaceae||Other|
|Zea mays (maize)||Poaceae||Other|
|Zea mays subsp. mays (sweetcorn)||Poaceae||Other|
Growth StagesTop of page Flowering stage, Fruiting stage
SymptomsTop of page
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/SignsTop of page
|Fruit / abnormal shape|
|Fruit / discoloration|
|Fruit / external feeding|
|Fruit / lesions: scab or pitting|
|Leaves / external feeding|
|Leaves / necrotic areas|
|Whole plant / external feeding|
Biology and EcologyTop of page
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.
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.
H. halys is a vector of Paulownia witches' broom (Yuan, 1984).
ClimateTop of page
|C - Temperate/Mesothermal climate||Preferred||Average temp. of coldest month > 0°C and < 18°C, mean warmest month > 10°C|
|Cf - Warm temperate climate, wet all year||Preferred||Warm average temp. > 10°C, Cold average temp. > 0°C, wet all year|
|Cs - Warm temperate climate with dry summer||Tolerated||Warm average temp. > 10°C, Cold average temp. > 0°C, dry summers|
|Cw - Warm temperate climate with dry winter||Tolerated||Warm temperate climate with dry winter (Warm average temp. > 10°C, Cold average temp. > 0°C, dry winters)|
Latitude/Altitude RangesTop of page
|Latitude North (°N)||Latitude South (°S)||Altitude Lower (m)||Altitude Upper (m)|
Air TemperatureTop of page
|Parameter||Lower limit||Upper limit|
|Absolute minimum temperature (ºC)||-17|
Natural enemiesTop of page
|Natural enemy||Type||Life stages||Specificity||References||Biological control in||Biological control on|
|Anastatus||Parasite||Eggs||not specific||Hou et al., 2009|
|Arma chinensis||Predator||not specific|
|Bogosia||Parasite||Adults||Kawada and Kitamura, 1992|
|Gryon japonicum||Parasite||Eggs||not specific|
|Isyndus obscurus||Predator||Kawada and Kitamura, 1992; Oda et al., 1982|
|Misumenops tricuspidatus||Predator||not specific||Qiu, 2007|
|Ophiocordyceps nutans||Pathogen||Sasaki et al., 2012|
|Trissolcus flavipes||Parasite||Qiu, 2007; Qiu et al., 2007; Zhang et al., 1993|
|Trissolcus itoi||Parasite||not specific||Arakawa and Namura, 2002|
|Trissolcus japonicus||Parasite||to species||Kawada and Kitamura, 1992; Li and Liu, 2004; Talamas et al., 2013; Yang et al., 2009|
|Trissolcus mitsukurii||Parasite||not specific||Arakawa and Namura, 2002|
Notes on Natural EnemiesTop of page
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 DispersalTop of page
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 CausesTop of page
|Crop production||Deliberate dispersal during search for host plant resources. Moves between agricultural crops throug||Yes||Yes||Nielsen et al., 2013; Wiman et al., 2013b|
|Disturbance||Association with distrurbed habitat and population hot spots.||Yes|
|Forestry||Deliberate dispersal during search for overwintering sites.||Yes||Yes|
|Hitchhiker||Frequently occurs due to H. halys seeking sheltered overwintering sites.||Yes||Yes||Hoebeke and Carter, 2003|
|Self-propelled||Deliberate dispersal to seek host plants or overwintering sites.||Yes||Yes||Wiman et al., 2013b|
Pathway VectorsTop of page
|Aircraft||Accidentally transported by aircraft.||Yes||Yes|
|Bulk freight or cargo||Frequently can occur accidentally due to H. halys seeking sheltered overwintering sites.||Yes||Yes||Hoebeke and Carter, 2003|
|Clothing, footwear and possessions||Wintering adults are often found in clothing and other possessions that may be transported.||Yes||Yes|
|Containers and packaging - non-wood||Frequently can occur accidentally due to H. halys seeking sheltered overwintering sites.||Yes||Yes|
|Land vehicles||Adults found in vehicles, especially when seeking shelter in the autumn.||Yes||Yes|
|Luggage||Overwintering adults are sometimes found in clothing or other possessions in luggage and transported||Yes||Yes|
Plant TradeTop of page
|Plant parts liable to carry the pest in trade/transport||Pest stages||Borne internally||Borne externally||Visibility of pest or symptoms|
|Bark||adults||Pest or symptoms usually visible to the naked eye|
|Leaves||adults; eggs; nymphs||Yes||Pest or symptoms usually visible to the naked eye|
|Plant parts not known to carry the pest in trade/transport|
|Fruits (inc. pods)|
|Growing medium accompanying plants|
|Stems (above ground)/Shoots/Trunks/Branches|
|True seeds (inc. grain)|
Wood PackagingTop of page
|Wood Packaging liable to carry the pest in trade/transport||Timber type||Used as packing|
|Solid wood packing material with bark||cardboard, plywood boards||Yes|
Impact SummaryTop of page
ImpactTop of page
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 ImpactTop of page
Large numbers of H. halys can become a nuisance when they seek shelter in houses during autumn and winter months.
Risk and Impact FactorsTop of page Invasiveness
- 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
- 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
- Highly likely to be transported internationally accidentally
- Difficult to identify/detect as a commodity contaminant
- Difficult/costly to control
Detection and InspectionTop of page
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/ConditionsTop of page
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 ControlTop of page
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.
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 NeedsTop of page
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.
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ContributorsTop of page
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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