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Research Article
Received: 15 January 2018 Revised: 7 July 2018 Accepted article published: 31 July 2018 Published online in Wiley Online Library:
(wileyonlinelibrary.com) DOI 10.1002/ps.5156
Successful management of Halyomorpha halys
(Hemiptera: Pentatomidae) in commercial
apple orchards with an attract-and-kill strategy
William R Morrison III,a* Brett R Blaauw,bBrent D Short,cAnne L Nielsen,d
James C Bergh,eGreg Krawczyk,fYong-Lak Park,gBryan Butler,h
Ashot Khrimianiand Tracy C Leskeyc
Abstract
BACKGROUND: Introduction of Halyomorpha halys (Stål) in the USA has disrupted many established integrated pest manage-
ment programs for specialty crops, especially apple. While current management heavily relies on insecticides, one potential
alternative tactic is attract-and-kill (AK), whereby large numbers of H. halys are attracted to and retained in a circumscribed area
using attractive semiochemicals and removed from the foraging population with an insecticide. The goal of this study was to
evaluate if AK implementation in commercial apple orchards can result in levels of H. halys damage that are equal to or less than
those from grower standard management programs.
RESULTS: Over 2 years at farms in five Mid-Atlantic USA states, we found that the use of AK resulted in 2–7 times less damage
compared with grower standard plots, depending on year and period. At selected trees on which AK was implemented, over
10,000 H. halys individuals were killed in two growing seasons, and the use of AK reduced the crop area treated with insecticide
against H. halys by 97%. Using AK had no impact on the natural enemy or secondary pest community over the same period.
CONCLUSIONS: Overall, the use of AK was effective at managing low to moderate H. halys populations in apple orchards, but
must be optimized to increase economic feasibility for grower adoption.
© 2018 Society of Chemical Industry
Supporting information may be found in the online version of this article.
Keyword s: behaviorally-based management; brownmarmorated stink bug; integrated pest management; pheromones; semiochemicals
1 INTRODUCTION
The unexpected introduction and establishment of a destructive
invasive pest species often forces researchers and growers to
rapidly develop alternative management tactics, as has been true
for the brown marmorated stink bug, Halyomorpha halys (Stål)
(Hemiptera: Pentatomidae). Halyomorpha halys were accidentally
imported from China1to the USA2in the late 1990s through four
separate events,3and it has spread to 44 USA states. It feeds on
>170 host plants, including many important food crops (www
.stopbmsb.org), and in 2010 its infestation of fruit and vegetables
reached outbreak status, causing about $37 million in damage
to USA Eastern apples.4Injury in apple usually consists of hard-
ened, inedible necrotic flesh (termed internal corking, hereafter),
with characteristic stylet penetration in the fruit, and discolored
dimpling at the site of feeding.5,6 Both adult and nymphal H.
halys inflict damage on tree fruits during the cropping period.6In
response, growers applied as much as four times more insecticide
to ameliorate this damage.7Since then, H. halys has become a
problem in Canada8and Europe,9with a projected global distribu-
tion to result in range expansion into many more locations.3,10–12
Since 2010, pheromone-based technology for H. halys has devel-
oped rapidly.13 Prior to 2012, large wooden pyramid traps14 baited
∗Correspondence to: WR Morrison III, Pest Management Science, USDA-ARS
Center for Grain and Animal Health Research, 1515 CollegeAvenue, Manhattan,
KS 66502, USA. E-mail: william.morrison@ars.usda.gov
aUSDA, Agricultural Research Service, Center for Animal Health and Grain
Research, Manhattan, KS, USA
bDepartment of Entomology, University of Georgia, Athens, GA, USA
cUSDA, Agricultural Research Service, Appalachian Fruit Research Station, Kear-
neysville, WV, USA
dDepartment of Entomology, Rutgers Agricultural Research and Extension Cen-
ter, Rutgers University, Bridgeton, NJ, USA
eVirginia Tech, Alson H. Smith, Jr. Agricultural Research and Extension Center,
Winchester, VA,USA
fDepartment of Entomology, Fruit Research and Extension Center,Pennsylvania
State University, Biglerville, PA,USA
gDivision of Plant & Soil Sciences, West VirginiaUniversity, Morgantown, WV, USA
hCarroll County Cooperative Extension, University of Maryland, Westminster,
MD, USA
iUSDA, Agricultural Research Service, Beltsville Agricultural Research Center,
Beltsville, MD, USA
Pest Manag Sci (2018) www.soci.org © 2018 Society of Chemical Industry
www.soci.org WR Morrison III et al.
with methyl (E,E,Z)-2,4,6-decatrienoate (MDT, hereafter) were used
to monitor H. halys populations. More recently, the male-produced
H. halys aggregation pheromone was identified as a mixture
of two stereoisomers of 10,11-epoxy-1-bisabolen-3-ol (aggrega-
tion pheromone, hereafter).15 When the aggregation pheromone
and MDT were combined in traps, a synergistic effect on field
attraction of H. halys adults and nymphs was observed.16 This
combination reliably captured all life stages and sexes of H.
halys throughout the growing season in the USA,17 Europe18,
and Asia.19
Halyomorpha halys often invades fields from wild hosts in
the landscape, and is usually most abundant along crop field
edges.20– 22 For example, H. halys densities were much greater
at the borders than the interior of peach orchards, with males
primarily driving this pattern.22 In apple, most injury was along
the edges of orchards in the Mid-Atlantic region of the USA.21
Rice et al.23 documented that forest shape and size in the
landscape surrounding commercial tomato fields significantly
influenced stink bug damage. As a result, monitoring for H.
halys is often along the edges of fields and orchards to intercept
the pest.
Alternative management tactics that exploit the
perimeter-driven behavior exhibited by H. halys have been investi-
gated. One such tactic uses weekly border insecticide applications
in peach orchards along with a suite of other integrated pest
management (IPM) tactics to reduce overall insecticide usage.24
Nielsen et al.25 demonstrated a differential attraction of H. halys
to various crops, particularly sorghum and sunflower. However,
trap cropping using a border of sunflower and sorghum,26,27
which have been shown to arrest H. halys movement into the
cash crop,28 was not successful at reducing damage to bell
peppers.
Pheromone-based technology is also being used for H. halys
management. For example, captures in pheromone-baited pyra-
mid traps on the exterior and interior of apple orchards have
been used to trigger alternate row middle (ARM) sprays over
2 weeks based on a cumulative provisional threshold.29 This can
reduce insecticide usage by 40% while maintaining crop quality.
Attract-and-kill (AK) involves attracting adults and nymphs to
a spatially circumscribed area and removing them via regular
pesticide applications. Morrison et al.30 evaluated the behavioral
basis of AK for H. halys in a research orchard and found: (i) a
pheromone dose-dependent increase in kill at baited trees, (ii)
minimal spillover of adults, nymphs, and damage into adjacent
trees, and (iii) a high, season-long average kill of adults at baited
trees. Indeed, over 25,000 H. halys adults were killed at six baited
trees with 1000 mg of H. halys aggregation pheromone over
a 6-day period.30 AK has been used to manage pests in other
systems, including Ceratitis capitata Wiedemann (Diptera: Tephri-
tidae) in citrus orchards in Spain,31 Rhagoletis pomonella (Walsh)
(Diptera: Tephritidae)32 and Conotrachelus nenuphar (Herbst)
(Coleoptera: Curculionidae)33 in northeastern USA apple orchards,
Rhynchophorus ferrugineus (Olivier) (Coleoptera: Curculionidae)
on date palm plantations in Saudi Arabia,34 and Phthorimaea
operculella (Zeller) (Lepidoptera: Gelechiidae) in potato fields in
Peru and Australia.35 These studies illustrate that AK can be used
successfully in a variety of systems, under different abiotic condi-
tions, and against a variety of taxa. The goal of the current study
was to demonstrate the effectiveness of AK in reducing H. halys
damage to levels that were equal to or less than grower standard
management programs in commercial apple orchards in five USA
Mid-Atlantic States.
Figure 1. Sampling schematic for a) attract-and-kill (AK) and b) grower
standard blocks on commercial farms in 2015– 2016. Schematic is repre-
sentative of key features, but not to scale.
2 MATERIALS AND METHODS
2.1 Study sites and sampling periods
This study included 10 commercial apple farms in five Mid-Atlantic
States in the USA (Table S1 in the supporting information, Fig. 1).
The farms included in this study were all commercial operations
ranging from low- to high-density plantings, and included a variety
of end uses, such as fresh market, processing, and pick-your-own
agritourism operations. The study was conducted from 1 June to
14 October 2015 and 6 June to 30 September 2016. Sampling in
these 2 years presented a test of AK under low population pressure
in 2015 and 2.5–27×higher population pressure in 2016 (Fig. 2,
Fig. 3).
2.2 Grower standard blocks
On each farm, one orchard was randomly assigned as the grower
standard (control) block and another as the attract-and-kill (AK,
treatment) block (Fig. 1). In the standard blocks, H. halys manage-
ment programs were solely determined by each grower. Manage-
ment of other orchard insects and diseases followed standard local
extension recommendations36 and were identical between the
standard and AK blocks within a farm.
2.3 Attract-and-kill blocks
In each AK block, AK sites were spaced every 50 m around
the perimeter of the orchard, except on the fourth internal
edge on farms in cases where orchards were bisected to cre-
ate two plots. At each AK site in an orchard, a tree was baited
with 840 mg of aggregation pheromone, which was distributed
on the perimeter-facing aspect of the tree as 20 high-dose
pheromone lures (42 mg per lure) of the stereoisomeric mix-
ture of cis-(7R)-10,11-epoxy-1-bisabolen-3-ols incorporated into
12 ×6.5 cm fiber pads (ChemTica, Inc., Heredia, Costa Rica).13,30 In
addition,eachbaitedtreehadonelurecontaining66mgofthe
pheromone synergist, MDT incorporated into a semi-permeable
sachet (AgBio, Inc., Westminster, CO, USA). The lures were covered
with 473-mL plastic cups (Dart Container Corps, Mason, MI) for
rain protection, and hung in the tree with twist ties. Both types
of lures were replaced every 4 weeks during the sampling period.
From the beginning of experimentation in June to the last fruit
harvest in September or October (depending on the field, grower,
and year), grower cooperators applied insecticide weekly to the
outward facing portion of the pheromone-baited tree and trees
within 5 m on either side, which together comprised each AK
wileyonlinelibrary.com/journal/ps © 2018 Society of Chemical Industry Pest Manag Sci (2018)
Attract-and-kill to manage H. halys www.soci.org
site. All seasonal insecticide programs followed legal regulations
(Table S2 in the supporting information).
2.4 Monitoring traps
In 2015 and 2016, three black pyramid traps (1.22 m tall; AgBio, Inc.,
Westminster, CO, USA) were deployed with a grey rubber septum
lure impregnated with 31 mg of crude murgantiol (aggregation
pheromone mimicking lure #11 in Leskey et al.37), containing
2mg and 3.2mg of (3S,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol
and (3R,6S,7R,10S)-10,11-epoxy-1-bisabolen-3-ol, respectively. A
separate lure containing 66 mg of MDT (AgBio, Inc.) was deployed
in the same traps. Along with the lures, a 5-cm kill strip con-
taining 10% 2,2-dichlorovinyl dimethyl phosphate (Vaportape
II, Hercon, Emigsville, PA) was also deployed in the collection jar
attheapexofthepyramidtraptoretaincapturedH. halys (see
Morrison et al. 201538 for physical specifications of the trap). The
aggregation pheromone and kill strips were changed at 2-week
intervals, and the MDT was replaced every 4 weeks. Traps were
positioned in a diagonal transect through the center of the block
and between apple trees in the rows, spaced approximately 50m
apart depending on block configuration, and checked weekly for
adults and nymphs. The season was divided into three periods:
early (initiation–30 June), mid (1 July–15 August), and harvest (16
August– 15 October). Traps were used to trigger two ARM sprays
to the whole block (one per week) if H. halys captures reached
or exceeded a cumulative threshold of 10 adults per trap, after
which the threshold was reset and insecticide applications to the
AK sites resumed.29
2.5 Fruit sampling
All apple cultivars selected for the study matured and were har-
vested from late September to early October to ensure that there
would be comparable levels of exposure to feeding by H. halys
in the AK and grower standard blocks. Three fruit samples were
collected during both growing seasons (5– 6-week intervals), in
mid-July, mid-August, and at harvest (September– October) (Table
S1 in the supporting information). The harvest sample was taken
when a majority of the cultivars were ripe and/or if more than
one block edge was to be fully harvested. For each sample,
fruit were collected from 16 interior and four perimeter trees,
with the perimeter trees at approximately 25 m away from a
pheromone-baited tree in the AK blocks. Initial placement of AK
sites was randomized at the beginning of each season, and sub-
sequently sampled thereafter through the season. In blocks that
were bisected to form a grower standardor AK block , a fourth edge
was lacking, and thus, only three perimeter trees were sampled for
fruit. For all blocks, interior samples were harvested from trees in
two intersecting perpendicular transects, with eight trees sampled
per transect, although this varied slightly by block configuration.
The initial selection of trees in a transect was randomized at the
beginning of a season, but in every case, trees were spaced to span
the interior of the block (approximately 10 m from the edge to the
center of the block; Fig. 1), with actual spacing depending on the
block size. These trees were flagged and subsequently sampled
in the early, mid, and harvest periods. Because of logistical con-
straints from commercial production in the orchards, it was impos-
sible to randomize the selection of trees between each sample, but
this method ensured that we had a representative sample of fruit
from the entire block. Ten random fruit per tree were harvested
from the mid- to upper-canopy, where damage is often most
severe,21 thus making fruit damage reduction estimates conserva-
tive. The proportion of injured fruit (frequency of damage) and the
Figure 2. Diagnostic pictures of H. halys feeding damage on apple, includ-
ing (A) discoloration of the flesh, (B) discolored dimpling, (C) internal cork-
ing (measured in this study), and (D) characteristic stylet penetration trail
into the apple’s flesh just below the surface of the skin.
Figure 3. Difference in H. halys population pressure between sampling
in 2015 and 2016 as measured by overall mean numbers of dead adults
on tarps beneath baited attract-and-kill trees on 3–4 commercial apple
orchards in the Mid-Atlantic region of the USA. Asterisks indicate significant
differences between years (t-test, 𝛼=0.05).
number of internal corking sites per fruit (severity of damage) was
recorded (see Fig. 2 for diagnostic injury pictures). Due to poor fruit
set in 2016, samples were only collected during harvest from two
farms, while three fruit samples were taken from all others.
2.6 Mortality of H. halys at attract-and-kill trees
To measure mortality of H. halys at baited AK trees, tarps were
secured beneath 5– 7 baited trees and compared with unbaited
trees in the standard block on 3– 4 farms across the same number
of states in the USA. Tarps in both treatments were placed on the
perimeter of blocks, with identical spacing, and number within
a farm. Tarps ranged in size from 2.1 ×3.0 to 3.7 ×4.3 m (W:L),
spanned the entire lower canopy of trees, and were checked
weekly for the number of H. halys adults and nymphs.
2.7 Natural enemy and secondary pest assessment
In 2015 and 2016, natural enemies were sampled using yellow
23 ×14 cm, back-folding sticky cards (Alpha Scents, Inc, West Linn,
Pest Manag Sci (2018) © 2018 Society of Chemical Industry wileyonlinelibrary.com/journal/ps
www.soci.org WR Morrison III et al.
OR,USA).Fourcards(twointheinteriorthirdandtwoonthe
exterior of the block) were deployed per block three times during
the season: 14–22 June, 6– 25 July, and 3– 26 August, depending
on the year and block. After 1 week, the cards were recovered and
held at −4∘C until they could be processed, when the number of
predators and parasitic wasps on each were recorded. All taxa pri-
marily classified as predators or parasitoids were counted, which
may have included each of the following depending on farm:
Anthocoridae, Asilidae, Bombyliidae, Cantharidae, Carabidae, Coc-
cinellidae, Geocoridae, Nabidae, Neuroptera (lacewings), parasitic
wasps (Parasitica), Pentatomidae (predatory), Reduviidae, Spheci-
dae, Staphylinidae, Syrphidae, Tachinidae, and Vespidae.
Mite sampling occurred in conjunction with the deployment
of sticky cards during the three periods described above. Five
leaves randomly collected from 10 trees per block at each farm
were brushed onto detergent-coated glass plates using standard
mite brushing machines in the laboratory. The following herbivo-
rous and predatory mite species were recorded: Panonychus ulmi
(Koch), Tetranychus urticae Koch, Zetzellia mali (Ewing), Neoseiulus
fallacis (Garman), and other phytoseiid mites.
2.8 Economic analysis of attract-and-kill technology
Asubsetofthreefarms(onefromMD,WVandVA)werechosen
for cost analysis to compare AK and grower standard programs
for insect management. The categories chosen for analysis were:
insecticide cost per ha (Table S3 in the supporting information),
cost of lures for baited trees, cost of labor to deploy and replace
lures on baited trees, crop loss adjusted for bushels harvested per
ha (whole plot and processing loss), and profits based on yield for
each experimental plot. At the time of this study, experimental
lures cost $5 per high-dose H. halys aggregation pheromone
lure, and $4.75 per 66 mg MDT lure. In this economic analysis,
apple downgrade to processing was calculated at an 80% loss in
value. Expenses not included were fuel and labor for insecticide
application, fruit loss on pheromone-baited trees, and monitoring
trap expenses (as trap expenses were identical between the AK and
grower standard blocks). Labor to deploy the lures was calculated
at $12/h ×1h×4 changes. Data were computed separately for
each year and farm and then averaged across farms within a year.
The cost of a bushel of apples was priced at $20 for all farms as
a fresh market standard in the Mid-Atlantic, USA.39 Whole plot
applications of insecticides were standardized at 378.5 L of water
per 0.405 ha. For the AK tree insecticide applications, the estimated
spray volume was conservatively calculated at 37.9 L per plot for all
farms as tree size and number of baited trees varied.
2.9 Statistical analysis
Pyramid trap data were analyzed separately by year with a lin-
ear mixed model. The number of adults or nymphs per trap was
used as the response in the model, with treatment (AK and grower
standard) and sampling period (early, mid, and harvest) as fixed
explanatory variables. The interaction between treatment and
sampling period was also included in the model. Orchard site was
used as a random blocking variable. Date was used as a repeated
measure in the analysis, with a first-order autoregressive corre-
lation/covariance matrix. Because data did not conform to the
assumptions of a normal distribution upon inspection of resid-
uals, they were log-transformed, after which assumptions were
fulfilled. Upon a significant result from the overall model, Tukey’s
HSD was used for pairwise comparisons. This same procedure
was used to analyze the mortality of H. halys adults and nymphs
that were killed on tarps, except for nymphs in 2015, which were
inverse-transformed instead of log-transformed.
The proportion of injured fruit per tree was analyzed separately
each year with a generalized linear mixed model. The model
structure was the same as above for the severity of damage.
However, because initial analysis revealed that overdispersion was
a problem with the model, a quasi-binomial distribution was used
to model the data which corrects for this issue.40 Likelihood ratio
tests based on a 𝜒2-distribution were used to test the significance
of the variables in the model. Post-hoc pairwise comparisons were
performed with 𝜒2-tests using a Bonferroni correction.
The severity of damage from the fruit sampling was analyzed
separately for each year using a linear mixed model. The num-
ber of internal corking sites per fruit was used as the response
variable, with the treatment, sampling period, and location of
the tree (perimeter or interior) as fixed explanatory variables. The
second-order and third-order interactions were also included in
the model. The field site was coded as a random blocking variable.
Upon inspection of the residuals, the data were log-transformed
to correct deviations from normality. Upon a significant result from
the model, Tukey’s HSD was used for pairwise comparisons.
Predators and parasitoids recorded from sticky traps were ana-
lyzed separately. A linear mixed model was used to analyze each
response variable in each year, particularly using treatment and
sampling period as fixed, explanatory variables. The two-way inter-
action between these variables was also included. Field site was
used as a random, blocking variable. Upon inspection of the resid-
uals, the data were log-transformed to correct deviations from
normality. Upon a significant result from the model, Tukey’s HSD
was used for pairwise comparisons. The same procedure was used
to analyze the mite data, using herbivorous mite species as one
response variable, and predatory mite species as another response
variable. For this and all other statistical analyses, R software41 was
used with 𝛼=0.05.
3RESULTS
3.1 Monitoring traps
In 2015, there was no significant difference between the treat-
ments in the mean number of adults captured (F1,49 =3.74;
P=0.053; Fig. 4(a)) but captures varied significantly by sampling
period (F2,274 =27.5; P<0.0001; Fig. 4(a)). In particular, there
were 7 and 10 times more adults captured in the harvest period,
compared with the early or mid-period, respectively. There was
no significant period by treatment interaction (F2,274 =2.59;
P=0.075). Nymphs were not consistently recorded across all
blocks in 2015, and are thus not reported. Across all plots in 2015,
threshold was reached a total of 16 times in grower standard
plots, while it was only reached seven times in AK plots, which was
significantly less (𝜒2=3.62; df =1; P<0.05).
In 2016, there was no significant difference between the treat-
ments in the mean number of adults captured (F1,49 =1.45;
P=0.229; Fig. 4(b)), but the period during which traps were
deployed affected captures significantly (F2,274 =223.8; P<0.0001;
Fig. 4(b)). Specifically, approximately five and 12 times more
adults were captured in the harvest period compared with the
early and mid-period, respectively. The interaction between
sampling period and treatment was significant (F2,274 =3.55;
P<0.05). Similar to adults, treatment did not significantly affect
captures of nymphs (F1,49 =0.891; P=0.345), although there
was a significant effect of sampling period on nymphal cap-
tures (F2,274 =367.3; P<0.0001). Approximately 180 and four
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Attract-and-kill to manage H. halys www.soci.org
Figure 4. Mean adult H. halys captured in monitoring pyramid traps located
in each block on 10 farms in five Mid-Atlantic states in the USA from 11
May to 14 October 2015 (a) and 31 May to 11 October 2016 (b). Letters
represent comparisons within life stages. Bars with shared letters were
not significantly different from each other (Tukey’s HSD, 𝛼=0.05). Nymphs
were not displayed in 2015, because they were only counted at a subset of
orchards. AK =attract-and-kill block, Control =grower standard block.
times more nymphs were captured during the harvest period
than either the early or mid-periods, respectively. There was a
significant interaction between treatment and sampling period
(F2,274 =124.4; P<0.0001), with over two times more nymphs
captured in grower standard blocks than in AK blocks in the mid-
and harvest period, but not in the early period. Across all plots in
2016, there was not a significant difference in the number of times
thresholdwasreachedinAKplots(18times)comparedtogrower
standard plots (19 times; 𝜒2=0.027; df =1; P=0.87).
3.2 Proportion of injured fruit
Treatment significantly affected the proportion of injured fruit
(𝜒2=4.43; df =1; P<0.04; Fig. 5(a)), almost halving the propor-
tion of fruit damaged per tree in the AK blocks compared with
the grower standard. Tree location influenced the proportion of
damage (𝜒2=13.5; df =1; P<0.001), with 1.6 times more dam-
age on trees on the perimeter of blocks. Sampling period also
significantly affected the proportion of fruit damage (𝜒2=84.6;
df =2; P<0.0001); damage was three times more frequent on
trees sampled in the mid- and harvest period compared with the
early period. The two-way interactions involving treatment were
not significant by location (𝜒2=0.01; df =1; P=0.914) or period
(𝜒2=1.55; df =2; P=0.462). The two-way interaction between
location and period was significant (𝜒2=11.0; df =2; P<0.01), as
was the three-way interaction among all the variables (𝜒2=7.70;
df =4; P<0.03).
Likewise, in 2016, the proportion of fruit damage on trees
depended on the treatment (𝜒2=9.12; df =1; P<0.01; Fig. 5(b));
on average, there was almost half as much damage on trees in the
Figure 5. Proportion of injured fruit per tree in the early (13 July to 15 July;
top panels), mid- (25 August to 2 September; middle panels), and harvest
period (17 September to 1 October; bottom panels) at 10 commercial apple
orchards in five Mid-Atlantic States of the USA in 2015 (a) and 2016 (b) for
attract-and-kill managed blocks (red) and grower standard blocks (black).
Bars with shared letters were not significantly different from each other
(𝜒2-test with Bonferroni correction).
AK blocks compared with the grower standard block. Tree location
also significantly influenced the proportion of damage (𝜒2=4.22;
df =1; P<0.05), with 1.5 times more frequent damage on perime-
ter than interior trees. The period during which the tree was sam-
pled also affected the proportion of fruit damage (𝜒2=119.5;
df =2; P<0.0001; Fig. 5(b)), with three and four times more dam-
age in the mid- and harvest period, respectively, compared with
the early period. None of the two-way interactions were significant
(treatment ×location: 𝜒2=0.426; df =1; P=0.514; treatment ×
period: 𝜒2=5.93; df =2; P=0.052; location ×period: 𝜒2=0.5.83;
df =2; P=0.054). The three-way interaction among each of the
variables was also not significant (𝜒2=1.26; df =2; P=0.533).
3.3 Fruit damage severity
A similar pattern was detected with the severity of damage found
on trees. In 2015, a total of 9990 fruit were harvested over the
course of the experiment. Importantly, the treatment signifi-
cantly affected the severity of damage on fruit (F1,398 =408.1;
P<0.0001; Fig. 6(a)); overall, less than half the number of inter-
nal corking sites were recorded on fruit collected from the AK
block compared with the grower standard block. Tree location
also significantly influenced damage severity (F1,398 =663.8;
P<0.0001), with almost twice as much damage on perimeter
trees compared with interior trees. Additionally, sampling period
also significantly influenced fruit damage severity (F2,398 =4421;
P<0.0001); there were over four times more internal corking
sites during the harvest compared with the early period. There
was a significant two-way interaction between treatment and
tree location (F1,398 =739.1; P<0.0001), treatment and sampling
period (F2,398 =1572; P<0.0001), and location and sampling
Pest Manag Sci (2018) © 2018 Society of Chemical Industry wileyonlinelibrary.com/journal/ps
www.soci.org WR Morrison III et al.
Figure 6. Severity of internal damage per fruit in the early (13 July to
15 July; top panels), mid- (25 August to 2 September; middle panels),
and harvest period (17 September to 1 October; bottom panels) at 10
commercial apple orchards in five Mid-Atlantic States of the USA in 2015
(a) and 2016 (b) for attract-and-kill managed blocks (red) and for grower
managed blocks (black). Bars with shared letters were not significantly
different from each other (Tukey’s HSD, 𝛼=0.05).
period (F2,398 =121.1; P<0.0001). Finally, there was also a signif-
icant three-way interaction among the variables (F4,398 =1618;
P<0.0001).
In 2016, a total of 9240 fruit were collected during the experi-
ment. As in 2015, the treatment significantly affected fruit damage
severity (F1,400 =770.0; P<0.0001; Fig. 6(b)), reducing the num-
ber of internal corking sites by 2.5 times on fruit collected from
the AK blocks compared with the grower standard control. More-
over, tree location affected the damage severity (F1,400 =14.8;
P<0.001), with 1.7 times more damage on fruit collected from
the perimeter than the interior of the orchard. Furthermore, the
sampling period significantly influenced the amount of dam-
age present (F2,400 =3192; P<0.0001). Specifically, there was over
seven times more damage on fruit in the harvest period compared
with the early period. All two-way interactions were significant,
for example treatment ×location (F1,400 =628.5; P<0.0001), treat-
ment ×period (F2,400 =196.2; P<0.0001), and location ×period
(F2,400 =185.5; P<0.0001), as well as the three-way interaction
among all variables (F4,400 =1072; P<0.0001).
3.4 Mortality of H. halys at baited attract-and-kill trees
In 2015 and 2016, 99.6% and 99.9% of the dead H. halys adults,
respectively, were from tarps beneath baited AK trees. Not sur-
prisingly, treatment had a significant influence on the mortal-
ity of adults in both 2015 (F1,45 =33.9; P<0.0001; Fig. 7(a)) and
2016 (F1,40 =16.2; P<0.0001; Fig. 7(b)), with 113 and 1630 times
more adults killed on AK trees than grower standard trees, respec-
tively. In addition, the number of adults recovered on tarps dif-
fered by sampling period in 2015 (F2,523 =32.2; P<0.0001) and
2016 (F2,576 =147.0; P<0.0001; Fig. 7). Over five and 15 times
more adults were killed in the 2015 harvest period compared with
Figure 7. Mean number of dead H. halys adult (black) and nymphs (grey)
collected on tarps in the early (top panel), mid- (middle panel), and harvest
period (bottom pa nel) at 3 commercial apple orchard s in three Mid-Atlantic
States of the USA deployed from 3 June to 21 September 2015 (a) and
6 June to 21 September 2016 (b) for attract-and-kill managed blocks
and for grower managed blocks. Letters represent pairwise comparisons
within each life stage, and bars with shared letters are not significantly
different from each other (Tukey’s HSD, 𝛼=0.05). AK, attract-and-kill; Con-
trol, grower standard block.
the early and mid-period, respectively, while seven and 14 times
more adults were killed in the 2016 harvest period compared with
the same two periods. There was a significant treatment ×sam-
pling period interaction in 2015 (F1,523 =15.2; P<0.0001) and 2016
(F1,576 =30.0; P<0.0001). There were 216 and 1988 times more
adults killed on AK trees in the 2015 and 2016 harvest period,
respectively, compared to grower standard trees.
In 2015 and 2016, 98.3% and 99.7% of the dead H. halys nymphs
were found on baited AK trees, respectively. Treatment signifi-
cantly influenced the mortality of nymphs in 2015 (F1,45 =1497;
P<0.0001; Fig. 7(a)) and 2016 (F1,40 =158.8; P<0.0001; Fig. 7(b)),
with 60 and 290 times more nymphs killed on AK trees than grower
standard trees in 2015 and 2016, respectively. The sampling period
also significantly affected mortality of nymphs on trees in 2015
(F2,523 =1524; P<0.0001) and 2016 (F1,576 =153.1; P<0.0001),
with 15 and 10 times more nymphs killed in the harvest period
compared to the mid-period, respectively. There was a signifi-
cant interaction between treatment and sampling period in 2015
(F1,523 =9474; P<0.0001) and 2016 (F1,576 =52.5; P<0.0001). In
particular, while mortality during the early season was statistically
equivalent between the treatments, not a single nymph was killed
in the control treatment under grower standard trees in the mid-
and harvest period.
3.5 Natural enemy assessment
An average of 9.7 ±1.6 (mean ±SE) and 11.3 ±1.3 predators and
parasitic wasps, respectively, were captured on yellow sticky cards
in AK blocks, while there were 9.5 ±1.1 and 11.2 ±1.7 in grower
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Table 1. Summary of costs for external inputs in US Dollars for 2015–2016 studies of commercial implementation of attract-and-kill compared to
grower standard practices
Grower standard Attract-and-kill
Farm WB sp rayaTotal WB sprayaBorder spray AgBio luresaLure labor Total
2015
MD 865 865 390 44 4646 119 5199
VA 489 489 667 59 6019 119 6865
WV 1077 1077 625 49 5674 119 6467
Mean 811 811 561 52 5446 119 6178
2016
MD 195 195 114 25 4646 119 4903
VA 324 324 376 32 6019 119 6546
WV 902 902 833 35 2716 119 3702
Mean 474 474 440 30 4460 119 5048
aSeason totals on a per ha basis.
WB, whole block.
standard blocks, respectively. Treatment did not significantly affect
the abundance of predators (ANOVA: F1,230 =0.239; P=0.626) or
parasitic Hymenoptera (F1,230 =0.756; P=0.387) on sticky cards.
However, deployment period did significantly affect the abun-
dance of predators (F2,230 =22.3; P<0.0001) and parasitic wasps
(F2,230 =16.5; P<0.0001). In particular, there were twice as many
predators and parasitic wasps in the early season compared with
the late season, in both treatments. There was a significant inter-
action between treatment and period for predators (F2,230 =4.10;
P<0.05), but not parasitic wasps (F2,230 =1.08; P<0.345).
In 2016, an average of 8.1 ±1.2 (mean ±SE) and 13.3 ±1.3
predators and parasitic wasps, respectively, were recorded from
yellow sticky cards in the AK blocks compared with 8.3 ±1.8 and
14.9 ±2.0 in the grower standard blocks. Similar to 2015, the treat-
ment did not significantly influence the abundance of predators
(ANOVA: F1,186 =2.08; P=0.157) or parasitic wasps (F1,186 =2.79;
P=0.098) captured. In contrast to the prior year, the deployment
period affected captures of predators (F2,186 =10.6; P<0.0001),
but not parasitic wasps (F2,186 =1.75; P=0.179). There was no sig-
nificant interaction between treatment and deployment period
for either predators (F2,186 =2.40; P=0.096) or parasitic wasps
(F2,186 =2.19; P=0.117).
3.6 Secondary pest assessment
Treatment had no effect on the numbers of herbivorous mites
(ANOVA: F1,154 =0.007; P=0.933), nor did the sampling period
(F2,154 =1.62; P=0.202). There was no treatment ×sampling
period interaction (F2,154 =0.118; P=0.889). Likewise, the treat-
ment did not significantly influence the number of predatory mites
(ANOVA: F1,154 =0.683; P=0.410), nor did the sampling period
(F2,154 =2.76; P=0.066). The interaction between the two vari-
ables was not significant (F2,154 =0.005; P=0.995).
Similar to 2015, neither the presence of AK (ANOVA:
F1,156 =0.489; P=0.486) nor the sampling period (F2,156 =1.25;
P=0.290) affected the number of herbivorous mites present in
2016. The interaction between treatment and sampling period
was not significant (F2,156 =1.56; P=0.215). Treatment had
no significant influence on the abundance of predatory mites
(ANOVA: F1,156 =0.319; P=0.574). However, sampling period sig-
nificantly affected the abundance of predatory mites (F2,156 =16.0;
P<0.0001) in 2016, with 33 times more mites at harvest compared
with the early period. The interaction between treatment and
sampling period was not significant (F2,156 =0.126; P=0.882).
3.7 Economic analysis of attract-and-kill technology
In 2015, AK was over seven times more expensive than grower
standard practices across the three Mid-Atlantic farms, with lures
making up 88% of the cost of the AK treatment (Table 1). Using
the AK strategy decreased monetary crop losses by almost 30%
in 2015 compared with grower standard practices, translating to
$1545–$1933 in additional value of the crop based on processing
and whole crop loss, respectively (Table 2). Moreover, the use
of AK resulted in $2685 greater value in yield over the grower
standard treatment (Table 2). However, when the additional cost
of experimental AK was included, on average growers would have
paid an additional $2555 to use AK over standard practices in 2015,
which represented 133% the cost of the grower standard program
(Table 3).
In 2016, total cost for the lures in the AK treatment decreased by
approximately $450 because of fewer baited trees, but the treat-
ment blocks were still over 10 times more expensive than the
cost of grower standard tactics (Table 1). The use of AK decreased
monetary crop losses by 16% in 2016, resulting in $779–$971 in
additional revenue for growers based on processing loss or whole
plot loss, respectively (Table 2). Because 2016 was a higher popu-
lation year for H. halys, growers only gained an average of $495 in
increased yield in the AK compared with the grower standard plots
(Table 3). Again, when the cost of each pest management strategy
was included, growers paid $2446 more to use AK, an increase of
140% over the price of grower standard practices (Table 3).
4 DISCUSSION
We have demonstrated that AK can be used to manage H. halys
in commercial apple orchards with equivalent or, in many cases,
superior control to standard grower practices. At harvest in both
years, the proportion of injured fruit was equivalent or reduced by
half on interior trees in AK compared with grower standard blocks.
By the mid- and harvest period, use of AK in both years reduced
the severity of fruit damage on interior trees by half to a third
compared with the grower standard blocks. Importantly, even in a
year with higher pest pressure (e.g. 2016, Fig. 3), with almost three
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www.soci.org WR Morrison III et al.
Table 2. Gross monetary losses and profits (in US Dollars) experienced by three farms in MD, VA, and WV as a result of crop damage and sales based
on yield from 2015 to 2016
Grower standard Attract-and-kill
Farm
Whole bushels
lossa,b
Processing
bushels lossb, c Plot profitsd
Whole bushels
lossb
Processing
bushels lossb, c Plot profitsd
2015
MD NA NA 33 393 NA NA 41 185
VA 5847 4678 11 794 6027 4821 19 137
WV 8310 6647 112 310 4268 3415 103 281
Mean 7080 5664 52 499 5147 4119 54 534
2016
MD NA NA 33 393 NA NA 41 185
VA 7206 5765 5414 5597 4478 26 078
WV 4838 3870 111 197 4505 3603 30 888
Mean 6022 4819 50 001 5051 4040 32 717
aAll losses are season totals on a per ha basis.
bNote: Because grower standard blocks and attract-and-kill blocks were of different sizes within a farm except for MD, the bushels for the larger field
was adjusted down to the equivalent bushels of the smaller field for fair comparisons between treatments.
cProcessing losses are discounted at an assumed 80% rate compared to whole block losses.
dWhole plot profits based on bushels produced per ha assuming a price of US $20 per bushel for fresh market and are expressed on a per ha basis.
Table 3. Summary of total monetary losses (US Dollars) experienced
by growers in MD, VA, and WV from 2015 to 2016, including additional
expenses as a result of treatments
Grower standard Attract-and-kill
Farm
Whole
lossa
Processing
loss
Whole
loss
Processing
loss
2015
MD 7537 6202 7299 6879
VA 6336 5167 12 891 11 686
WV 9388 7725 10 734 9882
Mean 7754 6365 10 309 9481
2016
MD 5137 4149 5397 5298
VA 7529 6089 12 143 11 023
WV 5740 4772 8206 7304
Mean 6136 5004 8582 7875
aEach of the values represent the total adjusted loss on a per ha basis.
times more H. halys than in 2015, AK adequately managed H. halys
populations. Prior research has demonstrated that a trap-based
threshold for H. halys can be used to manage the pest in apple.29
We have expanded the utility of the pheromone by demonstrating
that its direct use on an attractive host, in combination with a
killing agent, was effective at managing H. halys under low to
moderate population pressure in commercial apple orchards. As
a consequence, AK appears to be a promising technique, but
requires some refinement.
It is important to consider economic feasibility, which is a signifi-
cant drawback to this approach. In the economic analysis, we only
consider direct, in-season, and up-front costs, but do not include
equipment depreciation, land value changes, and other assorted
long-term costs. The cost for lures ranged between $2716– $6019
per ha and season, which exceeded the costs for the total stan-
dard spray program ($195– $1077 ha−1). On the other hand, there
was less damage in AK plots, which translated to 16– 30% greater
revenue for growersthan standard management techniques. How-
ever, this was not enough to offset the additional costs of lures
in AK. If one looks only at lowering the lure cost to negate the
monetary difference between the grower standard and AK blocks,
the price of the lures would need to drop from $5446 to $2552
(based on whole block losses) or $3120 (processing block losses)
per ha to equal standard apple production costs. Given the same
number of lures, lure changes, and number of AK sites per ha,
and loading of pheromone per lure, the lures would need to cost
approximately USD $3.79– $4.64 to be competitive against a tra-
ditional grower program. It should be noted that another option
for growers to increase fruit quality would be to apply additional,
well-timed insecticide sprays (each about $20/acre), which may be
a more economical route. According to Short et al.29 six well-timed
insecticide sprays, costing about $120 in total, controlled H. halys
damage in Mid-Atlantic orchards, and this represents a price tar-
get for AK lures to become competitive with grower standard pro-
grams. The costs represented in this paper were for experimen-
tal, special order lures that were not commercially available. Since
then, new synthetic pathways for producing these pheromones
have become available and more companies are producing them.
It is expected that lure price will continue to drop as synthetic path-
ways are optimized and more companies begin selling their own
products. Other measures may further optimize AK and improve
its economic viability. Ultimately, the plume reach of the H. halys
pheromone will determine how many AK sites would be needed
per block,42 which may allow for changes to the spacing of AK
sites and thereby decrease the amount of pheromone used in the
block. AK was deployed early in the season (in early June), but
because H. halys populations are usually very low at that time,39
it may be possible to delay deploying AK until later in the season,
potentially cutting lure costs by two thirds. In addition, whereas
we used 840 mg of H. halys pheromone per baited tree, it may
be that AK efficacy can be maintained by using less pheromone
per tree, thereby further reducing costs. Moreover, formulation
changes may result in season-long lure attractiveness (Leskey and
Short, unpublished), thus eliminating the need to replace lures and
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Attract-and-kill to manage H. halys www.soci.org
reducing the number of lures required annually.While the distance
of attraction to these semiochemicals is currently unknown,35 AK
may also act in areawide suppression of H. halys, locally depleting
individuals on a farm, which may increase the economic viability
of this approach. For example, a 40km2comprehensive areaw-
ide pest management program with at least one AK trap per km
yielded 91% and 61% reductions in fruit infestation in Hawaii by
Ceratitis capitata and Bactrocera dorsalis (Hendel), respectively.43
Finally, it may be possible to use AK when it is most needed, per-
haps in combination with trap-based thresholds. Hypothetically,
this approach would use a sprayable pheromone formulation that
could be tank-mixed with an insecticide and that gradually dissi-
pates as the insecticide loses efficacy, thereby creating temporary
AK sites (Leskey and Short, unpublished).
Trap cropping shares some similarities with AK, including requir-
ing that pest insects be retained in a spatially circumscribed area
and/or be removed from the foraging population to protect a
cash crop. Tillman and Cottrell44 used pheromone-baited traps
in combination with a sorghum trap crop to prevent the disper-
sal of Euschistus servus (Say) (Hemiptera: Pentatomidae) into cot-
ton, and found that this successfully prevented emigration from
sorghum. Researchers have found that a sorghum and sunflower
trap crop for H. halys (without supplemental pheromone) was
not effective at reducing injury under high population pressure.27
Blaauw et al.28 found that while H. halys was initially retained by
the same trap crop, adults ultimately dispersed to the cash crop in
the absence of other management tactics, but retention may be
improved with supplemental pheromone.30 Morrison et al.45 also
found that aggregation pheromone was a more important deter-
minant for retention than host stimuli, thus suggesting that inclu-
sion of pheromone, in addition to an attractive host, is pivotal for
retention and adequate management of H. halys. Here, we have
shown through the observation of H. halys on tarps that we can
manipulate the pest population in the AK block compared with
the grower standard, and concentrate individuals to a few select
baited apple trees in the orchard. We have demonstrated that we
can attract H. halys to a host and retain them long enough to be
killed.
In this study, we found significantly greater severity and pro-
portion of injured fruit collected from trees on the perimeter of
blocks, regardless of treatment, further supporting the hypothesis
of H. halys as a perimeter-driven pest.20 –22 As a result, special con-
sideration for orchard borders seems justified when considering
management for this species. We achieved damage suppression
on perimeter and interior trees using a perimeter-based AK tactic
compared with conventional grower methods. At a select number
of AK-baited trees over 2 years, over 10,000 H.halys were killed. This
translates to an average of 582 adults and 138 nymphs killed per
AK tree over a 5-month period. Presumably, AK sites intercepted H.
halys adults and nymphs at the border of apple blocks and retained
them long enough for exposure to a lethal dose of insecticide,
allaying concerns of sublethal exposure to killing agents.46,47 Other
perimeter-based methods, such as border sprays, have also been
successful for managing H. halys in peaches24 and soybean.48
Unexpectedly, use of AK over two seasons neither increased
natural enemy nor decreased secondary pest abundance. There
are multiple putative explanations for this pattern. For example,
AK may need to be implemented over a longer period before
improvements to the natural enemy community can be observed.
Because natural enemies are highly mobile, it may be possible
that more AK blocks in an area would be needed to reap the
benefits of decreased insecticide usage and increased refuges.
Indeed, prior work has shown that natural enemies, such as lady
beetles, responded to landscape features out to 1.5 km around
a focal field.49 In addition, even though sprays targeting H. halys
were reduced via AK, insecticides for other pests in these orchards
may have affected the natural enemy community. It is possible
that spraying the borders of the orchard resulted in an effective
barrier to the immigration of natural enemies into the AK blocks.
However, because only 20% of the border was sprayed in AK
blocks, compared with 100% of the border in the grower standard
blocks whenever sprays were applied, and because prior work
using weekly border sprays on the perimeter of peach orchards
found no harm to the natural community,24 this seems unlikely.
Nonetheless, the long-term effect of AK and other insecticide
reduction measures, including sprays triggered by trap-based
thresholds (either on the border or full block), on the natural
enemy community is worthy of further consideration.
For growers with large acreage, AK, as evaluated in this study,
may not be feasible because of the prescribed weekly spray sched-
ule and their need to manage diseases regularly. However, the
need to spray pheromone-baited trees may be ameliorated by
combining pheromone lures with long-lasting insecticide netting
as the killing mechanism50, by relocating such AK sites to locations
outside the orchard, or by using trunk injections of systemic insec-
ticides to kill adult BMSB at baited AK trees without needing to
spray, similar to what is done with emerald ash borer, Agrilus pla-
nipennis Fairmaire (Coleoptera: Buprestidae).51 Such an approach
would decrease the need for frequent sprays and replace it with a
killing mechanism that has demonstrated effectiveness for poten-
tially the whole growing season. Sprays could also be decreased by
linking AK to thresholds based on the pyramid monitoring traps,
which have been shown to be effective on their own and which
have sparked widespread grower interest and acceptance.
The commercial farms in our study ran through the spectrum
of available horticultural and cultural practices in the Mid-Atlantic
region, ensuring that our study is representative of apple produc-
tion in the eastern US. In our study, we had apples under high and
low density plantings, and apples destined for processing, fresh
market, and U-Pick/agritourism endpoints. Some of the orchards
in this study used trellises, while others did not. Sometimes blocks
contained multiple cultivars, and more rarely they were a single
cultivar. In every case, we selected blocks that had similar har-
vest dates ranging from late September to early October so that
damage measurements were comparable. Moreover, prior work
has demonstrated that there may be similar damage among apple
cultivars52,andH. halys abundance on apple cultivars is more sim-
ilar to each other than abundance of conspecifics on other plant
species.53 Similarly, other work has found that the H. halys aggre-
gation pheromone is more important than tree fruit volatiles in
recruiting and retaining conspecifics.45 Despite this great diversity
in cultural practices, markets, and apple cultivars among farms, it
is clear that AK managed H. halys populations as well if not orders
of magnitude better than grower standard practices within each
farm in 2015 and 2016 (e.g. Figs S1 and S2 in the supporting infor-
mation). In fact, in 36 possible comparisons between AK blocks and
grower standard blocks for frequency of damage at each of the
farms, the AK blocks performed equally or better than the grower
standard in 92% of the cases over both years. This suggests that the
success of AK is robust across commercial horticultural practices.
Overall, we have documented the novel use of pheromone tech-
nology in commercial apple orchards in the Mid-Atlantic region of
the USA, one of the regions impacted most severely by the invasive
H. halys.Wehavedemonstratedthatweareabletoreduceboth
Pest Manag Sci (2018) © 2018 Society of Chemical Industry wileyonlinelibrary.com/journal/ps
www.soci.org WR Morrison III et al.
the proportion and severity of injured fruit under differing popu-
lation intensity, while reducing the amount of area sprayed for H.
halys by 97%. However, the exact deployment methods, amount
of pheromone, distance among AK sites, and other considerations
need to be optimized to improve the economic viability of AK
compared with conventional management. Nonetheless, because
other studies have documented that pheromone-based tools are
effective at monitoring H. halys in other regions of the world
beyond the USA, for example in Asia19 and Europe18, it is likely that
AK tactics developed here could be adapted and adopted in other
circumstances to manage this invasive species.
ACKNOWLEDGEMENTS
We thank McKenzie Allen (USDA), Samuel Brandt (USDA), Lee
Carper (USDA), John Cullum (USDA), Morgan Douglas (USDA),
Nicole Halbrendt (PSU FREC), Chris Hott (USDA), Marcelo Zanelato
Nunes (PSU FREC), Britany Poling (NDSU), Ann Rucker (Rutgers),
Tony Rugh (USDA), Nick Serata (Rutgers), and Lauran Shaak (PSU
FREC) for their excellent technical assistance. This work was funded
by Northeast SARE Grant#LNE14-334. We would like to generously
thank our cooperating growers for allowing us to conduct this
research on their farm, including those from Maryland, New Jersey,
Pennsylvania, Virginia, and West Virginia. The use of trade names is
for the purposes of providing scientific information only, and does
not constitute endorsement by the United States Department of
Agriculture. The USDA is an equal opportunity employer.
SUPPORTING INFORMATION
Supporting information may be found in the online version of this
article.
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