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ABSTRACT
Efficacies of topical applications and dry residues of 9 common ready-to-use (RTU) insecti-
cides were evaluated against brown marmorated stink bug, Halyomorpha halys (Stål) (He-
miptera: Pentatomidae) at intervals of exposure of 1 and 48 h. Permethrin and acetamiprid,
were further evaluated to determine if H. halys recovered after an initial exposure. Topi-
cal applications of carbaryl, permethrin, insecticidal soap, petroleum oil, and acetamiprid,
and residues of permethrin and acetamiprid increased mortality of adults. Topical applica-
tions of spinosad, essential oils, carbaryl, permethrin, insecticidal soap, petroleum oil, and
acetamiprid, and residues of carbaryl, permethrin, and acetamiprid increased mortality of
nymphs. Topical applications of carbaryl, neem oil, insecticidal soap, and acetamiprid in-
creased egg mortality. In general, nymphs were more susceptible to insecticides than adults.
Adult H. halys recovered after exposure to topical applications, but not dry residues of per-
methrin. Clearly, several RTU insecticides in the marketplace demonstrated potential to
help gardeners manage H. halys.
Key Words: ready-to-use, brown marmorated stink bug, insecticide efficacy, IPM
RESUMEN
Palabras Clave: Insecticidas listos para usar, chinche hediondo marrón mármol, eficacia de
insecticidas, MIP
Stink bugs (Hemiptera: Pentatomidae) are & Hamilton 2011; Leskey et al. 2012ac). Further-
important pests of agricultural crops and orna- more, management of stink bugs can be challeng-
mental plants in the United States (McPherson ing with injury resulting despite the application
& McPherson 2000). Previous studies have dem- of broad-spectrum insecticides (Chyen et al. 1992;
onstrated that stink bug damage can be signifi- Leskey et al. 2012a).
cant to crops including tomato, soybean, peach, Halyomorpha halys is native to China, Japan,
and apples through feeding or the introduction of Korea, and Taiwan, but it has now been detected
pathogens (Underhill 1934; Emfinger et al. 2001; in 40 states and the District of Colombia since it
Nault & Speese 2002; Funayama 2004; Medrano was first discovered in North America near Al-
et al. 2007; Nielsen & Hamilton 2009b; Rucker lentown, PA in the late 1990’s (Hoebeke & Cart-
er 2003; Leskey et al. 2012c). Unfortunately, H. cation). Recent studies examined toxicities and
halys is polyphagous with over 300 reported host efficacies of several insecticides used in agro-
plants ranging from agricultural crops to orna- nomic systems for controlling stink bugs includ-
mental plants (Hoffman 1931; Hoebeke & Carter ing H. halys (Nielsen et al. 2008b; Kamminga et
2003; Bernon 2004; Nielsen & Hamilton 2009b). al. 2009; Rucker & Hamilton 2011; Leskey et al.
Furthermore, H. halys is a nuisance pest in resi- 2012ab; Leskey et al. 2013, Lee et al. in press).
dential settings due to its predilection to use hu- However, there is no published account of the effi-
man-made structures such as houses as overwin- cacy of common consumer-based RTU insecticides
tering sites where infestations can exceed 20,000 to control H. halys to date. The objectives of this
individuals (Watanabe et al. 1994; Hamilton et al. study were as follows. First, effects of topical ap-
2008; Sargent et al. 2011; Inkley 2012). plications and residues of RTU insecticides on the
Several recent studies conducted in the field mortality of H. halys nymphs and adults exposed
and laboratory in the United States provide in- for short (1 hour) and long (48 hour) intervals
sights into the utility of different classes of in- were evaluated. The effects of topical applica-
secticides to kill stink bugs and to mitigate their tions of RTUs to H. halys eggs were also evalu-
damage. Kamminga et al. (2009) focused on the ated. Previous reports of insecticidal activity
organic insecticides azadirachtin, pyrethrins, against H. halys noted adult stink bug recovery
and spinosad applied alone and in combination to after an initial exposure to insecticides (Nielsen
modify behavior, and to reduce feeding, survival, et al. 2008b; Leskey et al. 2012b). Two of the ac-
abundance, and damage caused by Chinavia hil- tive ingredients found in the RTUs in this study,
are (Say) and Euschistus servus (Say) in tomatoes permethrin and acetamiprid, were among those
and soybeans. Nielsen et al. (2008b) were among observed in previous studies of H. halys recovery
the first to evaluate organophosphate, pyre- (Nielsen et al. 2008b; Leskey et al. 2012b). An
throid, and neonicotinoid insecticides against dif- additional trial evaluated the ability of H. halys
ferent life stages of H. halys and found high levels adults to recover from exposure to topical applica-
of toxicity in several pyrethroids and neonicoti- tions of permethrin and acetamiprid. Information
noids. Leskey et al. (2012b) tested the lethality of from these studies will be useful in assisting con-
37 insecticides to adult H. halys under controlled sumers in their selection of RTU insecticides to be
laboratory conditions. Several classes of insecti- used against H. halys in home vegetable gardens.
cides including carbamates, organophosphates,
organochlorines, pyrethroids, and neonicotinoids MATERIALS AND METHODS
were highly lethal to H. halys after 7 days. Unfor-
tunately, 8 compounds most of which were pyre- Insect Source
throids declined in lethality over 7 days (Leskey et
al. 2012b). In a series of field trials, Leskey et al. Wild adults of H. halys were collected from
(2013) demonstrated that overwintered H. halys wheat, Triticum aestivum L., peach, Prunus per-
adults were more susceptible to insecticides than sica (L.), and sweet corn, Zea mays saccharata L.,
new adults of the summer generations and effica- from Jun 2011 through Oct 2012 in Central Mary-
cies of insecticide residues were less effective and land. Before use in bioassays, insects were placed
declined with time relative to freshly applied in- in plastic containers (30 × 19 × 20 cm, All Living
secticides. Lee et al. (in press) recently evaluated Things Critter Totes®) and fed organic nuts, fruits,
the efficacies of several insecticides approved for and vegetables including: raw peanut, Arachis hy-
organic production of specialty crops and found pogaea L (always provided) and carrots, Daucus
dry residues of several including potassium salts carota L.; green beans, Phaseolus vulgaris L.;
of fatty acids, spinosad, pyrethrins, pyrethrins + sweet corn, tomato, Solanum lycopersicum L. (in-
kaolin, and three experimental compounds to sig- dividually based on seasonal availability). Moist-
nificantly increase mortality of H. halys relative ened sponges were placed in small Petri dishes
to water controls. (Fisherbrand® 100 × 15 mm) as water sources.
In addition to the growing recognition that H. Food and water were changed twice weekly. Fil-
halys poses a serious threat to many crops, in- ter paper (Double Rings® #102, 12.5 cm diam) at-
quiries and complaints from the general public tached to one side of each container served as an
confirm its role as a serious pest in residential oviposition substrate. Egg masses were removed
vegetable gardens and landscapes (Sargent et al. daily and placed into separate Petri dishes (Fish-
2011; Inkley 2012). Homeowners regularly apply erbrand®, 100 × 15 mm) until they hatched. Once
premixed ready-to-use (RTU) insecticides to veg- hatched, nymphs were placed into plastic contain-
etables, fruits, shrubs, and trees to control insect ers described previously. Nymphs and adults were
pests (Baldwin et al. 2008; Matheny et al. 2009) fed and watered, as previously described. Contain-
and consumer interest and demand are high for ers were maintained in growth chambers kept at
methods of stink bug control including the use of 16:8 h L:D, 25 °C ± 1 °C, and 60 ± 10% RH. Second
insecticides for H. halys (J.H. Traunfeld, Univer- instar nymphs and egg masses were collected from
sity of Maryland Extension, personal communi- the colonies for use in insecticide trials.
TABLE 1. BRAND NAME, ACTIVE INGREDIENTS, AND VOLUMES OF READY TO USE PESTICIDE PRODUCTS APPLIED TO ADULTS, NYMPHS, AND EGGS OF HALYOMORPHA HALYS.
4.0 ± 0.1
4.1 ± 0.2
4.2 ± 0.1
4.0 ± 0.0
4.1 ± 0.2
4.1 ± 0.0
4.0 ± 0.1
4.2 ± 0.2
4.1 ± 0.1
4.8 ± 0.2
tail garden centers in metropolitan Washington,
DC during the first week of Jun in 2011. Each
product had a label indicating its use in control-
ling insect pests of vegetables, fruits, shrubs,
and trees. We chose insecticides representing
several different classes of compounds with dif-
ferent modes of action. Common names, brand
names, and concentrations of active ingredients
are listed in Table 1. Two of the 9 compounds,
one containing acetamiprid and one containing
AI concentration (%)1
carbaryl, identified stink bugs as a target pest,
0.00001125
label. To determine the volume applied of each
formulated RTU product used in our trials, be-
0.001
0.126
0.006
fore application, the applicator handle on each
0.02
1.0
2.0
0.9
spray bottle was fully compressed 30 times and
the spray was collected in a graduated cylinder. 100
After allowing the droplets to settle, the volume
of insecticide was measured to the nearest mL,
and the average volume delivered at each com-
pression was calculated by dividing the total
Rosemary, peppermint, thyme, & clove oil
Acetamiprid
From Aug 2011 to Sep 2012, trials were con- Topical Spray Trials
ducted with 500 nymphs and 500 adult H. halys
testing the dry residues of the 9 insecticides After 1 h of exposure, mortality of H. halys
used in the topical spray trials. Nine insecti- nymphs differed significantly among insecticidal
cides and distilled water were applied to the treatments (H = 40.8; df = 9; P < 0.0001). Insecti-
inside of each container and the container’s lid cidal mortality was least in nymphs treated with
using the methods described previously. Con- spinosad and essential oils. All other materials
tainers and lids were allowed to dry for 48 h produced relatively high (> 90%) mortality (Fig.
before cohorts of 5 adults and 5 nymphs were 1). Adults exposed for 1 h experienced signifi-
placed in each arena. Ten replicate cohorts were cantly different mortality among treatments (H
evaluated for each treatment. At 48 h after = 38.5; df = 9; P < 0.0001)(Fig. 1) with spinosad,
placement in the arena, all adults and nymphs horticultural oil, and capsaicin causing the least
were evaluated as in the topical spray trial. mortality and carbaryl, acetamiprid, and perme-
This study was repeated with an exposure in- thrin causing the most.
terval of 1 h rather than 48 h using 250 nymphs After 48 h of exposure, mortality of H. halys
and 250 adults assigned in cohorts of 5 to 10 nymphs and adults differed significantly among
treatments. All other procedures were followed insecticidal treatments (nymphs: H = 58.4; df = 9;
as described previously. P < 0.0001) (adults: H = 60.7; df = 9; P < 0.0001).
Fig. 1. Percentage mortality at 48 h post exposure of H. halys adults (black bars) and nymphs (gray bars)
exposed to topical sprays of insecticides for 1 hour. Bars represent means and vertical lines are standard errors.
Treatments differed significantly within each life stage (Kruskal - Wallis Analyses, P < 0.0001). Comparisons were
not made between life stages.
Insecticides producing the least mortality for P < 0.0001). Insecticides producing the least mor-
adults were neem oil, capsaicin, and spinosad and tality were capsaisin, spinosad, and essential oils
those producing the greatest mortality were car- and those producing the most mortality were car-
baryl, acetamiprid, and permethrin (Fig. 2). baryl, acetamiprid, and permethrin (Fig. 5). After
In the egg mortality trial, the average number 48 h of exposure, mortality of H. halys adults dif-
of eggs per egg mass was 26.7 ± 0.27 (SEM) and fered significantly among insecticidal treatments
did not differ among treatments (F 9,90 = 0.19, P (H = 60.7; df = 9; P < 0.0001) and, as with the 1 h
< 0.99). Mortality of eggs in response to topical exposure, permethrin produced the greatest lev-
applications differed significantly among treat- els of mortality (Fig. 5).
ments (H = 68.2; df = 9; P < 0.0001). Applications
of spinosad, permethrin, horticultural oil, and Adult Recovery Trials
capsaicin produced the least mortality and neem
oil, carbaryl, and acetamiprid produced the great- Exposure of adult H. halys to topical sprays of
est mortality (Fig. 3). permethrin resulted in an estimated mortality of
100 ± 0 (SEM)% at 24 h. However, at 96 h mor-
tality was 66.0 ± 7.3 (SEM)%. This reduction in
Dry Residue Trials
mortality was significant (T = 0; n = 10; P < 0.01).
Exposure to dry residues of permethrin resulted
Exposure to dry insecticide residues for 1 h
in mortality of 6.0 ± 3.1 (SEM)% after 24 h, but
resulted in significant mortality to nymphs (H =
at 96 h this increased significantly (T = 0; n = 10;
33.8; df = 9; P < 0.0001) and adults (H = 24.3; df
P < 0.01) to 38.0 ± 8.1 (SEM)%. Exposure to topi-
= 9; P < 0.004) (Fig. 4). Mortality of nymphs and
cal sprays and dry residues of acetamiprid did not
adults was the least when exposed to dry residues
result in differences in mortality between 24 and
of soap, horticultural oil, neem oil, and capsaicin.
96 h (P > 0.05), hence there was no indication of
The greatest mortality of nymphs was observed
recovery or increasing mortality following expo-
following exposure to dry residues of carbaryl,
sure to acetamiprid.
acetamiprid, and permethrin (Fig. 4), while only
permethrin produced high levels of mortality in
adults (Fig. 4). DISCUSSION
After 48 h of exposure, mortality of H. halys
nymphs to dry residues differed significantly The practical implication of these findings is
among insecticidal treatments (H = 43.0; df = 9; that several RTU products killed H. halys adults,
Fig. 2. Percentage mortality at 48 h post exposure of H. halys adults (black bars) and nymphs (gray bars) ex-
posed to topical sprays of insecticides for 48 h. Bars represent means and vertical lines are standard errors. Treat-
ments differed significantly within each life stage (Kruskal - Wallis Analyses, P < 0.0001). Comparisons were not
made between life stages.
nymphs, and eggs. In general, nymphs were more life stages, mortality in nymphs numerically ex-
sensitive than adults to both topical applications ceeded that of adults. This pattern has been ob-
of insecticides and their dry residues. In 34 of served in studies involving H. halys (Nielsen et al.
36 cases where insecticides were applied to both 2008b; Kuhar et al. 2012) and a variety of other
Fig. 3. Percentage mortality at 192 h post exposure of H. halys eggs exposed to topical sprays of insecticides.
Bars represent means and vertical lines are standard errors. Treatments differed significantly (Kruskal - Wallis
Analyses, P < 0.0001).
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Bergmann & Raupp: Ready to Use Insecticides against Halyomorpha halys 797
Fig. 4. Percentage mortality at 48 h post exposure of H. halys adults (black bars) and nymphs (gray bars)
exposed to dry residues of insecticides for 1 hour. Bars represent means and vertical lines are standard errors.
Treatments differed significantly within each life stage (Kruskal - Wallis Analyses, P < 0.0001). Comparisons were
not made between life stages.
Fig. 5. Percentage mortality at 48 h post exposure of H. halys adults (black bars) and nymphs (gray bars) ex-
posed to dry residues of insecticides for 48 h. Bars represent means and vertical lines are standard errors. Treat-
ments differed significantly within each life stage (Kruskal - Wallis Analyses, P < 0.01). Comparisons were not
made between life stages.
phytophagous pentatomids including C. hilare pers (Kuhar et al. 2012). Mortality of nymphs
Say, N. viridula L., and E. servus Say (Willrich et and eggs observed in trials reported here contrast
al. 2003). One unprecedented result of this study with those of Leskey et al. (2012b), who found
was the discovery of ovicidal activity of several high initial lethality of H. halys adults to residues
RTU products including carbaryl, neem oil, and of acetamiprid that declined dramatically over 7
acetamiprid. Our assessment of their efficacies d. This disparity could be attributed to the fact
as ovicides is based on the failure of nymphs to that exposure time of H. halys to pesticides used
hatch from eggs treated with these insecticides were 4.5 h in the laboratory (Leskey et al. 2012b)
rather than an observation that nymphs hatched and 24 h in the field (Leskey et al. 2013) whereas
and were subsequently exposed to insecticides exposure times to topical sprays and their resi-
and died. Isman (2006) noted the toxicity of neem dues in trials reported here were continuous and
oil to a wide variety of soft-bodied insects and at- lasted 48 h. Another potential limitation to the
tributed its activity to physical effects and disul- use of acetamiprid arises from the ability of stink
fides found in the oil. Davidson et al. (1991) and bugs to recover from exposure to this compound
Caldwell (2005) noted the ovicidal activity of oils (Leskey et al. 2012b). However, within 96 h no
against a wide range of insects and mites. Bográn evidence of this phenomenon was found in the
et al. (2006) list disruption of gas exchange and topical spray and dry residue trials reported here.
cell membrane structure and function as lethal A further limitation regarding the efficacy of
attributes of oil-bases insecticides. In addition acetamiprid comes from the work of Tillman &
to their physical properties, plant essential oils Mullinix (2004) who observed intermediate levels
are believed to have neurotoxic modes of action of mortality of E. servus nymphs (40%) and adults
including disruption of interference with neuro- (35%) exposed to residues of acetamiprid for 24
modulators and GABA-gated chloride channels h. Field evaluations by Greene & Capps (2002)
(Isman 2006). Other insecticides showing high and Ngo et al. (2002) for E. servus found minimal
levels of ovicidal activity were well-known nerve efficacy of acetamiprid applications. By contrast,
poisons that bind to nicotinergic receptors (acet- Rucker & Hamilton (2011) examined the effica-
amiprid) or inhibit acetylcholinesterase (carba- cies of acetamiprid and several other compounds
ryl). We do not know the mode of action of any of and found that acetamiprid alone or in combi-
these compounds as ovicides for eggs of H. halys nation with the growth regulator methoxyfeno-
and we suggest that this is a rich area for further zide reduced the amount of cat-facing on apples
study. caused by a complex of hemipterans consisting of
Topical applications and residues of the re- E. servus, E. tristigmus Say, C. hilare, H. halys,
duced risk insecticide spinosad demonstrated a and Lygus lineolaris Palisot de Beauvois. The
trend for increased mortality of nymphs, but less variability of responses to acetamiprid indicates
so for adults. These results contrast with those a strong need for further efficacy studies of this
of Kamminga et al. (2009) who found that adult compound for control of H. halys.
C. hilare, and E. servus tended to be more sus- Permethrin also dramatically increased mor-
ceptible to residues of spinosad than nymphs. tality relative to water of nymphs and adults, but
Lee et al. (in press) also found significant mortal- not eggs, as topical sprays and dry residues af-
ity of H. halys adults exposed to spinosad. Three ter exposure times of 1 and 48 h. These results
compounds, carbaryl, acetamiprid, and perme- are consistent with other laboratory assays that
thrin, exhibited relatively high levels of mortal- demonstrate high levels of mortality and lethality
ity. Carbaryl’s performance was best as a topical following the application of synthetic pyrethroids
spray increasing mortality in adults and nymphs. including permethrin (Nielsen et al. 2008b; Ku-
Residues of carbaryl were also effective in killing har 2012; Leskey et al. 2012b). Unlike a study by
nymphs. Dry residues of carbaryl showed little Leskey et al. (2012b) that demonstrated no de-
effect on adults, a result consistent with those of cline in efficacy of permethrin with time, the re-
Leskey et al. (2012b) who found the lethality of covery trial reported herein indicated a decrease
carbaryl residues to H. halys adults to be among in apparent mortality at 96 h compared with 24
the lowest of many compounds evaluated. h. Clearly, these results are suggestive of knock-
Acetamiprid elevated mortality of nymphs down recovery, and certainly deserve further at-
and adults relative to distilled water in topical tention.
spray trials at exposures of 48 h and to nymphs Neem oil and its active ingredient azadiractin
in residue trials of 48 and 1 h. Adults exposed to are insecticides popular amongst home vegetable
residues of acetamiprid for 1 or 48 h exhibited no growers and IPM practitioners (Isman 2006; Lee
greater mortality than adults exposed to distilled et al. in press). It is not surprising that topical
water controls. This result is consistent with the sprays of neem oil failed to increase mortality of
work of Kuhar et al. (2012) who found third instar H. halys adults as the clarified hydrophobic ex-
nymphs to be highly susceptible to acetamiprid tract of neem oil used in this study likely lacked
and adults less so. Acetamiprid provided moder- azadiractin. Related studies of neem products
ate levels of control in field trials involving pep- containing azadiractin also found a lack of signifi-
cant mortality in C. hilare or E. servus nymphs conducted under greenhouse and field conditions
and adults (Kamminga et al. 2009) and adults as efficacy under actual field conditions often lags
of H. halys (Lee et al. in press). However, results dramatically behind efficacy observed under labo-
of the topical neem oil spray, 1 h exposure with ratory conditions (Leskey et al. 2013).
second instar nymphs, demonstrated mortality
exceeding 80%. ACKNOWLEDGMENTS
The other botanically-based insecticides, cap-
saicin and a mixture of essential oils, produced We give special thanks to Paula Shrewsbury, Ryan
high levels of mortality as topical sprays to Wallace, Chris Riley, Caroline Brodo, Nancy Harding,
nymphs in 1 h exposure trials and slightly less so and Chris Sargent for their establishing and maintain-
in 48 h topical spray studies. Lee et al. (in press) ing the colony of H. halys. Three anonymous reviews
also reported activity of extracts of Eucalyptus sp. greatly improved the quality of this manuscript. This
against adult H. halys in a recent study of insecti- work was supported in part by USDA-NIFA SCRI #
2011-51181-30937 award and the Maryland Agricul-
cides used in the production of organic vegetables.
tural Experiment Station project #MD-ENTO-8732.
Horticultural oils and insecticidal soaps (po- Mention of trade names or commercial products in
tassium salts) are 2 groups of compounds often this publication are solely for the purpose of providing
recommended for use in vegetable gardens due to scientific information and do not imply recommenda-
their short period of residual activity, low mam- tion or endorsement by the institutions that employ
malian toxicity, and general compatibility with the authors.
integrated pest management programs (Davidson
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