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

Pentatomidae)
Kevin B. Rice,1,2 Chris J. Bergh,3 Erik J. Bergmann,4 Dave J. Biddinger,1 Christine Dieckhoff,5 Galen Dively,4 Hannah
Fraser,6 Tara Gariepy,7 George Hamilton,8 Tim Haye,9 Ames Herbert,10 Kim Hoelmer,11 Cerruti R. Hooks,4 Ashley Jones,4
Greg Krawczyk,1 Thomas Kuhar,12 Holly Martinson,4 William Mitchell,1 Anne L. Nielsen,8 Doug G. Pfeiffer,12
Michael J. Raupp,4 Cesar Rodriguez-Saona,8 Peter Shearer,13 Paula Shrewsbury,4 P. Dilip Venugopal,4 Joanne Whalen,14
Nik G. Wiman,13 Tracy C. Leskey,15 and John F. Tooker1
1
Department of Entomology, The Pennsylvania State University, University Park, PA.
2
Corresponding author, e-mail: kbr10@psu.edu.
3
Alson H. Smith Jr. Agricultural Research and Extension Center, Virginia Polytechnic Institute and State University, Winchester, VA.
4
Department of Entomology, University of Maryland, College Park, MD.
5
Agricultural Research Service, United States Department of Agriculture, Newark, DE.

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6
Agriculture Development Branch, Ontario Ministry of Agriculture and Food and Ministry of Rural Affairs, Vineland, ON.
7
Southern Crop Protection and Food Research Centre, Agriculture and Agri-Food Canada, London, ON.
8
Department of Entomology, Rutgers University, New Brunswick, NJ.
9
Centre for Agriculture and Biosciences International, Delemont, CH.
10
Tidewater Agriculture research and Extension Center, Virginia Polytechnic Institute and State University, Suffolk, VA.
11
Agricultural Research Service, United States Department of Agriculture, Montpellier, France.
12
Department of Entomology, Virginia Polytechnic Institute and State University, Blacksburg, VA.
13
Department of Horticulture, Oregon State University, Corvallis, OR.
14
Department of Entomology and Wildlife Ecology, University of Delaware, Newark, DE.
15
Agricultural Research Service, United States Department of Agriculture, Kearneysville, WV.

J. Integ. Pest Mngmt. 5(3): 2014; DOI: http://dx.doi.org/10.1603/IPM14002

ABSTRACT. Brown marmorated stink bug, Halyomorpha halys Stål, is an invasive, herbivorous insect species that was accidentally
introduced to the United States from Asia. First discovered in Allentown, PA, in 1996, H. halys has now been reported from at least 40
states in the United States. Additional invasions have been detected in Canada, Switzerland, France, Germany, Italy, and Lichtenstein,
suggesting this invasive species could emerge as a cosmopolitan pest species. In its native range, H. halys is classified as an outbreak pest;
however, in North America, H. halys has become a major agricultural pest across a wide range of commodities. H. halys is a generalist
herbivore, capable of consuming ⬎100 different species of host plants, often resulting in substantial economic damage; its feeding
damage resulted in US$37 million of losses in apple in 2010, but this stink bug species also attacks other fruit, vegetable, field crop, and
ornamental plant species. H. halys has disrupted integrated pest management programs for multiple cropping systems. Pesticide appli-
cations, including broad-spectrum insecticides, have increased in response to H. halys infestations, potentially negatively influencing
populations of beneficial arthropods and increasing secondary pest outbreaks. H. halys is also challenging because it affects homeowners
as a nuisance pest; the bug tends to overwinter in homes and outbuildings. Although more research is required to better understand the
ecology and biology of H. halys, we present its life history, host plant damage, and the management options available for this invasive pest
species.

Key Words: biological control, chemical control, crop damage, invasive, Pentatomidae

Origin and Spread as early as 1999 (Hamilton 2009). Since then, H. halys has spread
Halyomorpha halys (Stål), brown marmorated stink bug, is a polypha- throughout the state (Nielsen et al. 2013). By 2005, H. halys had been
gous stink bug native to China, Japan, Korea, and Taiwan (Hoebeke detected in other parts of the mid-Atlantic United States (Delaware,
and Carter 2003, Lee et al. 2013a) and is believed to have been Maryland, Virginia, and West Virginia) and in California and Oregon
introduced into the United States from a single introduction originat- (G. H., unpublished data). In 2010, H. halys population abundance in
ing from Beijing, China (Xu et al. 2014). The first known H. halys mid-Atlantic states exploded (Leskey et al. 2012b), resulting in in-
populations were reported in 1996 from Allentown, PA, but went creased awareness by the agricultural sector and the general public,
misidentified as the native brown stink bug, Euschistus servus (Say), which generated detections in additional states.
until 2001, when Karen Bernhard (Lehigh County Cooperative Ex- Today, H. halys is present in at least 41 states and the District of
tension, Allentown, PA) speculated that the stink bug entering Allen- Columbia (Leskey et al. 2014). A potential detection in Arkansas is
town residences and buildings in the mid- to late fall was not E. servus. awaiting verification and a Colorado find remains unofficial (Leskey
Based on Ms. Bernhard’s hunch, specimens were sent to Cornell and Hamilton 2013). In Delaware, Maryland, New Jersey, Pennsyl-
University for identification, resulting in the first confirmed report of vania, Virginia, and West Virginia, H. halys is currently considered a
an established H. halys population in the United States (Hoebeke and severe agricultural and nuisance pest, an agricultural and nuisance pest
Carter 2003). in New York, North Carolina, Ohio, and Tennessee, and a nuisance-
Following confirmation of its identity, reports of H. halys through- only pest in California, Michigan, Indiana, New Hampshire, Massa-
out Pennsylvania began to occur. In New Jersey, a review of uniden- chusetts, Connecticut, and Rhode Island (Leskey and Hamilton 2012).
tified stink bugs collected from black light traps maintained by the In Oregon and Washington, brown marmorated stink bug has recently
Rutgers Cooperative Extension Vegetable Integrated Pest Manage- shifted from being a nuisance-only pest to an agricultural pest (Wiman
ment Program revealed that H. halys was present in Phillipsburg, NJ, et al. 2014).
2 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 5, NO. 3

Pest Status in Other Invaded Regions Description of Life Stages

Given its expanding range in the United States and its tendency to White and black banding on their antenna and abdominal edges
stowaway in cargo, it is no surprise that H. halys has spread beyond distinguishes adults H. halys from native stink bug species in the United
Asia and the invaded range of the United States. Based on bioclimatic States (Fig. 1). Claspers located on the last ventral abdominal segment
variables, conditions appear favorable for establishment and spread of differentiate adult males from females (Fig. 2). Females lay egg masses
this pest species in Europe and North America, as well as parts of on the underside of leaves and freshly deposited eggs are light green, and
Australia and New Zealand (Zhu et al. 2012). Over the last several turn white (Fig. 3) before hatching. Brown marmorated stink bugs have
years, H. halys adults have been sporadically intercepted or collected five instars. First instars (Fig. 4) have black heads, red eyes, and reddish
singly on three continents [Europe: Liechtenstein (Arnold 2009), orange abdomens with black markings; the neonates emerge 3– 6 d after
oviposition, and feed from eggshells, possibly acquiring endosymbionts
Germany (Heckmann 2012), France (Callot and Brua 2013), Italy
(Taylor et al. 2014). Second instars (Fig. 5) emerge 3–5 d after first
(European and Mediterranean Plant Protection Organization [EPPO]
instars, disperse from egg masses, and feed on host plants. Third instars
2013); Australia: Australia (Walker 2009), New Zealand (Harris
are dark brown (Fig. 6) and molt 12–13 d after eggs hatch, whereas fourth
2010); North America: Canada (Fogain and Graff 2011)]. Established (Fig. 7) and fifth instars (Fig. 8) emerge 19 –20 and 26 –27 d after egg
populations, however, have only been confirmed outside the United hatch, respectively. Development from egg to adult requires 538 DD
States in Canada (H. F. and T. G., unpublished data) and Switzerland (32–35 d at 30°C) with a minimum and maximum developmental thresh-

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(Wermelinger et al. 2008), and evidence suggests potential establish- old of 14 and 35°C (Nielsen et al. 2008a).
ment in the Alsace region of France (EPPO 2013).
Canada. The first documented occurrence of H. halys in Canada Biology
was in 1993 when a specimen was intercepted in British Columbia In southern China, H. halys is multivoltine with four to six gen-
from a shipment originating in Asia. Since then, additional intercep- erations (Hoffmann 1931). In the mid-Atlantic United States where
tions from shipments originating in China, Japan, Korea, and the population densities are currently the greatest, it has one to two
generations per year (Nielsen et al. 2008a). Nonreproductive adults
United States have been recorded sporadically in the provinces of
overwinter in artificial and natural shelters, and gradually emerge
British Columbia, Ontario, and Quebec (Fogain and Graff 2011).
from these sites beginning in April. Termination of diapause does not
Numerous homeowner reports in Ontario beginning in 2010 strongly
occur immediately upon leaving overwintering sites and is likely
suggested presence of an established population. In July 2012, pres- driven by photoperiod (threshold of 14.8 –15.5 h; Yanagi and Hagi-
ence of eggs, nymphs, and adults in Hamilton, ON, confirmed official hara 1980). Photoperiod, however, also interacts with temperature,
establishment of breeding populations of H. halys in Canada (H. F. and once the daylength threshold has been met, it may override
and T. G., unpublished data). Numbers of H. halys collected from photoperiod requirements for diapause termination. Females re-
residential locations in greater Toronto and Hamilton continue to quire an additional 148 DD before becoming reproductively mature
increase, and homeowner discoveries have been reported in new (Nielsen et al. 2008a). Reproductively mature H. halys can disperse
locations within the province. Despite regular scouting and monitoring into crops, but hardwood trees and shrubs may be important inter-
efforts in 2012 and 2013, H. halys has not been found in agricultural mediate hosts after leaving overwintering sites, before crop inva-
crops in Canada and remains a minor household and nuisance pest in sion. Females are polyandrous and typically lay clusters of 28 eggs
urban areas around Toronto and Hamilton (H. F. and T. G., unpub- (mean ⫽ 26.08 ⫾ 0.31) on the underside of leaves (Kawada and
lished data). Although H. halys has only been found in natural habitats Kitamura 1983, Nielsen et al. 2008a). Brown marmorated stink bug
(primarily on invasive buckthorn, Rhamnus spp.), the proximity of can complete development on peach (Prunus persica (L.)) and tree
these populations to major fruit-growing regions (e.g., Niagara Pen- of heaven (Ailanthus altissima [Miller] Swingle) but has ⬎100 host
insula) has raised serious concerns about its potential movement into plants that include tree fruit, small fruit, vegetable, ornamental and
agricultural crops. field crop species (Leskey et al. 2012a, 2013a).
Switzerland (and Other Parts of Europe). The first established pop-
ulation of H. halys in Europe was officially documented in 2007 in
Zurich, Switzerland (Wermelinger et al. 2008); however, photo-
graphic evidence suggests this species was present in the region as
early as 2004 (T. H., unpublished data). Between 2007 and 2010,
homeowner reports of H. halys in Zurich increased exponentially
(Mueller et al. 2011), and now it has expanded its range to include the
cantons of Basel-Stadt, Basel-Land, Aargau, Bern, St. Gallen, Schaff-
hausen, and Ticino (Wyniger and Kment 2010, Haye and Wyniger
2013). The original population in Zurich appears to have been the
source of H. halys in these cantons, rather than new introductions
coming from Asia or North America (Gariepy et al. 2014). Similarly,
the well-established Swiss populations are likely sources of H. halys
occurrences in neighboring Liechtenstein (Arnold 2009), Germany
(Heckmann 2012), France (Callot and Brua 2013), and Italy (EPPO
2013). Although established in Switzerland for at least 9 yr, H. halys
remains mostly an urban and household pest; however, 38 local host
plant species (native and otherwise) have been identified as hosts for
H. halys (Haye and Wyniger 2013) and some ornamental species can
harbor heavy infestations (Wermelinger et al. 2008). Moreover, some
evidence suggests that H. halys may become an agricultural pest in the
near future; fruit-bearing trees in private gardens in Zurich have been
injured (T. H. and T. G., unpublished data) and peppers (Capsicum Fig. 1. Adult brown marmorated stink bug. (Photo by Ian
annuum L.) in Aargau have sustained economic damage (Sauer 2012). Grettenberger, Penn State University.)
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Fig. 2. Female (left) and male (right) brown marmorated stink bugs. Males have claspers on the terminal abdominal segment. (Photo by Ian
Grettenberger.)

Fig. 4. First instar brown marmorated stink bugs. (Photo by Ian

Grettenberger.)
Brown marmorated stink bug is well-known as a nuisance pest; large
Fig. 3. Brown marmorated stink bug eggs. (Photo by Ian numbers of adults often invade human-made structures to overwinter
Grettenberger.) inside protected environments (Inkley 2012). This behavior is rather
unique among Pentatomidae and may improve overwintering survivor-
ship of H. halys relative to other species such as Nezara viridula L.
The strong capacity of H. halys to disperse at landscape scales (Kiritani 2007). Similar to other pentatomid species, H. halys also will
throughout the year may aid its polyphagous behavior. In flight-mill overwinter, at least in the mid-Atlantic region, in natural settings, includ-
studies, tethered adults from wild populations flew an average of 2 km ing dry crevices in dead, standing trees with thick bark, particularly oak
in 24 h (T.C.L, unpublished data). With field observations, H. halys (Quercus spp.) and locust (Robinia spp.; Lee et al. 2014b). For trees with
flies about 3 m/s along a straight line from take-off to landing (Lee et overwintering H. halys, searches of 20% of above-ground tree area
al. 2013b). Flight also occurs at night as adults seek out mates or yielded approximately six adults per tree (Lee et al. 2014b).
alternative food sources; therefore, black light traps can be effective Black light traps attracting foraging H. halys adults can be used to
monitoring tools for landscape-level movement of H. halys. Although document season-long, landscape-level populations (Nielsen et al. 2013).
flight activity varies through the year, a large peak in black light Brown marmorated stink bug response to light-based stimuli is affected
captures tends to occur at 685 DD (Nielsen et al. 2013). Some of the by intensity and wavelength under both laboratory and field conditions,
longest flights may occur at the onset of the winter aggregation period with adults most attracted to white, blue, and black (UV) stimuli (Leskey
in the late summer and fall (Wiman et al. 2014). Nymphs actively et al. 2014). During summer months, large aggregations of adults have
disperse by walking and second through fifth instars show strong been observed at outdoor dusk-to-dawn light sources. Nymphs have
tendencies in the laboratory and field to move (Lee et al. 2014a). never been documented responding to light-based stimuli.
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Fig. 5. Second instar brown marmorated stink bugs. (Photo by Ian
Grettenberger.)

Fig. 7. Fourth instar brown marmorated stink bug. (Photo by Ian

Grettenberger.)

Fig. 6. Third instar brown marmorated stink bug. (Photo by Ian

Grettenberger.)

Ecology
Chemical Ecology. Brown marmorated stink bug males produce a
recently identified two-component aggregation pheromone, (3S,6S,7R,
10S)-10,11-epoxy-1-bisabolen-3-ol and (3S,6S,7R,10R)-10,11-epoxy-
1-bisabolen-3-ol (Khrimian et al. 2014, Zhang et al. 2013; U.S. patent
WO2013090703 A1). Aggregation pheromones differ from sex pher-
omones in a few important ways. First, aggregation pheromones tend
Fig. 8. Fifth instar brown marmorated stink bug. (Photo by Ian
to elicit responses from all mobile life stages, presumably identifying
Grettenberger.)
a resource such as a host plant, mate, or overwintering site. Secondly,
aggregation pheromones tend to bring respondents to an area, but
unlike sex pheromones with which responders will generally attempt region, sensitivity to the aggregation pheromone deployed in traps
to locate the exact point source of the stimulus, responders to aggre- coincides with initial dispersal from overwintering sites and peak
gation pheromones will be attracted to and may be arrested by stimuli population densities are typically detected from late July to late
several meters away from the stimulus source. In the mid-Atlantic September. Brown marmorated stink bugs also respond to the kairo-
SEPTEMBER 2014 RICE ET AL.: BROWN MARMORATED STINK BUG ECOLOGY AND MANAGEMENT 5

mone 2,4,6, E,E,Z methyl decatrienoate, the aggregation pheromone

of Plautia stali Scott (Heteroptera: Pentatomidae), which was used for
many of the initial pheromone trials in the United States, though this
stimulus is only attractive beginning in early August (Aldrich et al.
2009, Nielsen et al. 2011, Leskey et al. 2012a). The 2,4,6, E,E,Z
methyl decatrienoate pheromone also has proven to be a strong syn-
ergist for the aggregation pheromone of H. halys, increasing sensitiv-
ity of baited traps season-long (Weber et al. 2014).
Host Plants. Brown marmorated stink bug has ⬎100 reported host
plants (Bergmann et al. 2013). It is common in woodlots and is widely
considered an arboreal species. Host plants such as A. altissima,
Paulownia tomentosa (Thunberg) Steudel, Acer spp., and Fraxinus
spp. appear important for supporting populations, particularly during
initial invasions into a region (Nielsen and Hamilton 2009b). The
ability to disperse among host plants seems important for development
and survival of H. halys, which can complete development exclusively

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on A. altissima and P. tomentosa; however, despite often inflicting Fig. 9. Brown marmorated stink bug damage on lima bean pods
heavy late-season injury, H. halys survivorship on apple (Malus do- (Phaseolus lunatus L.). (Photo by Thomas Kuhar, Virginia Polytechnic
mestica Borkh) is low (Funayama 2002, 2004). Many economically Institute and State University.)
important crop species are hosts for H. halys including peach, apple,
filbert nut (Corylus avellana L.), pear (Pyrus communis L.), wheat
(Triticum aestivum L.), grapes (Vitis spp.), small fruit, field corn (Zea
mays L.), soybean (Glycine max L. Merrill), sorghum (Sorghum
bicolor L.), and many vegetable crops such as sweet corn, tomato
(Solanum lycopersicum L.), pepper, okra (Abelmoschus esculentus
(L.) Moench), and eggplant (Solanum melongena L.). On these plant
species, H. halys prefers to feed upon reproductive structures. In
soybean, for instance, they do not colonize the crop in large numbers
until the R3 stage and peak population abundance occurs at R5 when
the pods begin to fill (Nielsen et al. 2011). Brown marmorated stink
bugs appear to move readily among crops and crop phenology may
drive its movement.
Invasion Ecology. The close association of H. halys with humans
can distress some residents (Inkley 2012), but it also can prompt
volunteer citizen scientists to help track pest invasions. Many univer-
sities, such as Rutgers, Penn State, and Oregon State University have
developed websites with varying levels of verification to track citizen
reports of H. halys. In some instances, reports to these databases have
become the first sightings in a state.
Lights can attract H. halys adults as they disperse across the
landscape (see Biology). In New Jersey, a network of black light traps
located at farms throughout the state has been used to track the spread
of H. halys. These traps attract males and females equally well and
their captures can detect movement of early dispersers into tree fruit, Fig. 10. Damage on tomato resulting from brown marmorated
an event coinciding with sexual maturation of female bugs. Data from stink bug feeding. (Photo by Thomas Kuhar.)
this statewide network of traps indicated a 75% annual population
increase from 2004 to 2011, which equated to an annual invasion of
2.8 farms (Nielsen et al. 2013). These findings illustrate the scale of able portion of the crop. Feeding injury to beans (Phaseolus spp.) may
the H. halys invasion and emphasize that the bug is an efficient result in scarred, faded sunken areas, and deformed pods (Fig. 9);
disperser. Further analyses of data from this network suggests that similar pod injury can occur when the bugs feed upon okra. Injury to
landscape features in New Jersey may be associated with H. halys fleshy fruit, like tomatoes and peppers, will produce white spongy
population hotspots (Wallner et al. 2014). Early in the invasion, there areas on the skin (Figs. 10 and 11) and internal tissue damage (Fig.
was a strong association of H. halys population abundance with urban 12). Along with reduced quality of marketable produce, feeding injury
environments. Railroads and wetlands appear to facilitate population to vegetables may reduce fruit set and subsequent yield by causing
spread and populations eventually settle in agricultural regions (Wall- abortion of flower buds and young fruiting bodies. In addition to direct
ner et al. 2014). This analysis supports the hypothesis that the agri- damage, the feeding stylets of H. halys can also transmit pathogenic
culture– urban interface may drive populations, with urban settings bacteria or yeasts, such as Eremothecium coryli, which can cause fruit
providing overwintering habitat and increased overwintering survival, rot (Fig. 13). Under heavy infestations, losses ⬎50% due to H. halys
while agricultural crops provide resources for development and pop- damage have been common. Among vegetables, sweet corn, okra, and
ulation increase (see Hufbauer et al. 2013). pepper appear to be highly preferred host plant species for adult
colonization and reproduction (Kuhar et al. 2012f). Eggplant and
Host Plant Species, Economic Damage, and Sampling or green bean (Phaseolus vulgaris L.) are also suitable for oviposition
Scouting Procedure and nymphal development. Tomato appears to be less suitable for H.
Vegetables. Brown marmorated stink bug can cause significant halys reproduction, but can suffer severe fruit damage, particularly in
injury to a wide range of vegetable crop species when bugs insert their late August. Brown marmorated stink bugs will also feed on other
feeding stylets into plant fruiting bodies, which are often the market- vegetable species such as asparagus (Asparagus officinalis L.), cucur-
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Fig. 11. Brown marmorated feeding damage on bell pepper. (Photo
by Peter Shearer, Oregon State University.)

Fig. 13. Indirect damage (bacterial rot) on tomato caused by brown

marmorated stink bug. (Photo by Doug Inkley, National Wildlife
Federation.)

Fig. 12. Peeled tomato revealing corky tissue formation caused by

brown marmorated stink bug feeding. (Photo by Shelby Fleischer,
Penn State University.)

bits, or brassicas, but to a lesser degree and depending on their

proximity to more preferred vegetables.
In the mid-Atlantic region, H. halys attacks the majority of vege-
table crops present from late July to October (Kuhar et al. 2012a). In
mixed vegetable plantings, or on small farms with diverse crops, over
the growing season H. halys adults and nymphs often move signifi-
cantly among crops, depending upon the relative attractiveness of each
Fig. 14. Brown marmorated stink bug damage on apple. (Photo by
crop. Vegetable crops nearest overwintering shelters or directly bor-
Tracy Leskey, Agricultural Research Service, United States Department
dering wooded areas are at the highest risk of H. halys attack. Late in
of Agriculture.)
the season, vegetables bordering a more attractive host plant such as
soybeans may suffer less H. halys damage than those that do not.
Fruit. In Asia, H. halys is an occasional outbreak pest of tree fruit attacks peaches, nectarines (Prunus persica (L.) Batsch), apples, and
(Lee et al. 2013a). Damage to apples (Fig. 14) and pears in the United Asian pears (Pryrus pyrifolia Nakai).
States first appeared in Allentown, PA, and Pittstown, NJ, in 2006 In the mid-Atlantic United States in 2008 –2009, increasing H.
(Nielsen and Hamilton 2009a). In orchards where it establishes, H. halys populations caused late-season damage to fruit crops (Leskey
halys quickly becomes the predominant stink bug species and, unlike and Hamilton 2010a), but H. halys was not a widely recognized pest
native stink bug species, is a season-long pest of tree fruit (Nielsen and until late in the 2010 season. Damage from H. halys feeding during the
Hamilton 2009a, Leskey et al. 2012a). In particular, H. halys heavily 2010 outbreak resulted in US$37 million in losses to mid-Atlantic
SEPTEMBER 2014 RICE ET AL.: BROWN MARMORATED STINK BUG ECOLOGY AND MANAGEMENT 7

In wine grapes, H. halys establishment raised concern about stink

bugs tainting grape juice. Some preliminary data indicate that the taint
does not survive fermentation and bottling, while others indicate it
may (Mohekar et al. 2014, Tomasino et al. 2014). Brown marmorated
stink bug uses grapevines as reproductive hosts, and both nymphs and
adults feed upon grape clusters (Pfeiffer et al. 2012). This feeding
results in necrosis and deformation at the feeding site, and many bugs
may be seen on individual clusters. Action thresholds need to be
determined.
Field Crops. The main field crop species colonized thus far by H.
halys are corn and soybeans. There is some evidence that stink bug
populations can accumulate in fields of wheat, cotton (Gossypium
hirsutum L.), hops (Humulus lupulus L.), sorghum, and possibly
sunflower (Helianthus annuus L.). This latter crop is relatively scarce
in the mid-Atlantic region where stink bugs are currently so abundant,
but the host plant species is being explored as a trap crop for H. halys

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in vegetable production, so it seems reasonable to suspect that large
fields of sunflower would be attractive to H. halys. Thus far, H. halys
nymphs have mainly been discovered in corn and soybeans, suggest-
ing these crops are attractive to adult bugs and suitable for oviposition
and nymphal development. Based on population abundance at differ-
ent times of the season, it seems that H. halys colonizes corn fields
when ears are developing (July), and later in the year bug populations
Fig. 15. Damage from brown marmorated stink bug on immature develop in soybean fields when pods form and seeds are filling
peach. (Photo by Tracy Leskey.) (August and September). This knowledge can increase the efficiency
of scouting by allowing scouts to focus only on those fields in
apples alone (American/Western Fruit Grower 2011) with some stone susceptible growth stages. Further, given that H. halys populations are
fruit growers losing ⬎90% of their crop (Leskey and Hamilton worse in crop fields adjacent to woods (see below), it appears that
2010b). wooded areas are sources of bugs, but research has yet to explore the
Feeding injury from H. halys to stone fruit, principally peaches movement of bugs among habitats or how this movement might be
(Fig. 15) and nectarines, causes depressed or sunken areas that may exploited for management.
become cat-faced as fruit develops. On pome fruit, including apples Field Corn. Brown marmorated stink bug populations are highest in
and pears, feeding results in indented depressions on the surface and field corn during ear formation, specifically during the milk (R3
corky spots in the flesh of fruit. Feeding may also cause fruiting growth stage) and dough (R4) stages. The bugs appear to feed pri-
structures to abort prematurely (Nielsen and Hamilton 2009a). In- marily on developing kernels by piercing the husk, and the resulting
creases in targeted insecticide applications, particularly postbloom, damage discolors and shrink individual kernels (Fig. 16). Some evi-
has mitigated H. halys damage in orchard crops (Leskey et al. 2012a). dence from Pennsylvania suggests that feeding by H. halys on late-
Residual activity of most insecticides on fruit and foliage against H. stage, vegetative corn plants can abort ear production, but more
halys is very short, necessitating narrower application intervals of research is needed to explore this potential phenomenon. Populations
broad-spectrum materials to maintain fresher residues (Lee et al. 2012, of bugs on corn plants, particularly in field edges, can often exceed
Leskey 2012c). Increased reliance on chemical control has increased three bugs per ear, but in some fields, it is not uncommon to find as
secondary pest outbreaks that are typically controlled by natural
enemies (Leskey et al. 2012c).
Brown marmorated stink bug has the potential to feed and repro-
duce in small fruit crops such as blueberries (Vaccinium spp.), rasp-
berries (Rubus idaeus L.), grapes, and blackberries (Rubus spp.; Les-
key and Hamilton 2010b); however, little is known about its economic
impact in these crops. Studies are underway in the United States to
determine its potential impact, spatial distribution, and seasonal abun-
dance in small fruit crops. In the northeastern United States, blueberry
growers first found H. halys during the late-season in 2010 and many
growers in New Jersey have since reported it in and around structures
and houses. Contamination risks are a great concern for blueberry
growers who mechanically harvest and then sell their berries to
processors or ship them to other countries and regions within the
United States. During 2011–2012, H. halys population abundance in
New Jersey blueberry farms remained low and did not require control
measures.
In caneberries (raspberries and blackberries), stink bug species
cause two types of injury. In early season, H. halys feeding may cause
death of buds, though this apparent damage needs to be further
explored. In late season, H. halys attacks mature berries, inserting their
stylets between drupelets, and possibly feeding on the receptacle; this
feeding causes discoloration and collapse of individual drupelets. Fig. 16. Damage to field corn by brown marmorated stink bug,
Droppings produced by feeding stink bugs can add an unpleasant taste which feed through the husk on individual kernel. (Photo by Galen
to berries. No damage by H. halys has been observed in cranberries. Dively, University of Maryland.)
8 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 5, NO. 3

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Fig. 17. Brown marmorated stink bug nymphs feeding on an ear of Fig. 18. “Stay-green” syndrome caused by brown marmorated
corn. (Photo by Ronald Hoover, Penn State University.) stink bug feeding on the edge of a soybean field near Lancaster, PA.
(Photo by Jeff Graybill, Penn State Extension.)
many as 20 bugs on some ears (Fig. 17). Brown marmorated stink bug
population in field corn is typically highest within 12 m of field edges
and decrease significantly toward the centers of fields. The highest
population densities tend to be in corn fields adjacent to wooded areas,
but significant populations can also occur in fields in proximity to
alfalfa (Medicago sativa L.) and sorghum fields, and even buildings;
fields with the fewest bugs tend to be adjacent to open areas (D. V.,
unpublished data).
Research from 2012 suggests that adult infestations occurring at
the R3 growth stage caused significantly lower yields compared with
infestations at R4. For a similar experiment conducted in 2011, the
trend was in the same direction yet analyses did not reveal a signif-
icant yield reduction between the timing of infestations. In both years,
H. halys feeding affected grain quality, with infestations occurring at
growth stage R2 (blister stage) and R3 resulting in the greatest number
of damaged kernels per ear (Cissel, unpublished data). Additional
research needs to evaluate the impact of H. halys feeding on yield
when sustained infestations occur during the entire grain fill period.
Because feeding damage by the brown stink bug was correlated with
increased aflatoxin levels in corn (Ni et al. 2011), the influence of H.
halys feeding damage on aflatoxin development should also be ex-
plored. While economic thresholds for field corn are still being de-
veloped, it must be acknowledged that effectively treating infested
corn fields can be challenging because of the height of mid- to
late-season corn plants and the amount of foliage between the top of Fig. 19. Flattened soybean pods caused by brown marmorated stink bug
the plant and the ear (Reisig 2011). feeding directly on seeds through the pod. (Photo by Jeff Graybill.)
Soybean. Brown marmorated stink bug populations tend to invade
soybean fields during the R4 (fully elongated pods) to R6 (fully stink bug tends to feed on developing seeds directly through the pod.
developed seed) plant growth stages. Before these stages, bug popu- As with field corn, H. halys populations typically remain on field
lations can be found but numbers tend to be lower. Brown marmorated edges, especially those bordering wooded areas, corn fields, and
SEPTEMBER 2014 RICE ET AL.: BROWN MARMORATED STINK BUG ECOLOGY AND MANAGEMENT 9

on native stink bugs indicates that the most susceptible stages of wheat
development are the milk and soft dough stages (Viator et al. 1983).
This coincides with the stage of the wheat fields when H. halys adults
have been observed in wheat (J. W., unpublished data). In the absence
of a more preferred host species, wheat may be attractive to H. halys,
though more studies are needed to determine if H. halys poses a
significant risk. Similar to soybean and field corn, we observed higher
densities of H. halys in wheat field edges bordering wooded areas.
Ornamental Plants in the Eastern United States. Host Plant
Breadth. Before its arrival in the United States, H. halys was known
to feed on a wide variety of woody ornamental plants in Asia (Hoe-
beke and Carter 2003). This included both gymnosperms such as
Cryptomeria (Funayama 2005) and angiosperms such as Malus (Fu-
nayama 2004) and Paulownia (Hiruki 1999). In one of the earliest
accounts of host use in the United States, 50 woody tree and shrub
species were identified as hosts for H. halys (Bernon 2004). This list
Fig. 20. Relationship between brown marmorated stink bug

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was broadened and researchers noted marked temporal changes in
density and yield difference in treated and untreated soybean zones.
patterns of host use as H. halys moved among woody plants in various
stages of development (Nielsen and Hamilton 2009b). In general, they
buildings, while low infestations tend to be in field edges bordering detected correlations between the abundance of H. halys nymphs and
open areas (D. V., unpublished data). Field edge-only insecticide the presence of maturing pods and fruit. Of the nine woody trees
applications have been promoted to growers and repeat posttreatment and shrubs studied, all supported populations of H. halys (Nielsen and
field visits have verified that these treatments can be effective in Hamilton 2009b). The most current compilation of hosts in the United
managing infestations. In late summer and early autumn, H. halys States includes ⬎120 species of woody trees and shrubs and at least
populations on the edges of soybean fields often leave a signature three herbaceous perennials growing in protected culture and as wild
because their feeding often causes a “stay green” syndrome in which hosts in the invaded range (Bergmann et al. 2013). This list will
attacked plants exhibit significantly delayed senescence relative to continue to expand. Ongoing surveys at three commercial ornamental
uninfested portions of the field. Thus, in the mid-Atlantic region in plant nurseries in central Maryland between 2011 and 2012 revealed
September and October it is not uncommon to find yellowing fields that H. halys used 174 of the 200 cultivars of woody trees and shrubs
with bright green edges (Fig. 18). It should be noted, however, that as hosts (E. B., unpublished data). Plants with the greatest abundances
other factors (e.g., plant pathogens and nutrient stress) can cause of H. halys in protected culture and on wild hosts included cultivars
similar “stay-green” effects, but there is an obvious abundance of in the genera Acer, Ailanthus, Catalpa, Cercis, Ilex, Magnolia, Malus,
green edges in areas with large H. halys populations. Brown mar- Mimosa, Morus, Paulownia, Platanus, Prunus, and Syringa (Berg-
morated stink bug feeding on developing seeds during the R5 growth mann et al. 2013, E. B., unpublished data). Hosts include those used
stage causes the greatest crop injury, resulting in shriveled seeds and solely for feeding and those which also used for feeding and ovipo-
flatten pods (Fig. 19), damage similar to that caused by native stink sition.
bug species. Recent field cage-based research on the influence of H. Direct and Indirect Damage. In Japan, H. halys is a pest on cedar and
halys on soybean yield showed that a density of four stink bugs per cypress farms (Funayama 2005) and is reported to injure various shade
0.3 m of row decreased seed quality (Owens et al. 2013). This study
did not detect a significant relationship between H. halys densities and
yield loss (Owens et al. 2013). However, an ongoing field study in the
mid-Atlantic region comparing yields of pyrethroid-treated and un-
treated R4 stage plots indicated that one H. halys per 0.3 m of row
resulted in a loss of 375 g per ha or 2.2 bushels per acre (Fig. 20);
(G. D., unpublished data). Brown marmorated stink bug feeding on R6
or R7 stage soybeans appears less likely to cause yield loss, but can
decrease soybean quality, which can influence the value of the grain.
When completed, these additional studies will increase our under-
standing of the exact relationship between H. halys densities and yield
loss. Further, a field cage study showed that feeding injury caused by
H. halys is similar to that caused by native stink bug species, indi-
cating that all stink bug species can be combined for determining the
economic threshold for a field. Peak abundance of native stink bugs
occurs at similar reproductive stages in soybean (Herbert and Toews
2012). While still under development, tentative economic thresholds
are one to two H. halys per row foot, or five stink bugs per 15 sweeps
of a net. We recommend scouting field edges 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 can be effective, if applied at the right time.
Wheat. We have seen populations of adult H. halys develop in the
milk and soft dough stages of wheat fields (J. W., unpublished data).
Given the apparent preference of H. halys for developing seeds of Fig. 21. Brown marmorated stink bugs feed through the bark of
other grains, it seems likely that bugs are feeding on developing seeds, ornamental trees releasing sap that stains the tree attracting ants
though this, and any influence of their feeding on yield and any and stinging Hymenoptera. (Photo by Michael Raupp, University of
associated economic thresholds, remains to be established. Research Maryland.)
10 JOURNAL OF INTEGRATED PEST MANAGEMENT VOL. 5, NO. 3

trees (Hoebeke and Carter 2003). In China, H. halys damage orna- sampling methods allow for comparison of H. halys densities among
mental plants such as Hibiscus, Celosia, and Paulownia (Hoebeke and plant species and changes in densities over time.
Carter 2003). In the mid-Atlantic United States in 2010, the population
abundance of H. halys grew enormously. With this population explo- Biological Control
In Asia, several natural enemies of H. halys have been identified
sion, H. halys became an important pest and economic threat to
including arthropod predators, dipteran parasitoids, and hymenopteran
ornamental woody and herbaceous plants in commercial nurseries and
egg parasitoids (Qiu 2007, Qiu et al. 2007, Leskey et al. 2012b,
landscapes via direct (Leskey et al. 2012b) and potential indirect
Leskey et al. 2013). Predators found in Asia attack all life stages of H.
feeding damage (Hoebeke and Carter 2003). By midsummer 2010,
halys, while parasitoids use adult and egg stages as hosts. The highest
direct feeding damage by H. halys was first noted in Maryland as
levels of parasitism reported in Asia ranged from 63 to 85% for
disfigured fruits and wilted foliage of Malus, Crateagus, and
hymenopteran egg parasitoids in the genera Trissolcus (Zhang et al.
Amelanchier (Leskey et al. 2012b). Brown marmorated stink bug
1993, Qiu 2007, Qiu et al. 2007, Yang et al. 2009, Talamas et al. 2013)
feeding on foliage can result in stippling damage, which then pro-
and Anastatus (Hou et al. 2009). Pathogens may also contribute to H.
gresses to a brown and scab-like appearance (Hoebeke and Carter
halys mortality, including Ophiocordyceps nutans (Hypocreales:
2003). In August of 2010, H. halys became very abundant in Maryland
Phiocordycipitaceae) (Sasaki et al. 2012) and an intestinal virus of P.
and West Virginia nurseries and landscapes on trunks of trees such as stali (Hemiptera: Pentatomidae) (Nakashima et al. 1998).
Platanus, Acer, and Ulmus. Brown marmorated stink bugs demon-

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In North America, field surveys conducted primarily in the eastern
strate a unique habit of feeding through the bark (Fig. 21), a behavior United States have identified several natural enemies associated with
not reported for this species and is unusual for stink bugs in general H. halys (Biddinger et al. 2012). Chewing and sucking predators of H.
(Panizzi 1997, Martinson et al. 2013). The resulting injury included halys eggs, nymphs, and adults have been identified in the following
copious sap flow, fluxes, and discolored bark at feeding sites. Several families: Anthocoridae, Asilidae, Chrysopidae, Coccinellidae, Cra-
species of native ants and wasps fed on these exudates, which had high bronidae, Forficulidae, Geocoridae, Mantidae, Melyridae, and Redu-
sugar concentrations; thus, it appears that bark feeding by H. halys viidae. In addition, spiders have been observed feeding on all life
facilitate native Hymenoptera by creating a novel feeding niche (Mar- stages of H. halys (Kawanda and Kitamura 1992, Lan-fen 2010,
tinson et al. 2013). Bark feeding has since been observed on several Leskey et al. 2012b). Mortality of H. halys eggs owing to predation
additional host species (E. B., unpublished data). Wilting and death of and other unknown causes reached 40 –70% in corn and soybean plots
herbaceous perennials due to heavy feeding damage by H. halys has in Pennsylvania, Maryland, and New Jersey, averaged 23% in orna-
been reported on a small number of species (Leskey et al. 2012b). mental nurseries surveyed in Maryland, and predators alone caused
In addition to direct damage from feeding, H. halys may also cause ⬇25% egg mortality in Pennsylvania orchards (Biddinger et al. 2012,
indirect damage. In Asia, H. halys is a vector of witches’ broom C.R.R.H., D.J.B., and P.M.S., unpublished data). Coccinellidae (par-
disease, which can greatly alter growth patterns of afflicted plants ticularly Harmonia axyridis Pallas) and Forficulidae (earwigs) are the
(Bak et al. 1993, Hiruki 1999, Yu and Zhang 2009). The disease– primary predators in orchard systems surveyed in Pennsylvania (Bid-
vector potential of H. halys has raised concerns, but to date has not dinger et al. 2012, D.J.B., unpublished data). In addition, late H. halys
been reported on ornamental plants in the United States. instars composed the majority (95%) of nest provisioning by sand
Sampling and Monitoring. Ornamental environments consist of a wasps (Crabronidae) in 40 nests surveyed in Pennsylvania, New
diversity of plant species of varying shapes and sizes, which makes Jersey, and Maryland (D.J.B., unpublished data).
standardized sampling somewhat challenging. The most common A wide-spread survey of parasitoids using sentinel (e.g., laboratory
methods of quantifying H. halys activity on ornamentals has been the reared) egg masses found telenomine platygastrids to be the predom-
use of standardized beat sampling methods (Nielsen and Hamilton inant parasitoids emerging from H. halys eggs in the mid-Atlantic
2009b) and timed visual counts (E. B., unpublished data). These United States and Oregon (Table 1). Rates of parasitism recorded

Table 1. North American natural enemies of Halyomorpha halys reported from field surveys (D.J.B., C.R.R.H., A.L.J., T.P.K., P.M.S.,
N.G.W., and J. W., unpublished data)
Order Family (subfamily if known) Species H. halys life stages attacked Locality
Araneae Arachnida Eggs, nymphs, adults Maryland, Oregon, Pennsylvania
Coleoptera Coccinellidae Harmonia axyridis Eggs Pennsylvania
Dermaptera Forficulidae Eggs Pennsylvania
Diptera Tachinidae Trichopoda pennipes Adult, late instars Pennsylvania
Hemiptera Anthocoridae Orius sp. Eggs Maryland
Geocoridae Geocoris sp. Eggs, nymphs Maryland, Oregon, Pennsylvania
Reduviidae Arilus cristatus Eggs, nymphs, adults Maryland, Oregon, Pennsylvania
Hymenoptera Crabronidae Astata unicolor Adults, late instars Pennsylvania
Astata bicolor Late instars Oregon
Bicyrtes quadrafaciata Late instars Pennsylvania
Encyrtidae Ooencyrtus sp. Eggs Delaware, Maryland
Eupelmidae Anastatus mirabilis Eggs Delaware, Maryland
Anastatus pearsalli Eggs Delaware, Maryland, Pennsylvania
Anastatus reduvii Eggs Delaware, Maryland, Delaware
Platygastridae (Scelioninae) Gryon obesum Eggs Maryland
Platygastridae (Telenominae) Telenomus podisi Eggs Maryland, Pennsylvania
Telenomus utahensis Eggs Virginia
Trissolcus brochymenae Eggs Delaware, Maryland, Virginia
Trissolcus edessae Eggs Delaware, Maryland, Virginia
Trissolcus euschisti Eggs Delaware, Maryland, Oregon
Trissolcus thyantae Eggs Virginia
Trissolcus utahensis Eggs Oregon
Mantodea Mantidae Tenodera sinensis Nymphs, adults Maryland
Neuroptera Chrysopidae Unidentified larvae Eggs, early nymphs Maryland, Oregon, Pennsylvania
SEPTEMBER 2014 RICE ET AL.: BROWN MARMORATED STINK BUG ECOLOGY AND MANAGEMENT 11

during these surveys were low (⬍1% to 11%) and highly variable insecticides applied and provides a reservoir for natural enemies in the
between locations and years. In addition, a tachinid fly, Trichopoda center of the field. Tree fruits are vulnerable to H. halys feeding injury
pennipes F. (Diptera: Tachinidae), parasitized H. halys adults. Para- through the fruiting period, with some stone fruit (e.g., peaches) being
sitism rates for T. pennipes averaged 1–5% (up to 20% in some particularly susceptible from the early stages of fruit development
locations) but emergence rates were negligible (D.J.B. and K.A.H., onward. Given the long time between fruit set and maturity of many
unpublished data). In apple orchards in Pennsylvania, Telenomus tree fruit crops, especially late season apple and peach varieties,
podisi Ashmed was the most common species found to attack H. halys growers have been forced to use certain insecticides in the postbloom
egg masses (D.J.B., unpublished data). In 2012, parasitism of naturally period, such as pyrethroids, that had not been used previously. This
occurring egg masses in Maryland nurseries averaged 31% (P.M.S. has resulted in increased incidences of secondary pest outbreaks,
and A.L.J., unpublished data). Notably, species of parasitoids fre- especially woolly apple aphid and scale insect species. An assessment
quently found emerging from H. halys eggs in field crop and vegetable of the distribution of H. halys injury to late-season apple varieties at
systems were absent or rarely detected in ornamental nurseries. Con- harvest revealed that, in general, fruit on trees border rows adjacent to
versely, the most common parasitoids found during egg surveys in woodlands suffered more injury than those in the orchard interior
ornamental nurseries were either absent or rare in field crop and (C. B., unpublished data). Further, fruit from the top of trees received
vegetable plots (C.R.R.H., P.M.S., and A.L.J., unpublished data). more injury than lower scaffolds in the canopy. These observations
Thus, predators and parasitoids inflicting mortality on H. halys eggs suggest possible benefits from more aggressive H. halys management

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appear to be highly variable depending on the ecosystem (Leskey et al. at orchard-block perimeters and adequate covering tree tops with
2012b, 2013), which suggests the local composition of host plant sprays.
species and landscape features may influence the species composition Developing novel insecticides that target stink bugs with less
of indigenous natural enemies associated with H. halys. impact on beneficial insects would significantly advance grower ca-
Based upon their success suppressing H. halys populations in Asia, pabilities of combating H. halys, and of course fit better into integrated
several Trissolcus species are currently being evaluated in the United pest management programs. If chemical control is truly needed for a
States quarantine facilities as potential agents for field releases. In given situation, entomologists and crop consultants should recom-
field crop systems, experiments are being conducted to determine the mend use of effective selective chemical tools over more disruptive,
potential use of insectary plants to enhance the effectiveness of the broad-spectrum insecticides. Frequent rotation of insecticide classes
local natural enemy fauna in managing H. halys and indigenous stink should minimize potential insecticide resistance.
bug species. Ultimately, classical biological control using parasitoids Future studies may explore an “attract and kill” strategy for man-
native to Asia and conservation biological control to enhance the aging H. halys on select plants at field or orchard borders baited with
effectiveness of introduced and indigenous natural enemies may pro- lures designed to attract and aggregate them in spatially precise
vide the most promising long-term solutions for landscape-level re- locations. By only treating these plants or rows with insecticide, the
duction of H. halys populations (Leskey et al. 2012b). overall amount of material applied against H. halys would be reduced.

Chemical Control Acknowledgments

We thank the three anonymous reviewers for helpful comments
Since the widespread outbreak of H. halys in the mid-Atlantic
United States in 2010, chemical control has been the most widely used that improved the quality of this manuscript. Funding for our brown
strategy for managing its damage to crops. Tree fruit growers in this marmoratted stink bug research comes from the U.S. Department of
region increased the number of insecticide applications, in some cases Agriculture–National Institute of Food and Agriculture–Specialty
nearly fourfold from 2010 to 2011 and have reduced the interval Crops Research Initiative 2011-51181-30937.
between sprays to maintain residues (Leskey et al. 2012a).
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