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4 October 2022

Halyomorpha halys (brown marmorated stink bug)

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)

Pictures

Halyomorpha halys (brown marmorated stink bug); adult feeding on a cherry.
Adult
Halyomorpha halys (brown marmorated stink bug); adult feeding on a cherry.
©CABI Switzerland - 2012
Halyomorpha halys (brown marmorated stink bug); adult feeding on cherries.
Adults
Halyomorpha halys (brown marmorated stink bug); adult feeding on cherries.
©CABI Switzerland - 2012
Halyomorpha halys (brown marmorated stink bug); egg mass.
Egg mass
Halyomorpha halys (brown marmorated stink bug); egg mass.
©CABI Switzerland - 2012
Halyomorpha halys (brown marmorated stink bug); newly emerged nymphs around egg mass.
Nymphs
Halyomorpha halys (brown marmorated stink bug); newly emerged nymphs around egg mass.
©CABI Switzerland - 2012
Halyomorpha halys (brown marmorated stink bug); various nymphal instars.
Nymphs
Halyomorpha halys (brown marmorated stink bug); various nymphal instars.
©CABI Switzerland - 2012
Halyomorpha halys (brown marmorated stink bug); natural enemy - parasitoid wasps (Trissolcus japonicus) parasitizing eggs of the brown marmorated stink bug.
Natural enemy
Halyomorpha halys (brown marmorated stink bug); natural enemy - parasitoid wasps (Trissolcus japonicus) parasitizing eggs of the brown marmorated stink bug.
©CABI Switzerland - 2012
Brown marmorated stink bugs feeding on cherries
CABI
Halyomorpha halys
Halyomorpha halys
Halyomorpha halys
Kurt Andreas
Halyomorpha halys
SONY DSC Halyomorpha halys
Halyomorpha halys
(c) 2011 e_monk rjSchuerger
Halyomorpha halys
CABI
An adult of the brown marmorated stinkbug feeds on an unripe cherry.
Halyomorpha halys
An adult of the brown marmorated stinkbug feeds on an unripe cherry.
CABI
Halyomorpha halys laying eggs
Halyomorpha halys
Halyomorpha halys laying eggs
CABI
Halyomorpha halys
CABI

Distribution

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Host Plants and Other Plants Affected

HostHost statusReferences
Abelia grandiflora (Glossy abelia)Other 
Abelmoschus esculentus (okra)Other 
Acer campestre (field maple)Other 
Acer circinatumOther 
Acer japonicum (full-moon maple)Wild host 
Acer macrophyllum (broadleaf maple)Other 
Acer negundo (box elder)Other
Gariepy et al. (2015)
Acer palmatum (Japanese maple)Other 
Acer pensylvanicum (striped maple)Other 
Acer platanoides (Norway maple)Other 
Acer rubrum (red maple)Other 
Acer saccharinum (silver maple)Other 
Acer saccharum (sugar maple)Wild host 
Acer tegmentosumOther 
Actinidia chinensis (Chinese gooseberry)Unknown
Andreadis et al. (2018)
Actinidia deliciosa (kiwifruit)Other 
Aesculus glabra (Texas buckeye)Other 
Ailanthus altissima (tree-of-heaven)Other
Jhalendra and Duncan (2017)
Amaranthus caudatus (love-lies-bleeding)Other 
Amelanchier laevis (Allegheny serviceberry)Other 
Amorpha fruticosa (false indigo-bush)Unknown
Gariepy et al. (2015)
Ion and Raluca (2019)
Antirrhinum majus (snapdragon)Other 
Arctium minus (common burdock)Other 
Armoracia rusticana (horseradish)Other 
Asimina triloba (Pawpaw-apple)Wild host 
Basella alba (malabar spinach)Other 
Betula nigra (river birch)Other 
Betula papyrifera (paper birch)Other 
Betula pendula (common silver birch)Other 
Brassica oleracea (cabbages, cauliflowers)Other 
Buxus sempervirens (common boxwood)Unknown
Ion and Raluca (2019)
Cannabis sativa (hemp)Unknown
Britt et al. (2019)
Capsicum annuum (bell pepper)Other
Vétek and Korányi (2017)
Caragana arborescens (Siberian pea-tree)Other
Nielsen and Hamilton (2009)
Carpinus betulus (hornbeam)Other
Gariepy et al. (2015)
Carya illinoinensis (pecan)Other 
Carya ovata (shagbark hickory)Other 
CatalpaOther 
Celastrus orbiculatus (Asiatic bittersweet)Other 
CelosiaOther 
Celosia argentea (celosia)Other 
Celtis (nettle tree)Other 
Celtis australis (European nettle wood)Unknown
Ion and Raluca (2019)
Celtis occidentalis (hackberry)Other 
Cephalanthus occidentalis (common buttonbush)Other 
Cercidiphyllum japonicum (katsura)Other 
Cercis canadensis (eastern redbud)Wild host 
Cercis siliquastrum (Judas tree)Unknown
Ion and Raluca (2019)
Chenopodium (Goosefoot)Wild host 
CitrusOther 
Citrus junos (yuzu)Main 
Cladrastis kentukea (American yellowwood)Other 
Cornus (Dogwood)Other
Macavei et al. (2015)
Cornus florida (Flowering dogwood)Wild host 
Cornus officinalisOther 
Cornus racemosa (gray dogwood)Other 
Cornus sanguinea (dogwood)Unknown
Ion and Raluca (2019)
Cornus sericea (redosier dogwood)Other 
CorylusOther 
Corylus avellana (hazel)Unknown
Murvanidze et al. (2018)
Crataegus laevigataOther 
Crataegus monogyna (hawthorn)Wild host 
Crataegus viridisOther 
Cucumis sativus (cucumber)Other 
Cucurbita pepo (marrow)Other 
Diospyros (malabar ebony)Unknown
Bariselli et al. (2016)
Diospyros kaki (persimmon)Main
Bariselli et al. (2016)
Elaeagnus angustifolia (Russian olive)Wild host
Nielsen and Hamilton (2009)
Elaeagnus umbellata (autumn olive)Wild host 
FicusOther 
Ficus carica (common fig)Other
Rot et al. (2018)
Forsythia suspensaOther 
Fraxinus americana (white ash)Wild host
Nielsen and Hamilton (2009)
Fraxinus excelsior (ash)Unknown
Ion and Raluca (2019)
Fraxinus pennsylvanica (downy ash)Wild host 
Ginkgo biloba (kew tree)Other 
Gleditsia triacanthos (honey locust)Other 
Glycine max (soyabean)Main
Nielsen and Hamilton (2009)
Rot et al. (2018)
Hamamelis virginiana (Virginian witch-hazel)Wild host 
Helianthus (sunflower)Other 
Helianthus tuberosus (Jerusalem artichoke)Unknown
Ion and Raluca (2019)
Hibiscus rosa-sinensis (Chinese rose)Other 
Hibiscus syriacus (shrubby althaea)Unknown
Rot et al. (2018)
Ion and Raluca (2019)
Humulus lupulus (hop)Other 
Ilex aquifolium (holly)Other 
Inula helenium (Elecampane)Unknown
Ion and Raluca (2019)
Juglans nigra (black walnut)Wild host 
Juniperus virginiana (eastern redcedar)Other 
Koelreuteria paniculata (golden rain tree)Other 
Lagerstroemia indica (Indian crape myrtle)Other 
Larix kaempferi (Japanese larch)Other 
Ligustrum sinense (Chinese privet)Wild host 
Liquidambar styraciflua (Sweet gum)Other 
Liriodendron tulipifera (tuliptree)Wild host
Ion and Raluca (2019)
Lonicera (honeysuckles)Wild host 
Lonicera tatarica (Tatarian honeysuckle)Wild host 
Lythrum salicaria (purple loosestrife)Wild host 
Magnolia grandiflora (Southern magnolia)Other 
Mahonia aquifolium (Oregongrape)Wild host 
Malus baccata (siberian crab apple)Other 
Malus domestica (apple)Main
Nielsen and Hamilton (2009)
Bariselli et al. (2016)
Ion and Raluca (2019)
Malus zumiOther 
Medicago sativa (lucerne)Unknown
Otavă et al. (2019)
Mimosa (sensitive plants)Other 
Morus (mulberrytree)Other 
Morus alba (mora)Other
Ion and Raluca (2019)
Olea europaeaUnknown
Rot et al. (2018)
Oryza sativa (rice)Unknown
Lupi et al. (2017)
Gyawali et al. (2019)
Paulownia tomentosa (paulownia)Wild host
Nielsen and Hamilton (2009)
Ion and Raluca (2019)
PhalaenopsisOther 
Phaseolus (beans)Other 
Phaseolus lunatus (lima bean)Other 
Phaseolus vulgaris (common bean)Other
Vétek and Korányi (2017)
Pisum sativum (pea)Main 
Prunus (stone fruit)Unknown
Zimmermann et al. (2018)
Prunus armeniaca (apricot)Unknown
Bariselli et al. (2016)
Prunus avium (sweet cherry)Main
Rot et al. (2018)
Prunus cerasifera (myrobalan plum)Other
Ion and Raluca (2019)
Prunus domestica (plum)Unknown
Bariselli et al. (2016)
Prunus laurocerasus (cherry laurel)Other 
Prunus mume (Japanese apricot tree)Other 
Prunus persica (peach)Main
Bariselli et al. (2016)
Jhalendra and Duncan (2017)
Zimmermann et al. (2018)
Rot et al. (2018)
Penca and Hodges (2018)
Prunus serotina (black cherry)Wild host 
Prunus serrulata (Japanese flowering cherry)Other 
Prunus subhirtella (weeping Japanese cherry)Other 
Pyracantha (Firethorn)Other 
Pyracantha coccinea (scarlet firethorn)Unknown
Ion and Raluca (2019)
Pyrus (pears)Other
Bariselli et al. (2016)
Nielsen and Hamilton (2009)
Pyrus calleryana (bradford pear)Other 
Pyrus communis (European pear)Other
Bariselli et al. (2016)
Rot et al. (2018)
Pyrus pyrifolia (Oriental pear tree)Other
Nielsen and Hamilton (2009)
Quercus alba (white oak)Other 
Quercus coccinea (scarlet oak)Other 
Quercus robur (common oak)Other 
Quercus rubra (northern red oak)Other 
Rhamnus cathartica (buckthorn)Wild host 
Robinia pseudoacacia (black locust)Wild host
Ion and Raluca (2019)
Rosa canina (Dog rose)Other 
Rosa multiflora (multiflora rose)Wild host 
Rosa rugosa (rugosa rose)Other
Nielsen and Hamilton (2009)
Rubus (blackberry, raspberry)Other 
Rubus idaeus (raspberry)Other 
Rubus phoenicolasiusOther 
Salix (willows)Wild host 
Sassafras albidum (common sassafras)Wild host 
Solanum lycopersicum (tomato)Other
Bariselli et al. (2016)
Solanum melongena (aubergine)Other 
Solanum nigrum (black nightshade)Other 
Solidago canadensis (Canadian goldenrod)Unknown
Ion and Raluca (2019)
Sorbus americana (American mountainash)Wild host 
Sorbus aria (whitebeam)Other 
SpiraeaOther 
Styrax japonicaOther 
Syringa pekinensisOther 
Tilia americana (basswood)Other 
Tilia cordata (small-leaf lime)Other 
Tilia tomentosa (silver lime)Other 
Tsuga canadensis (eastern hemlock)Wild host 
Ulmus americana (American elm)Other 
Ulmus parvifolia (lacebark elm)Other 
Ulmus procera (english elm)Other 
Vaccinium corymbosum (blueberry)Other 
ViburnumOther 
Viburnum prunifolium (blackhaw viburnum)Unknown
Nielsen and Hamilton (2009)
Viburnum trilobumUnknown
Nielsen and Hamilton (2009)
Vitis riparia (riverbank grape (USA))Wild host 
Vitis vinifera (grapevine)Other
Zimmermann et al. (2018)
Zea mays (maize)Other 
Zea mays subsp. mays (sweetcorn)Other 
Ziziphus sativaMain 

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

Symptom or signLife stagesSign or diagnosis
Plants/Fruit/abnormal shape  
Plants/Fruit/discoloration  
Plants/Fruit/external feeding  
Plants/Fruit/lesions: scab or pitting  
Plants/Leaves/external feeding  
Plants/Leaves/necrotic areas  
Plants/Whole plant/external feeding  

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.

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).

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Published online: 4 October 2022

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